ORIGINAL RESEARCH ARTICLE

published: 31 August 2012

doi: 10.3389/fpsyg.2012.00303

From emotions to consciousness – a neuro-phenomenal

and neuro-relational approach
Georg Northoff *
Mind, Brain Imaging and Neuroethics Research Unit, Institute of Mental Health Research, University of Ottawa, Ottawa, ON, Canada

Edited by: The James–Lange theory considers emotional feelings as perceptions of physiological
Lihong Wang, Duke University, USA
body changes. This approach has recently resurfaced and modified in both neurosci-
Reviewed by:
entific and philosophical concepts of embodiment of emotional feelings. In addition to
Lihong Wang, Duke University, USA
Mauro Adenzato, University of Turin, the body, the role of the environment in emotional feeling needs to be considered.
Italy I here claim that the environment has not merely an indirect and instrumental, i.e.,
*Correspondence: modulatory role on emotional feelings via the body and its sensorimotor and vegeta-
Georg Northoff , Mind, Brain Imaging tive functions. Instead, the environment may have a direct and non-instrumental, i.e.,
and Neuroethics Research Unit,
constitutional role in emotional feelings. This implies that the environment itself is con-
Institute of Mental Health Research,
1145 Carling Avenue, Ottawa, ON, stitutive of emotional feeling rather than the bodily representation of the environment.
Canada K1Z 7K4. I call this the relational concept of emotional feeling. The present paper discusses
e-mail: georg.northoff@rohcg.on.ca recent data from neuroimaging that investigate emotions in relation to interoceptive
processing and the brain’s intrinsic activity. These data show the intrinsic linkage of
interoceptive stimulus processing to both exteroceptive stimuli and the brain’s intrin-
sic activity. This is possible only if the differences between intrinsic activity and intero-
and exteroceptive stimuli is encoded into neural activity. Such relational coding makes
possible the assignment of subjective and affective features to the otherwise objec-
tive and non-affective stimulus. I therefore consider emotions to be intrinsically affec-
tive and subjective as it is manifest in emotional feelings. The relational approach thus
goes together with what may be described as neuro-phenomenal approach. Such neuro-
phenomenal approach does not only inform emotions and emotional feeling but is also
highly relevant to better understand the neuronal mechanisms underlying consciousness
in general.
Keywords: consciousness, emotion, emotional feeling, insula, James–Lange theory

INTRODUCTION in emotional feeling (Colombetti and Thompson, 2005, 2007;

The well-known James–Lange theory determined feelings as per- Colombetti, 2008)1 .
ceptions of physiological body changes in the autonomic, hor- The emphasis on the body raises the question for the role of the
monal, and motor systems. Once we become aware of phys- environment in constituting emotional feelings. The body stands
iological bodily changes induced by danger, we feel fear and in direct contact with the environment via its sensorimotor func-
subjectively experience emotional feelings. James (1884, p. 190) tions which are emphasized in recent body-based, e.g., embodied
consequently considered bodily changes as central to emo- concepts of emotional feelings (see Niedenthal et al., 2005; Nieden-
tional feelings; “we feel sorry because we cry, angry because thal, 2007). The body is supposed to represent the environment in
we strike, afraid because we tremble, and not that we cry, sensorimotor terms and it is these bodily representations that are
strike, or tremble, because we are sorry, angry, or fearful, considered crucial in constituting emotional feelings. The envi-
as the case may be.” Modern empirical versions of this the- ronment may have then an indirect and modulatory role via the
ory resurface in current neuroscientific models of emotion as, body in the constitution of the emotional feelings.
for instance, in Damasio and others (Damasio, 1999, 2010; One could also imagine that the environment has a direct and
Craig, 2003, 2004, 2005, 2009, 2011; Bechara, 2004; Niedenthal, constitutive role in emotional feeling; the environment may then
2007).
Conceptually, the embodied approach to emotion emphasizes
the crucial role of the body in emotional feeling. If the body 1 Itshould also be pointed out that feelings cannot be considered to be conscious
and its vegetative and sensorimotor function play a crucial role perceptions of the neural activity in those brain regions that induce emotion as
in constituting emotional feelings, the body can no longer be con- for instance LeDoux assumes. We cannot become conscious of neural activity in
the first-order emotion regions (see also Bennett and Hacker, 2003, 208) since we
sidered in a merely objective way but rather as subjective and remain principally unable to perceive our brain’s neural activity as such which I
experienced – the mere Koerper as objective body must be dis- recently called “autoepistemic limitation” (Northoff, 2004; Northoff and Musholt,
tinguished from the lived body as subjectively experienced body 2006, see chapter 1 and 2 in Northoff, 2011).

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 1

Northoff Emotion and consciousness

directly constitute emotional feeling independent of the body’s exteroceptive-directed attention. Interoceptive attention to the
sensorimotor (and vegetative) functions. In this case, emotional own heartbeat increased activity in the right insula (and the
feelings should be constituted directly by the respective person’s SACC/DACC and the somatomotor cortex) while exteroceptive
and its brain’s relation to the social environment (see below for def- attention to the tone suppressed activity in the very same region.
inition) rather than indirectly via bodily representations. Since the Activity in the right insula also correlated with both the per-
person-environment relation is crucial here, I call such approach formance in the heartbeat detection task and subjective anxiety
the relational concept of emotional feeling (see Northoff, 2004 for symptoms which also correlated with each other. These findings
a general outline of such relational approach and Ben-Ze’ev, 1993 suggest close relationship between interoceptive awareness and
for the characterization of perception as relational). emotional feeling.
The general aim of the present paper is to review recent human Other studies demonstrated the modulation of these intero-
imaging data on emotional feelings in relation to both intero- ceptive stimulus changes by exteroceptive stimuli. Using fMRI,
ceptive processing and the brain’s intrinsic activity. This will be Critchley (2005), for instance, investigated regional neural activity
accompanied by discussing the empirical and conceptual implica- changes during presentation of happy, sad, angry, and disgusted
tions of these data which I assume to favor a relational approach faces. They observed heart rate changes to be dependent upon the
to emotions. Such relational concept characterizes emotions and emotional category with sad and angry faces inducing the strongest
emotional feeling to be intrinsically affective and subjective. Neu- heart rate changes. Emotional face-responsive regions like the
ronally I assume this to be related to the interaction of the stimuli right (and left) insula, the SACC/DACC, the midbrain/brain stem,
with the brain’s intrinsic activity, i.e., rest-stimulus interaction (see and the right amygdala were also found to be correlating with
below for definition). Finally, the empirical and conceptual impli- the changes in heart rate magnitude. These results indicate that
cations of such relational approach to emotions for consciousness different emotions may be mediated by differential interoceptive
are pointed out. response patterns which may be mediated by neural activity in
the right insula, the SACC/DACC, the midbrain/brain stem, and
EMPIRICAL DATA: INTEROCEPTION AND EMOTIONAL the amygdala. According to the authors themselves, these results
FEELING provide support for the hypothesis that interoceptive stimulus pro-
BRAIN IMAGING OF INTEROCEPTIVE AWARENESS cessing may be involved in differentiating between different types
Recent imaging studies using fMRI investigated neural activity of emotional feelings.
during interoceptive stimulus processing like evocation of blood The group around Pollatos conducted a series of studies
pressure changes during isometric and mental tasks, heart beat on heartbeat perception and emotional feeling. Pollatos et al.
changes and perception, anticipatory skin conductance during (2007a) investigated attention toward heartbeats and cardiovas-
gambling, and heart rate modulation during presentation of emo- cular arousal; regions implicated in both conditions included the
tional faces (Critchley, 2005 for a review, Craig, 2002, 2003, 2004, right insula, the somatomotor cortex, the SACC/DACC, and the
2009, 2011; Pollatos et al., 2007a,b). These studies observed neural dorsomedial prefrontal cortex (DMPFC). They observed activity
activity changes in the right insula, the anterior cingulate cortex in the right insula and the DACC to be correlating with the degree
extending from supragenual to dorsal regions (SACC/DACC), and of interoceptive awareness while negative feelings correlated with
the amygdala. This led to the assumption that specifically the right the BOLD response of the interoceptive awareness condition in the
insula and the SACC/DACC integrally represent autonomic and DACC and DMPFC. Using EEG, they distinguished between good
visceral responses that are transferred from the spinal cord through and poor heartbeat perceivers. Good heartbeat perceivers (Pol-
the midbrain, the hypothalamus, and the thalamocortical pathway latos et al., 2005, 2007a,b) showed higher arousal ratings as well as
to the right insular cortex (Craig, 2002, 2003, 2004, 2009; Critch- higher P300 amplitudes and slow-wave latency ranges than poor
ley, 2005). Based on these results, these regions are assumed to be heartbeat perceivers during presentation of emotional pictures.
involved in re-presenting the autonomic and visceral state of the Taken together, these studies show behaviorally a close rela-
body and thus interoceptive processing. Craig (2002, 2003, 2004, tionship between interoceptive awareness, arousal, and emotional
2009, 2010, 2011) assumes specifically the right insula to be cru- feeling. While neuroanatomically, they confirm the involvement of
cially involved which receives autonomic and visceral afferences the right insula, the SACC/DACC, and the DMPFC in mediating
from lower centers (see above) and re-represents the interocep- the relationship between interoceptive awareness and emotional
tive body state in an integrated way. This allows the insula to give feeling.
rise of a “mental image of one’s physical state” which, according
to Craig, provides the basis for subjective awareness of emotional INTEROCEPTIVE AND EXTEROCEPTIVE AWARENESS
feeling and one’s self as “material me.” The question is whether the above described data support an
See Figure A1 in Appendix for the different regions, and embodied concept of emotional feeling with exteroceptive stimuli
Glossarium for the terms. being merely modulatory and instrumental or epiphenomenal. Or
If these regions mediate interoceptive processing, the ques- whether the data might be interpreted rather in favor of a relational
tion for their role in the subjective experience of bodily and concept of feelings with interoceptive stimuli in relation to extero-
thus interoceptive changes as the basis for emotional feeling ceptive stimuli being constitutive and thus central. Presupposing
arises. Critchley et al. (2004) led subjects evaluate whether the the James–Lange theory, most of the above cited authors have
own heart beat was synchronous or asynchronous with an audi- interpreted their data in favor of the interoceptive-based concept.
tory feedback note which allowed to compare interoceptive- and However, I will argue that there are strong arguments which make

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 2

Northoff Emotion and consciousness

the data rather compatible with what I call the intero-exteroceptive potentials and stronger dipole strength in cortical sources that
relational concept of emotional feeling. I argue that there seems to included the SACC/DACC, the right insula, the DMPFC, and
be a mismatch between empirical data and their interpretation in the secondary somatosenory cortex when compared to poor
current imaging studies on emotional feelings and interoceptive heartbeat perceivers. Interestingly, they also observed the dipole
processing which I want to support by making the three following sources in the SACC/DACC and DMPFC to occur earlier (around
points. 280 ms) than the ones in the insula and the somatosensory
First, all paradigms employed did not investigate interocep- cortex (around 370 ms). A similar temporal distribution is sug-
tive stimuli in isolation from exteroceptive stimuli but rather in gested by Tsuchiya and Adolphs (2007) who assume involve-
relation to them. Critchley et al. (2004), for instance, investigated ment of subcortical regions like brain stem nuclei and hypo-
heart beat perception in relation to auditory tones as exterocep- thalamus that mediate interoceptive stimuli to occur after and
tive stimuli while Pollatos et al. (2005, 2007a,b) directly compared later than activation in higher regions like the DMPFC. If the
both conditions with each other. Neural activity changes assumed interoceptive-based model were true, one would rather expect
to be specific for interoceptive awareness thus reflect a relation the opposite temporal pattern with early insula and somatosen-
or dynamic balance between intero- and exteroceptive processing sory involvement and late SACC/DACC and DMPFC involve-
rather than mirroring isolated interoceptive stimulus processing ment.
remaining (more or less) independent of exteroceptive stimulus Late SACC/DACC and DMPFC involvement may then reflect
processing. Dynamic modulation of the right insula activity as some abstract internal cognitive evaluation of interoceptive
observed by Critchley may thus reflect a dynamic balance between stimulus processing with consecutive top-down modulation of
intero- and exteroceptive attention in the heartbeat-auditory tone interoceptive brain regions as interpreted by advocates of the
detection task rather than pure interoceptive heartbeat stimulus interoceptive-based concept (Craig, 2002, 2009; Tsuchiya and
processing. Such intero-exteroceptive relational concept would Adolphs, 2007). What is the role of the SACC/DACC and the
thus assume that the above mentioned regions like the right DMPFC? These higher cortical regions have been associated
insula, the SACC/DACC, and the DMPFC are rather respon- with processing of higher-order exteroceptive stimuli particularly
sive to changes in intero-exteroceptive balance than to isolated those that are highly self-related to the organism (Northoff and
interoceptive changes remaining independent of exteroceptive Bermpohl, 2004; Northoff et al., 2006).
changes. The fact that these regions are apparently implicated from early
Second, neither of the above mentioned studies addressed the on in interoceptive awareness gives some though indirect support
question of emotional valence that indicates whether a feeling is to the assumption that exteroceptive stimuli are involved early
positive or negative (see also Colombetti, 2005 for a discussion of in interoceptive processing. Such early involvement indicates that
the concept of emotional valence). Pollatos et al. (2005, 2007b) the role of exteroceptive stimulus processing goes beyond mere
did not observe any significant difference between good and poor modulation of interoceptive processing which would be better
heartbeat perceivers in terms of their emotional valence ratings compatible with late involvement. In other terms, early involve-
while both groups did differ in emotional arousal. Interoceptive ment of these regions may indicate that interoceptive stimulus
awareness may thus be linked to emotional arousal and subjec- processing is coded in relation to exteroceptive stimuli going
tive experience of emotional intensity while it apparently does not beyond mere modulation of the former by the latter. The observed
seem to determine the valence of the emotional feeling. Regions early spatio-temporal pattern may thus reflect neural coding of the
that have been associated with emotional valence, as distinguished relationship between intero- and exteroceptive stimulus process-
from emotional arousal, include the medial orbitofrontal cortex ing, i.e., their actual balance. Otherwise there would be no need
(MOFC), the subgenual and pregenual anterior cingulate cortex for regions predominantly associated with exteroceptive stimu-
(PACC), and the ventromedial prefrontal cortex (VMPFC; Craig, lus processing to be implicated so early. While it seems to be
2002, 2009; Phan et al., 2002; Critchley, 2005; Kringelbach, 2005; less compatible with the assumption of primarily independent
Grimm et al., 2006). interoceptive processing that becomes secondarily modulated by
Interestingly, these regions are densely and reciprocally con- exteroceptive stimuli.
nected with the right insula, the SACC/DACC, and the DMPFC Finally, direct empirical support for intero-exteroceptive con-
that are supposed to represent the body’s interoceptive state vergence comes from a recent study by Farb et al. (2012). He
(Ongur and Price, 2000). The connectivity pattern thus argues investigated interoceptive awareness (i.e., attention to breath-
strongly in favor of the intero-exteroceptive relational concept ing rate) and exteroceptive awareness (i.e., visual attention) in
of emotional feeling which seems to make isolated interocep- the same subjects. While both intero- and exteroceptive aware-
tive processing and thus an interoceptive-based concept of emo- ness yielded dissociable networks (i.e., visual cortex and pos-
tional feeling rather unlikely. What however is needed to fur- terior insula), they overlapped in especially the anterior insula.
ther support this point are investigations of both regional activ- Unlike the posterior insula that responded strongly to intero-
ity and connectivity patterns during intero- and exteroceptive ceptive awareness, the anterior insula activity was as much pre-
stimulus processing (see Hurliman et al., 2005 for some first dicted by exteroceptive awareness as interoceptive awareness.
support). Hence, there seems to be intero-exteroceptive convergence in
Third, Pollatos et al. (2005, 2007b) investigated the temporal especially the anterior insula with both being integrated in the
course with EEG during heartbeat perception task. They observed middle insula as bridge from posterior to anterior parts of the
that good heartbeat perceivers showed higher heart-evoked insula.

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 3

Northoff Emotion and consciousness

EMPIRICAL IMPLICATIONS: CONNECTIVITY AND CODING Taken together, both connectivity pattern and imaging data
ANATOMICAL CONNECTIVITY AND INTERO-EXTEROCEPTIVE suggest that neural processing in aCMS is supramodal and
CONVERGENCE domain-independent: what apparently matters for inducing
The MOFC and the VMPFC have been demonstrated to be impli- neural activity in the aCMS is not so much the modality or
cated in interoceptive processing. Using biofeedback arousal and domain, i.e., the origin of the stimulus, as either intero- or exte-
relaxation tasks in fMRI, Nagai et al. (2004) demonstrated that roceptive or cognitive, motor, sensory, or emotional. Instead it is
resting state activity in the VMPFC and MOFC co-varied with the important how the neural activity in the aCMS is related to the
basal level of sympathetic skin conductance. While regions like respective intero- or exteroceptive stimulus (see below for further
the SACC/DACC, the insula, and the hypothalamus were related discussion).
to the rate of change in skin conductance. The level of neural In addition to the aCMS, subcortical midline regions like the
activity in VMPFC and MOFC, which are part of the so-called periaquaeductal gray (PAG), the colliculi, the dorsomedial thala-
anterior cortical midline structures (aCMS), may thus represent mus, and the ventral striatum may also be considered in processing
the basal sympathetic or autonomic tone independent of some interoceptive stimuli in relation to exteroceptive ones. Panksepp
actual stimuli. Since the aCMS have been shown to be modulated (1998; and also Damasio, 1999, 2010), for instance, assumes that
also by exteroceptive stimuli, neural activity within these regions these regions are crucial in constituting emotional feelings. Since
may mirror a dynamic balance between attention to extero- and the very same regions are also characterized by strong motor con-
interoceptive stimuli (see also Nagai et al., 2004). This assump- nections both afferent and efferent, he and others like Ellis (2005;
tion is well compatible with the connectivity pattern of these unlike Damasio who assumes a sensory-based view of feelings)
regions. assume emotional feeling to be motor-based. This is well com-
The MOFC and VMPFC as the entrance door to the aCMS patible with Panksepp’s characterization of emotional feeling as
receive connections from all regions associated with primary reaching-out to the environment thus reflecting what I called the
and/or secondary exteroceptive sensory modalities (olfactory, gus- relational concept of emotional feeling.
tatory, somatosensory, auditory, and visual; see Rolls et al., 1999; Unfortunately, subcortical regions have often been neglected
Barbas, 2000; Rolls, 2000; Damasio, 2003, 2010; Kringelbach and in imaging studies of emotions which, at least in part, may be
Rolls, 2004). The aCMS are also densely connected to regions due to the fact that neural activity in these regions is rather
(insula, hypothalamus, and nuclei in the brain stem as such difficult to reliably visualize in current imaging techniques like
PAG, colliculi, etc.) processing interoceptive sensory signals; these fMRI. However, animal experiments demonstrate the crucial role
include the proprioceptive and vestibular senses, the visceral sense, of these subcortical midline regions in constituting emotional feel-
and the sense of the interoceptive milieu which can be taken ings (Panksepp, 1998, 2005). Future studies in humans are thus
together with that of pain and temperature (Carmichael and needed to investigate subcortical neural activity during emotional
Price, 1996; Price, 1999; Rolls et al., 1999; Rolls, 2000; Dama- feeling in order to bridge the current gap between animals and
sio, 2003, 2010; Barbas, 2004; Kringelbach and Rolls, 2004). The humans. Furthermore, the relationship between emotional feel-
aCMS, especially the MOFC, VMPFC and SACC/DACC, are also ing and motor function also needs to be investigated in detail
connected to regions associated with distinct functional domains by, for instance, investigating emotional feeling in dependence on
including motor (premotor and motor cortex, basal ganglia), cog- variation of motor function and its neural underpinnings (and
nitive (lateral prefrontal cortex), and emotional (amygdala, brain vice versa).
stem) domains (Carmichael and Price, 1996; Rolls et al., 1999;
Barbas, 2000; Ongur and Price, 2000; Rolls, 2000; Kringelbach and TRANSLATIONAL VERSUS RELATIONAL CODING
Rolls, 2004). Due to such extensive intero- and exteroceptive con- What is the implicit presupposition that drives most of the above
nections, the MOFC and VMPFC (and, in conjunction with the cited authors to interpret their data in favor of the James–Lange
amygdala) can be characterized as polymodal convergence zone theory? They seem to presuppose a clear-cut distinction between
(Rolls et al., 1999; Rolls, 2000; LeDoux, 2002; Schore, 2003). intero- and exteroceptive stimulus processing with both systems
This connectivity pattern predisposes the aCMS for neural pro- being separate, distinct, and only interacting at specific node
cessing irrespective of the sensory modality of the respective stim- points. According to such view, exteroceptive stimuli are trans-
ulus, i.e., supramodal processing. The assumption of supramodal lated into interoceptive stimulus processing whose perception, in
processing in aCMS is supported by results from imaging stud- turn, is supposed to induce feeling. Exteroceptive stimuli thus have
ies. Emotions in either exteroceptive modality (visual, auditory, at best an only indirect and mediated impact on emotional feeling
gustatory, olfactory) induce neural activity in various regions of in that they must first be translated into interoceptive stimulus
the aCMS (see above as well as Phan et al., 2002; Northoff and processing before they can modulate feelings. I therefore call this
Bermpohl, 2004). Moreover, processing of interoceptive stimuli model the interoceptive-based translational concept of feeling.
induces also activation in aCMS regions like MOFC, VMPFC, Since exteroceptive stimuli have only an indirect and mediated,
and ACC (Craig, 2002, 2003, 2004, 2009; Wicker et al., 2003; the interoceptive-based translational concept attributes no con-
Critchley et al., 2004; Nagai et al., 2004). Finally, stimuli from stitutive role of exteroceptive stimuli and the environment thus
different origins, i.e., of different sensory modalities or of different presupposing an “embodied” concept of emotional feeling.
functional domains (motor, emotional, cognitive, and sensory) However, anatomical connectivity suggests otherwise. Through-
induced analogous activation in aCMS (Northoff and Bermpohl, out the brain at all levels both subcortical and cortical and
2004; Northoff et al., 2006). especially in the subcortical-cortical midline system there is

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 4

Northoff Emotion and consciousness

convergence between intero- and exteroceptive inputs. This is feelings but actively participates in constituting emotional feelings.
especially true for regions like the colliculi, the PAG, the tectum, This is well in accordance with the Schacter/Singer experiments
and the aCMS where both intero- and exteroceptive afferences where different contexts resulted in different types of emotional
converge onto common neurons (see Panksepp, 1998, 2005; Rolls feelings. If the role of the context were merely modulatory, sub-
et al., 1999). This suggests that interoceptive stimuli are not only jects would not have shown completely different and opposing
modulated by exteroceptive stimuli at specific node points but emotional feelings in the two situations but rather variants of
rather that the relation, e.g., the degree of convergence and diver- the same feeling. These experiments thus lend further support
gence, between intero- and exteroceptive stimuli is coded in neural to the assumption of a constitutive role of the environmen-
activity in the subcortical-cortical midline regions. Exteroceptive tal context in emotional feelings (rather than remaining merely
stimuli are not translated into interoceptive stimulus processing modulatory).
but rather directly and unmediated related to them and it is this How are intero- and exteroceptive stimuli related and bal-
relation that seems to be coded in neural activity. I therefore call anced with each other in relational coding? Rather than coding the
this model the intero-exteroceptive-based relational concept of intero- or exteroceptive stimulus itself, the degree of correspon-
feelings (see also Figure 1). dence between intero- and exteroceptive stimuli is coded. If, for
Is there any empirical evidence in favor of the intero- instance a lion approaches, the heart rate may increase, which may
exteroceptive relational model of neural coding? Critchley (2005, signal strong correspondence and convergence between intero-
p. 162), one of the main investigators of interoceptive processing and exteroceptive stimuli. This consecutively leads to the consti-
in imaging, states, that the “right insula maps bodily arousal states” tution of a corresponding emotional feeling, the feeling of fright
and “it does so contextually” which therefore “represents an inte- and anxiety. If, in contrast, the approach of the lion is not accom-
gration of external emotional information with peripheral states panied by heart rate increases, as for instance if one is not clear
of arousal” (Critchley, 2005, p. 759). What seems to be coded in whether the lion is real or not, there may be a mismatch between
the brain is not so much the interoceptive stimulus itself but its intero- and exteroceptive stimuli. This may result in a different
relation to the respective exteroceptive stimulus. If neural activity emotional feeling, the feeling of doubt and hesitation. The degree
codes the actual relationship and balance between intero- and exte- of convergence and divergence between intero- and exteroceptive
roceptive stimuli, one would expect strong contextual dependence stimuli may thus determine the kind of emotional feeling. That is
of emotional feelings. well in accordance with the relational concept rather than with the
The constitution of the emotional feeling, the type of feeling, translational one that claims for an interoceptive- and thus bodily
should then depend on the respective emotional context which based approach.
implies that different contexts may lead to different types of Taken together, I assume that our brain’s design is such
emotional feelings even in identical situations. In other terms, that there is no way for interoceptive stimuli other than to be
the environmental context does not only modulate emotional processed in relation to exteroceptive stimuli and vice versa.

FIGURE 1 | The figure compares two different ways of neural coding in James–Lange theory leads to emotional feelings. This is different in
emotional feeling. On the left side translational coding describes how relational coding on the right side. Here intero- and exteroceptive stimuli
intero- and exteroceptive stimuli are separately represented and are coded in relation to each other with this relation resulting in emotional
meta-represented in the neural activity of the brain. This feeling and subsequent experience of the relationship between body and
meta-representation is then perceived which following Damasio and the environment.

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 5

Northoff Emotion and consciousness

Interoceptive stimulus processing remaining isolated, unrelated What does such non-instrumental or constitutional, as I will
and independent from exteroceptive stimulus processing is conse- call it in the following (see also Colombetti, 2008), dependence
quently assumed to remain (principally) impossible. This implies imply for the relationship between body and environment in
what I call intero-exteroceptive relational coding while it excludes emotional feeling? If the relationship between emotional feel-
interoceptive-based translational coding. What does this imply in ing and environment is direct and therefore constitutional, i.e.,
experimental regard? The experimental efforts to isolate intero- non-instrumental, changes in the environment should be able to
ceptive stimulus processing and to search for its specific neural impact and constitute emotional feelings independently of the
correlates may be futile since exteroceptive stimulus processing body’s sensorimotor representation. The environment itself may
may always already be implicated in interoceptive stimulus pro- then directly involved in constituting emotional feelings. Thereby,
cessing. One may better focus on experimentally investigating the concept of environment is meant here in a social sense, social
different intero-exteroceptive stimulus configurations and thus environment, as distinguished from the merely physical world (or
different constellations between body and environment as nicely physical environment).
demonstrated in the Schacter/Singer experiments (see Northoff, This has empirically been paradigmatically exemplified in a
2012a for more details on the question of neural coding). recent study on reward (Fliessbach et al., 2007). Two subjects a and
b were simultaneously scanned while receiving rewards. While the
CONCEPTUAL IMPLICATIONS: RELATIONAL APPROACH TO reward for the subject a was fixed, the one for subject b was varied;
EMOTIONAL FEELING this and the converse case, increasing rewards for subject a and
RELATIONAL CONCEPT OF EMOTIONAL FEELING fixed rewards for subject b, allowed to investigate its impact of the
The philosopher Hurley (1998, pp. 10, 341–342, 362–364) distin- environment, i.e., subject b, on subject a. Interestingly, emotional
guishes between instrumental and non-instrumental dependence feelings and neural activity in reward circuitry in subject a did not
(see also Colombetti, 2008 who also applies this distinction) with so much depend on the size of the reward it received but rather on
regard to the relationship between input and output in perceptual the relation of or balance to its own reward when compared to the
content. If the relationship between input and output is indirect one received by subject b. If, for instance, subject a received 60$
and thus merely instrumental, changes in perceptual content are and subject b only 30$, subject a showed happiness and increased
dependent upon changes in the input. Every change in motor out- reward circuitry activation. If, in contrast, subject b received 120$
put has to modulate sensory input in order to have an impact with subject a still receiving 60$, subject a no longer showed hap-
on perceptual content implying that the output can not change piness and increased neural activity in reward circuitry. Though
independently of the input: “This kind of dependence of per- sensorimotor input was exactly the same for subject a in both cases
ceptual content on output is merely instrumental. It operates via (only subject’s b reward amount changed), playing the same game
changes in input; changes in output are a means to changes in and receiving the same reward, emotional feelings, and neural
input” (Hurley, 1998, p. 10). activity in reward circuitry differed in dependence on the amount
What does this mean with regard to emotional feelings and their of reward subject b received when compared to the amount subject
relation to the environment? Presupposing instrumental depen- a received.
dence, the environment can impact emotional feelings only indi- This means that, to put it into conceptual terms, emotional feel-
rectly via the body, i.e., by being represented either in the body’s ings and neural activity in subject a were not merely instrumentally
sensorimotor (and vegetative) functions or in those brain regions dependent upon the social environment (since then changes in
that register the body’s sensorimotor (and vegetative) functions. subject b could have impact subject a only if they had changed
The latter approach is, for instance, advocated by the propo- subject’s a reward) but rather instrumentally or constitutionally.
nents of Damasio’s theory of emotional feeling where the relation More specifically, it is the relationship between person and (social)
between body and environment remains at best modulatory (and environment, the actual difference or balance between subjects’ a
contributing but not as constitutive). This is nicely reflected in and b rewards, that seemed to determine emotional feelings and
a quote from a recent paper about emotion and consciousness: neural activity. It is such constitutional, i.e., non-instrumental,
“Here, we follow the common view that emotion and conscious- dependence of emotional feelings on the social environment
ness emerge as a result of neuronal activity in the brain, but some and its relationship to the person that I will characterize as the
accounts view emotions or consciousness as relationships between relational concept of emotional feelings2 . Such intrinsic linkage
an organism and its environment (here we acknowledge such rela- between emotional feelings and the social environment is empiri-
tionships as contributing but not as constitutive)” (Tsuchiya and cally further supported by the observed overlap between emotion
Adolphs, 2007, p. 159; see also Bechara and Naqvi, 2004). processing and social processing (like social intentions; see Cia-
Non-instrumental dependence, in contrast, is described by ramidaro et al., 2007) in especially aCMS like the anterior cingulate
Hurley as direct dependence of perceptual content on motor
output independent of sensory input; even if the sensory input 2 The here advanced relational concept may be considered an extension of the
remains the same and fixed, perceptual content can vary depending embodied approach by Colombetti and Thompson, who also emphasize the sit-
on motor output. This means that motor output has direct access uated, extended and thus embedded nature of emotional feeling. Since the main
to perceptual content independent of sensory input and therefore focus here is on the neurophilosophical aspect, I cannot go into the philosophical
details about the relational approach (see below for the discussion of some philo-
no longer operates indirectly via sensory input as in instrumental sophical implications and Northoff, 2004 for a general outline). See also Ben-Ze’ev
dependence; instead, perceptual content may vary in orientation (1993, 81–99) who advocates a relational approach to perception and, in some part,
on motor output independent of sensory input and thus directly. also to emotion (see Ben-Ze’ev, 2000)

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 6

Northoff Emotion and consciousness

cortex and the DMPFC (see Schilbach et al., 2012). These (and person-environment relations rather than to the representa-
other) data end strong support to an intrinsically social and thus tional capacities of specific functions, i.e., motor, cognitive, or
relational concept of emotional feeling. physiological-registering.
If emotional feelings are intrinsically relational, i.e., depending
EMBEDDED APPROACH TO EMOTIONAL FEELING upon the person-environment relation rather than some repre-
The relational approach shifts the focus of attention from the sentational capacities in motor, cognitive, or neural-subcortical
body, as in the embodied approach, to the role of the environ- function, one would expect different feelings to reflect differ-
ment in emotional feelings. Rather than modulating emotional ent kinds of person-environment relationships. Ratcliffe (2005,
feelings indirectly via bodily representations, the environment is 2008) does indeed assume exactly this and assumes what, rely-
supposed to be involved directly in constituting emotional feel- ing on Heidegger’s phenomenology, he calls “existential feelings.”
ings. How does the person-environment relation account for “Existential feelings” include feelings of homeliness, belonging,
the variety of different specific emotional feelings? The lack of separation, unfamiliarity, power, control, being part of some-
specificity concerning distinct emotions has often been criti- thing, being at one with nature, and “being there.” These feelings
cized in feeling theories like the James–Lange theory (see also have in common that they describe “ways of finding ourselves
Niedenthal et al., 2005). Autonomic bodily changes like arousal in the world” which metaphorically circumscribes what I called
are rather unspecific reactions that do not allow to distinguish the person-environment relation. What Ratcliffe calls existential
between distinct emotions. This criticism has been furnished feeling presupposes what I here advance as relational concept of
by the Schachter and Singer (1962) experiments demonstrat- emotional feeling. How does the person and thus the subject come
ing that subjects with autonomous nervous system stimulation, into play in emotional feelings? This will be the focus in the next
as induced by epinephrine, experienced the resulting arousal as sections.
either anger or euphoria in dependence on the respective con-
text (they were placed in a room with either an angry or happy EMPIRICAL DATA: INTRINSIC ACTIVITY AND EMOTIONAL
actor). FEELING
The conclusion is often drawn that physiological bodily changes EMOTIONS AND RESTING STATE
and arousal themselves remain unspecific and cannot contribute I so far focused on the relationship between intero- and exterocep-
to determine specific emotions); determination and distinction of tive stimulus processing in emotional feeling. Neurobiologically
specific feelings can consequently not be based upon physiologi- this was supposed to be related to the anatomical convergence
cal bodily changes but must be found elsewhere. This argument between the respective pathways and the kind of coding, i.e., rela-
of the lack of specificity of bodily representations has been coun- tional coding rather than translational coding. While conceptually
tered in different ways by referring to motor, cognitive, or neural this implied a shift from the embodied concept of emotional feel-
representation. Zajonc (1998, 2000), for instance, claims that ing to a relational concept (or as the philosophers may want to
the motor system allows for extremely subtle distinctions which say an extended concept). This pointed out the intrinsic relation
means that even a number of limited bodily states can support to emotional feelings to the environment as bridge between body
a very large number of representational distinctions of distinct and environment.
emotional feelings. Rather than referring to motor capacities, cog- What remains unclear though are two aspects: why are emo-
nitive theories, e.g., appraisal theories (Solomon, 2004; and also tional feelings not objective but rather subjective as manifest in an
Schachter and Singer, 1962) resort to cognitive representations emotional experience? And why are emotional feelings affective
and higher-order cortical brain functions which may allow for a and thus emotional? Taking a purely logical stance one could well
much more fine-grained distinction between different emotional imagine mere feelings without any emotions. Both questions dent
feelings. deeply in various domains of research including consciousness
Damasio (1999, 2003, 2010) suggested a middle way between (see Northoff, 2012a,b) which though I will avoid here to keep
motor and cognitive representation. He focuses on those sub- matters simple. I will here focus only on some neurobiological
cortical brain regions that register physiological bodily states mechanisms while leaving the philosophical implications open. In
which may allow for a wider representational spectrum than order to shed some light on these questions, I turn to recent results
the muscles and viscera themselves that are actually repre- about the relation between resting state activity and emotions.
sented in the respective neural states. All these approaches have A recent study by Sreenivas et al. (2012) investigated different
in common that they still presuppose representation of emo- emotional faces (sad, happy, neutral) in fMRI and focused thereby
tional feelings in motor, cognitive, or neural-subcortical func- predominantly on the midline regions of the default-mode net-
tions. work (DMN). They demonstrated that sad faces induced a higher
The relational approach, in contrast, claims that the wide degree of deactivation, i.e., negative signal changes in the VMPFC,
variety of different emotional feelings may ultimately be traced the PCC, and the precuneus when compared to happy faces. In
back to the relation between person and environment rather contrast, activation and thus positive emotional signal changes
than to motor, cognitive, or neural-subcortical representation. were observed in the lateral fronto-parietal regions (except in left
Since an abundant variety of different person-environment rela- middle frontal gyrus). Finally, functional connectivity pattern also
tions are possible, different emotional feelings can be con- differed between sad and happy emotions for the connections
stituted. The question for the specificity of emotional feel- between the midline and the lateral regions with VMPFC, PCC,
ings is thus traced back to the possible (and impossible) and precuneus being central nodes.

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 7

Northoff Emotion and consciousness

While this study demonstrates that emotions are associated neutral larger rest after fearful) revealed higher signal changes in
with midline regions that show high resting state activity, it leaves various regions of the DMN (VMPFC, PACC, DMPFC, STG).
open whether that is related to intero- or exteroceptive stim- This means that the inclusion of fearful emotions in the preceding
uli. This was tested for by a study by Wiebking et al. (2011) movie had a clear effect on the level of subsequent resting state
from our group. Subjects had to perform the above mentioned activity. The stronger resting state effects of the preceding emo-
intero-exteroceptive awareness with long resting state intervals tional movies are further confirmed by the more delayed recovery
(8–13 s) in-between. These served to subtract both intero- and of the signal changes during the resting state period (90 s) after
exteroceptive signal changes from the resting state which, as emotional movies.
expected, yielded higher activity changes in the midline regions. This study clearly demonstrates that emotions have an impact
We then determined the degree of deactivation during both on the subsequent resting state thus implying what we coined
intero- and exteroceptive awareness. That yielded stronger deacti- as stimulus-rest interaction (see Northoff et al., 2010). This was
vation in exteroceptive awareness when compared to interoceptive also observed in another study. Veer et al. (2011) investigated a
awareness. psychological stress task in healthy subjects and scanned them in
How is all that related to emotions? For that Wiebking et al. their resting state one hour later in fMRI. This revealed increased
(2011) included psychological measures of emotions (i.e., the functional connectivity from the amygdala to the cortical mid-
Florida Affect battery and the Beck Hopelessness scale) and corre- line structures like the MPFC, the PCC, and the precuneus. This
lated them with the signal changes in the midline regions dur- indicates that psychological stress implicating strong and nega-
ing the different conditions. Interestingly, we did not observe tive emotions can affect the subsequent resting state activity thus
any correlation of the emotion measures with the midline sig- implying stimulus-rest interaction.
nal changes during interoceptive awareness alone. Instead, the Taken together, these studies demonstrate the close relation-
emotion measures significantly correlated with especially sig- ship between resting state activity and emotion-related activity.
nal changes in VMPFC, DMPFC, and PCC during rest and This seems to be especially apparent in the midline regions as core
exteroceptive awareness: The stronger the emotion score, the nucleus of the DMN. The high intrinsic activity in these regions
smaller the degree of deactivation in the midline regions thus being seems to be closely related to emotion processing in though yet
closer to the resting state activity level. In contrast, no correlation unclear ways. Different emotions seem to modulate the degree of
was observed with signal changes during interoceptive awareness. stimulus-related deviation from the high resting state activity in
Hence, these results underline the central importance of intrinsic different ways. The close relationship between emotions and rest-
and thus resting state activity for emotions. ing state is further supported albeit indirectly by the observation
of severe resting state alterations in major depressive disorder (see
MODULATION OF RESTING STATE BY EMOTIONS Alcaro et al., 2010; Northoff et al., 2011; for recent overviews).
These results show the strong association between resting state
activity and emotions. They though leave open whether emotions EMPIRICAL IMPLICATIONS: INTRINSIC ACTIVITY AND THE
can also modulate resting state activity or whether the latter pre- SUBJECTIVE NATURE OF EMOTIONAL FEELING
dict the former. Several recent studies demonstrated the prediction In order to better understand the potential role of the brain’s
of stimulus-induced activity by the preceding resting state activity intrinsic activity in emotional feeling, we need to go back to the
implying rest-stimulus interaction (see Northoff et al., 2010 for psychological level. For that I turn to two of the major proponents
a review). This was mainly shown in the in the sensory domain of emotional feeling, Jaak Panksepp and Jim Russell, and how they
while, as to my knowledge, such studies are not yet available in the conceptualize especially the subjective-experiential component of
domain of emotions. There are though a couple of studies that emotional feeling. This will be then linked in subsequent sections
show the reverse, modulation of resting state activity by preceding to the above described findings of the close relationship between
emotions. intrinsic activity and emotions.
Focusing on emotions, Eryilmaz et al. (2011) investigated the
impact of fearful, joyful, and neutral movie clips (50 s presenta- PANKSEPP AND RUSSELL ON EMOTIONAL FEELING
tion) on subsequent resting state activity (90 s eyes closed). They Based on the centrality of affect and emotions, Panksepp (1998,
asked the participants after the resting state period about their 2010) developed a neuroscientifically based theory of primary
thoughts. This revealed that the subjects’ personal relevant issues process affects as raw emotional feelings which he associates with
in their thoughts were increased after neutral movies, less increased evolutionary ingrained subcortical circuits. Russell (2003) shifted
after joyful movies, and significantly decreased after fearful movies. from an earlier Psychological Construction Theory of emotions
These results show a clear behavioral or better psychological effect to the assumption of what he calls “Core Affect” as a basic and
of emotions on the thought contents in subsequent resting state foundational unit (or building block) of any specific emotional
periods; fearful movies seem to leave apparently the strongest feeling. While Panksepp’s concept of “primary process affect” over-
traces in the subsequent resting state’s thought contents. laps at least conceptually (and also to some degree empirically)
Neuronally, they showed that the resting state periods after fear- with Russell’s concept of Core Affect (see especially Russell’s p.
ful faces showed higher neuronal activity in subcortical regions 6–7 commentary on Panksepp), they are not the same.
(pallidum, anterior thalamus, hypothalamus) than the ones fol- Panksepp distinguishes between three distinct kinds of primary
lowing neutral movies (rest after fearful larger than rest after process affects, homeostatic, sensory, and emotional. Homeostatic
neutral). Most interestingly, the reverse comparison (rest after affect provides information about the body and thus interoceptive

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 8

Northoff Emotion and consciousness

stimuli, sensory affect is related to exteroceptive stimuli, and conceptual remark here. The meaning of the term subjective refers
emotional affect is associated with the brain (or BrainMind as here only to the experience of affect, it does not say anything about
Panksepp says) and hence with what one may call “neural stim- the underlying neuronal mechanisms that may well be objective.
uli.” These distinctions make it clear that primary process affect This raises the question how affective assignment makes it
is linked with stimuli generally, and more specifically with stimuli possible to transform the originally objective stimulus, interocep-
of different origins, be they of bodily (i.e., interoceptive), envi- tive, exteroceptive, or neural, into a subjective one. Hence, “non-
ronmental (i.e., exteroceptive), or neural origin. Hence, primary affective-affective transformation” is not limited to transforming
process affect must be somehow assigned to stimuli since otherwise a non-affective into an affective stimuli but with transforming the
Panksepp could not associate primary process affect with stimuli objective into a subjective stimulus. I therefore speak of “objective-
of such different origins. I call such association of stimuli with subjective transformation.”“Objective-subjective transformation”
affect or primary process affect “affective assignment” meaning raises the following question: how do the neuronal mechanisms
that a stimulus of whatever origin can be assigned affect. enable the transformation of an objective stimulus into a subjective
Analogous to Panksepp, Russell must also presuppose affec- one? Such that, in conjunction with “non-affective-affective trans-
tive assignment though in a slightly different way. He does not formation” the stimulus can be subjectively and thus internally
associate what he describes as Core Affect itself with a specific and privately experienced.
type of stimulus since unlike Panksepp he does not speak of sen-
sory, homeostatic, or emotional Core Affect. Instead, Core Affect “OBJECTIVE-SUBJECTIVE TRANSFORMATION”
is continuously present independent of the presence or absence of Both Russell and Panksepp seem to presuppose some kind of
particular stimuli. One though has to mention that Russell seems intrinsic stimuli to be crucial in generating affect. Russell does
to refer here only to the absence of exteroceptive stimuli since he so by explicitly distinguishing Core Affect from extrinsic stimuli
does not explicitly talk about interoceptive or even neural stimuli and related emotional episodes, while Panksepp argues that neural
in this context. This means that it cannot be excluded that Core activity in the subcortical circuits is not dependent upon extrinsic
Affect may be related to the assignment of affect to either neural stimuli, i.e., exteroceptive stimuli. This means that both must pre-
or interoceptive stimuli. Hence Russell’s concept of Core Affect suppose some kind of intrinsic activity for the generation of affect
would then also presuppose what I call affective assignment. (Figure 2).
Rather than to interoceptive stimuli, Russell explicitly refers to What could such intrinsic activity be? One may assume it is
the assignment of affect to exteroceptive stimuli when he describes that activity that can be observed in the absence of any extrin-
the transition from Core Affect to emotional episodes and emo- sic stimulation by either intero- or exteroceptive stimuli. Intrinsic
tional meta-experience. In the moment when the continuously means then that the origin of that activity must be traced back
present Core Affect is related to an episodically occurring extero- to the brain itself as distinguished from body and environment.
ceptive stimulus, an emotional episode and meta-experience may One may refine such intrinsic activity as the brain’s resting state
occur. This however is possible only if the Core Affect is linked activity, or that activity in the brain in the absence of any intero-
and thus assigned to the exteroceptive stimulus thus presupposing and exteroceptive stimuli (see Northoff et al., 2010). And it is such
what I here call affective assignment. resting state activity as intrinsic activity that can be observed in all
While both Panksepp and Russell seem to presuppose the brain regions cortical and subcortical (see Northoff et al., 2010).
assignment of affect to stimuli, the exact functional mechanisms The fact that resting state activity is present throughout the
that enable and predispose such affective assignment remain whole brain means that there may already be some neural interac-
unclear in their accounts. What functional mechanisms are neces- tions between the different brain regions within the resting state
sary to enable and predispose the transformation of a non-affective itself. For instance the resting state activity level in the sensory
stimulus into an affective one? I call this the “non-affective- cortex may interact with the resting state activity level in the
affective transformation.” The “non-affective-affective transfor- subcortical regions so that one may want to speak of rest–rest
mation” raises the question how it is possible that a stimulus is interaction. The above described results lend clear empirical sup-
suddenly associated with either Core Affect or primary process port to the assumption that such resting state activity in especially
affect. It is especially worthwhile to consider that the stimulus the midline regions is central for emotions and most likely for
of interoceptive, exteroceptive, or neural origin must be non- emotional feelings.
affective. Hence“non-affective-affective transformation” raises the And there is further interaction. As soon as an inter- or exte-
question: what kind of functional mechanisms and neural input roceptive stimulus enters the brain it interacts with the brain’s
the brain must provide in order to assign affect to the stimulus. resting state activity level thus yielding what can be called rest-
The question about the “non-affective-affective transforma- stimulus interaction (Northoff et al., 2010). Such rest-stimulus
tion” raises another issue. Both Panksepp and Russell consider interaction may be specified according to the stimulus type either
affect to be essentially subjective rather than objective. Panksepp rest-interceptive stimulus interaction or rest-exteroceptive stimu-
refers to primary process affect as subjective by describing it as lus interaction (which in the following I will describe as rest-intero
an “internal experience” while Russell describes Core Affect as and rest-extero interaction).
subjective in the sense of a private experience. Hence, Panksepp How do the three types of interaction, rest–rest, rest-intero,
distinguishes internal from external and Russell private from pub- and rest-extero relate to affective assignment and more specif-
lic when they characterize Core Affect or primary process affect ically to the non-affective-affective transformation and the
as subjective rather than objective. One should need to make a objective-subjective transformation? The resting state activity level

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 9

Northoff Emotion and consciousness

FIGURE 2 | The figure shows the relationship between intrinsic activity non-affective and objective. That rest-stimulus interaction leads to the
and stimuli (on the left) and emotional feeling (on the right). The intrinsic assignment of affect and subjectivity to the stimulus resulting in emotional
activity of the brain interacts with the stimuli that are by themselves feeling.

is different not only between different regions but even more This however is to neglect that the brain’s resting state can
importantly, different between different persons. This means that interact with itself, as for instance the resting state activity level
the same stimulus encounters a different brain in different per- in the subcortical circuits interacting with cortical regions. There
sons meaning it must interaction with a different resting state may thus be what could be called “rest–rest interaction” where the
activity level. Rest-stimulus interaction individualizes the stimu- neural stimuli of one particular region’s resting state may interact
lus and adapts its processing according to an individual brain’s with those of another region. Recent imaging data show that such
resting state activity level. Due to the individual resting state activ- rest–rest interactions do indeed occur (see Northoff et al., 2010 for
ity level and its impact on rest-stimulus interaction, the stimulus recent review). In the case of such rest–rest interaction, the resting
is processed in a very individual and ultimately private way. state activity level of one network is set against that of another
By individualizing and privatizing the stimuli with respect to network.
the brain’s actual resting state activity level, the originally objective
stimulus is transformed into a subjective one. Hence what I called SUBJECTIVE CHARACTER OF EMOTIONS
above objective-subjective transformation may correspond on a This has major implications for the conceptual characterization
functional level to rest-stimulus interaction. Any processing of the of emotions. Any stimulus, internal, external, or neural, cannot
stimulus, interoceptive or exteroceptive, in relation to the brain’s avoid but to interact with the brain’s resting state activity. If that
resting state activity level (and hence its neural stimuli) may pri- very same resting state activity individualizes and privatizes stim-
vatize and individualize the stimuli, and thereby transform it from uli and their encoding into neural activity, any emotions must
an objective to a subjective one. be individualized and privatized. That though means that any
Russell and Panksepp may now want to argue that this accounts emotions must necessarily be subjective meaning that it cannot
only for half of the story. Panksepp may say that this leaves avoid objective-subjective transformation. There is consequently
emotional affects as based on the stimuli from the BrainMind no emotion without emotional feeling with the latter being at the
itself and hence its neural stimuli out; this may be so because very core of the former. This nicely corresponds to what Russell
rest-stimulus interaction concerns only the interaction with describes as “Core affect” and Panksepp as “primary process affect”
intero- and exteroceptive stimuli. Hence, my assumption of rest- and, more generally as “BrainMind.”
stimulus interaction corresponding to objective-subjective trans- To empirically support this assumption, future studies are
formation may well account for what Panksepp calls homeostatic needed to test whether the preceding level of resting state activity
affects and sensory affects, but not emotional affects. predicts the degree of especially the subjective-experiential com-
Russell may want to make an even stronger point. My assump- ponent of emotions, i.e., the emotional feeling. I would hypothe-
tion of rest-stimulus interaction misses Core Affect altogether size that the preceding resting state activity predicts especially the
because Core Affect is neither related to interoceptive nor exte- subjective-experiential component of emotions. While other com-
roceptive stimuli. Instead the core affect precedes both kind ponents like the vegetative and the cognitive aspects of emotions
of stimuli that becoming relevant only in emotional episodes. may rather be predicted by the degree of stimulus-induced activity
Hence, my assumption that rest-stimulus interaction corresponds itself.
to objective-subjective transformation may hold for emotional One may finally raise the question how the here suggested role
episodes and emotional meta-experience but not for Core Affect of the resting state in objective-subjective transformation stands
itself. to the above proposed relational coding. I would argue that both

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 10

Northoff Emotion and consciousness

are well compatible. While above I focused on the relation between exteroceptive stimuli. How can exteroceptive stimuli be assigned
intero- and exteroceptive stimuli, I now extend the focus to include affect and how can they undergo the non-affective-affective trans-
the brain’s intrinsic activity and thus its neural stimuli into the formation? Very simple. They may be linked to interoceptive stim-
equation of relational coding. uli resulting in an intero-extero interaction. They would thereby
Let me be more specific. The incoming stimulus must be coded be valued, which in turn would lead to a non-affective-affective
in relation to the intrinsic activity level and thus relative to it. The transformation with the subsequent assignment of affect. Hence,
resulting neural activity must then be considered the integral of one may consider the interaction of stimuli of various origins
their interaction, i.e., rest-stimulus interaction, rather than being with specifically interoceptive stimuli from the body as a neces-
related to the stimulus alone. That though is possible only if neural sary condition for the non-affective-affective transformation. This
activity is coded in terms of a relation between stimulus and intrin- may apply to the brain’s neural stimuli with rest-intero interaction
sic activity as distinguished from neural coding of the stimulus by which then leads to what Russell described as Core Affect and
itself. I thus assume rest-stimulus and stimulus-rest interaction Panksepp as homeostatic affect. It may also apply to exterocep-
to presuppose relational coding in very much the same way as tive stimuli with intero-extero interaction that may then result in
the relation between intero- and exteroceptive stimuli is encoded what Russell characterized as emotional episodes and Panksepp as
into neural activity (see Northoff, 2012a for more details on the sensory affect.
question of neural coding).
DISSOCIATION BETWEEN SUBJECTIVITY AND AFFECTIVITY
“NON-AFFECTIVE-AFFECTIVE TRANSFORMATION” One may now be puzzled. I characterized objective-subjective
How about the second feature of affective assignment, that non- transformation by the interaction of any kind of stimulus with
affective-affective transformation? What functional mechanisms the brain’s resting state activity, i.e., its neural stimuli, so that any
correspond to the transformation of a non-affective stimulus into kind of rest-stimulus interaction will do the job. And I considered
an affective one? Panksepp (2010, p. 13) himself gives one hint in the interaction of any stimulus with interoceptive stimuli from the
this direction. He considers primary process affect to be intrinsi- body as being necessary for the non-affective-affective transforma-
cally valuative (in a wider sense as not being restricted to reward) in tion. Hence, both transformations, objective-subjective and non-
that it mirrors the value of environmental, bodily, and neural infor- affective-affective are characterized by interactions with different
mation for the organism. How can such value be generated, and stimuli, the brain’s neural stimuli and the body’s interoceptive
what kind of functional mechanisms are necessary in order to value stimuli.
stimuli of different origin, exteroceptive, interoceptive, or neural? As on a psychological level where affectivity and subjectivity
In order for stimuli of various origins to be valued for the organ- co-occur, non-affective-affective, and objective-subjective trans-
ism, they must be related to the organism itself, including its body formations also co-occur in the “normal” case. There is interaction
and brain. More specifically, exteroceptive stimuli from the envi- with the body’s interoceptive stimuli (e.g., intero-extero interac-
ronment need to be related to the brain’s neural stimuli leading to tion), and there is interaction with the brain’s resting state and thus
rest-extero interaction and the body’s interoceptive stimuli lead- its neural stimuli (e.g., rest-intero and rest-extero interaction).
ing to intero-extero interaction. The same holds for interoceptive This means that affectivity and subjectivity are co-constituted,
stimuli which need to be related to the brain’s neural stimuli thus which is reflected in both Panksepp and Russell definitions of
requiring rest-intero interaction. Finally, as demonstrated above, affect by.
the brain’s resting state activity itself may be valued when rest–rest If one interaction takes over at the expense of the respective
interaction occur. other, the co-constitution between affectivity and subjectivity may
How does affect enter these various interactions? Russell tells become dysbalanced. This is, for instance, the case in schizophre-
us that Core Affect is continuously present even in the absence nia where rest-intero and rest-extero interactions may be reduced
of exteroceptive stimuli. Unlike exteroceptive stimuli which arise leading to an abnormal loss of subjectivity (Northoff and Qin,
more episodically, there is continuous interoceptive input and thus 2011). There is thus still non-affective-affective transformation
continuous rest-intero interaction in the brain. Due to the con- while the objective-subjective transformation seems to fail: These
tinuous presence of the body, continuous interoceptive input and patients thus still experience emotional feelings while their respec-
subsequent continuous rest-intero interaction cannot be avoided. tive contents are no longer experienced as subjective but objective.
One may consequently consider rest-intero interaction as one While the reverse seems to be the case in depression, where
possible candidate functional mechanism that may correspond to rest-intero interaction seems to predominate over intero-extero
what Russell describes as Core Affect. It is by the continuous neural interaction (Alcaro et al., 2010; Northoff et al., 2011). In the most
processing of the body’s interoceptive stimuli against the brain’s extreme case, depressed patients say that they no longer feel any
neural stimuli that affect may be generated. Hence, interaction of emotion, the feeling of non-feeling. Hence, non-affective-affective
the interoceptive stimuli with the neural stimuli may transform transformation may be blocked while at the same time this state
the originally non-affective interoceptive stimulus into an affec- is experienced as highly subjective implying objective-subjective
tive one. The hypothesis is thus that rest-intero interaction may transformation. The cases of depression and schizophrenia thus
correspond on the functional level to the non-affective-affective indicate the possibility of dissociation between both forms of
transformation and thus to what Russell described as Core Affect. transformation.
However, there is not only Core Affect but also emotional Interoceptive processing and consecutively intero-extero inter-
episodes (Russell) or sensory affect (Panksepp) in relation to action may also be altered or disrupted in alexithymia that

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 11

Northoff Emotion and consciousness

concerns the inability to identify and describe emotional feeling. Due to the very basic and foundational character of the brain-
The exteroceptive stimuli and their respective contents can then body-environment relation, the relational concept considers emo-
no longer be associated with emotional feelings: While the con- tional (and existential) feelings basic and primary for emotions,
tents are experienced as subjective (due to functioning rest-intero i.e., feelings are then the “core nucleus” of emotions. This is very
and rest-extero interactions), they are not assigned emotional feel- much in line with the neuroscientific approach by Panksepp (1998,
ing (due to deficient intero-extero interaction). Empirically this is 2005) who assumes what he calls “primary affective conscious-
supported by a recent study that shows the degree of interoceptive ness.” He regards “primary affective consciousness” as basic and
awareness to predict the degree of alexithymia with high intero- crucial for all forms of subjective experience and thus for con-
ceptive awareness going along with a low degree of alexithymia sciousness in general. Analogously, the relational view considers
(Herbert et al., 2011). our relation to the world primary, basic and crucial to our subjec-
tive experience or, as Ratcliffe would probably say, the relation is
existential.
CONCEPTUAL IMPLICATIONS: EMOTIONAL FEELING AND
CONSCIOUSNESS
NEURO-PHENOMENAL APPROACH TO EMOTIONAL FEELING
RELATIONAL APPROACH TO EMOTIONAL FEELING
Since the relational concept characterizes the brain-body-
How should emotional feelings be conceptualized on the basis
environment as basic, primary, and constitutive of feelings, the
of the intero-exteroceptive relational model of neural coding?
here advanced relational concept of emotional feelings seems to
What we subjectively experience as emotional feeling is thus not
complement the empirical approach by Panksepp in conceptual
so much mere perception of an interoceptive stimulus like the
regard. Feelings and thus affective consciousness can only be pri-
heartbeat perception but rather the relation between intero- and
mary and basic, as Panksepp claims, because they are our relation
exteroceptive stimulus processing relative to our brain’s intrin-
to the world. Another complementary point is Panksepp’s (and
sic activity. Emotional feelings can no longer be determined in
other authors like M. Sheets-Johnstone, N. Humphrey and R.
an interoceptive-based way as perceptions of physiological body
Ellis) insistence on the close linkage between motor function
changes. Instead, emotional feelings may better be described in
and emotional feeling, i.e., the primary motor basis of affective
an neural-intero-exteroceptive relational way thus focusing more
consciousness.
on the relation between brain, body and environment than on
In contrast to Damasio (2010), who opts for a rather sensory-
either the body or the environment itself 3 . What is constitutive
based view of emotional feeling, Panksepp (and others like Ellis,
of emotional feelings is thus the relation between brain, body,
2005) argues for a primary “motor view” of affective consciousness
and environment so that feelings reflect the respective person’s
and emotional feeling because all presumably involved subcortical
relationship to the world.
regions like the PAG, the colliculi, etc. show strong connections
This is paradigmatically reflected in what the philosopher Rat-
to the motor system receiving motor afferences from and send-
cliffe (2005, 2008) calls existential feelings. Based on Heidegger, he
ing out motor efferences to other cortical and subcortical regions.
describes existential feelings as feelings that characterize our rela-
Accordingly, Panksepp (and others like Ellis, 2005) claims that
tion to the world, i.e., as ways of “finding ourselves in the world.”
there is intrinsic linkage between motor action and emotional
This is also pointed out by Solomon (2004, pp. 77–78, 84) in a more
feeling resulting in what may be described as “I act, therefore I
recent writing when he claims for “an existential notion of emo-
feel.” The assumption of motor underpinnings as being crucial to
tions” which he considers to be “subjective engagements within the
emotional feeling is well compatible with the relational concept.
world4 .”For instance, different existential feelings characterize dif-
The here suggested relational approach also needs to be distin-
ferent relations to the world like feelings of homeliness, separation,
guished from cognitive approaches. Cognitive approaches focus
belonging, power, control, etc. Most important, emotional feelings
on the awareness and thus reflection of emotional and cogni-
like anger, grief, etc. presuppose existential feelings so that both
tive contents thus presupposing access or reflective consciousness,
emotional and existential feelings can be characterized as rela-
the awareness of subjective experience. For that various cognitive
tional. If so, the body itself may only be considered the medium
functions are assumed to be necessary. This is different in the rela-
through which feelings can be constituted. Feelings are the relation
tional approach that focus on phenomenal consciousness and thus
between person/body and environment rather than some percep-
on subjective experience itself and how it is generated and trans-
tion of either bodily or environmental changes; in other terms,
formed into a phenomenal state (see below) on the basis of the
feelings are this relation implying that this relationship is felt.
brain’s neuronal states.
The relational approach can thus be characterized as “neuro-
3 This is well compatible with the relational approach to meaning and personal
phenomenal approach” rather than “neuro-cognitive approach”
significance as suggested by Ben-Ze’ev (1993, 2000) that undercuts the traditional
(see Northoff, 2012b). Since the cognition, i.e., awareness and
assumption that higher-order cognitive functions are necessary to give meaning and reflection, of subjective experience and its contents presup-
personal significance to otherwise meaningless and personally insignificant sense poses its generation, I assume the “neuro-phenomenal approach”
data. to be more basic and prior to the neuro-cognitive approach.
4 One may off course argue that we can have subjective experience without emotion
Future studies may therefore want to investigate how the
in for instance so-called “cold” cognitions. “Cold” cognitions may however be con-
sidered just as an extreme case on a continuum in the relationship between emotion
here described neuronal processes of non-affective-affective and
and cognition where feelings may still be involved in the background though being objective-subjective transformation impact cognitive functions
maximally suppressed. and their respective neural substrates.

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 12

Northoff Emotion and consciousness

FIGURE 3 | The figure shows the relationship between emotional assigned to the intero- and exteroceptive stimuli. This in turn makes
feeling and phenomenal consciousness. By interacting with the possible the generation of emotional feeling and phenomenal
brain’s intrinsic activity via relational coding affect and subjectivity is consciousness.

EMOTIONS AND CONSCIOUSNESS consciousness (see below for further explication). In contrast,
How is the transformation of the brain’s neuronal states into the “realizing what emotion one feels” might be considered to impli-
phenomenal states of consciousness possible? The relational con- cate higher-order cognitive functions and thus be associated with
cept presupposes bilaterally dependent and constitutive linkage what has been called reflective consciousness.
between brain, body, and environment. Mere linkage by sensory By considering feeling as constitutive of emotion and phenom-
function would result in unilateral and rather instrumental linkage enal consciousness, the relational concept of emotional feeling
where the person/body cannot directly impact the environment. argues against the explanation of feelings in terms of higher-order
It is only by motor function that the person/body becomes intrin- cognitive and reflective functions mirroring what is called reflec-
sically anchored in and non-instrumentally, i.e., constitutionally tive consciousness. Roughly, reflective consciousness describes the
linked to the environment. In other terms, motor function must person’s awareness that it has subjective experience and thus phe-
be considered the empirical means by means of which what I nomenal consciousness – reflective consciousness may thus focus
conceptually described as relational becomes possible. Panksepp’s on higher-order cognitive functions.
insistence on motor underpinnings of emotional feelings may Phenomenal consciousness, in contrast, does not describe cog-
thus be considered complementary to the here advanced relational nitive and behavioral aspects associated with subjective experience.
concept of emotional feeling (Figure 3). Instead, it focuses on the subjective-experiential aspect itself that
Once emotional feelings are considered to be the core nucleus is described as the “phenomenal aspect” (Chalmers, 1995; Block,
of both emotions and consciousness, the often made distinction 1996). A number of alternative terms and phrases pick out approx-
between “having an emotion” and “feeling an emotion” becomes imately the same core property of phenomenal consciousness.
no longer applicable. Following Bennett and Hacker (2003, pp. These include “qualia,” “phenomenology,” “subjective experience,”
210–214), there is no principal distinction between “having an and “what it is like” which, despite subtle differences, we here con-
emotion” and “feeling an emotion” since, as Kripke (1972) already sider to describe the same phenomenon for pragmatic purposes. I
pointed out, the having of pain is to be identified with the feel- characterize emotional feeling by “qualia” and “what it is like” thus
ing of pain. Either we have pain and subjectively experience or presupposing phenomenal consciousness.
feel pain or we do not feel any pain and then we have no pain. The here proposed relational account is well in accordance with
“Having an emotion” is consequently to be identified with “feel- Peter Goldie’s approach who emphasizes the phenomenal, e.g.,
ing an emotion” and their distinction remaining untenable and unreflective, qualitative, and“what it is like”character of emotional
implausible. feeling (Goldie, 2000, pp. 68–69). Goldie (2000, pp. 1–2, 41) argues
According to Bennett and Hacker (2003, p. 214), the main that the phenomenal character of feelings is due to the involve-
difference should better be drawn between “feeling an emotion,” ment of a point of view, a perspective, by means of which they
as being identical with “having an emotion,” and “realizing what become “fundamentally personal.” The relational concept claims
emotion one feels.”“Feeling an emotion” might then indicate sub- that such personal point of view is established by constituting the
jective experience and thus what currently is called phenomenal relationship between brain, body, and environment and thus by

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 13

Northoff Emotion and consciousness

constituting feelings be they existential or emotional. How such concept of emotional feeling is empirically plausible, even inte-
personal point can be established by relating brain and body to roceptive awareness should implicate brain regions that process
the environment remains to be discussed in detail which how- exteroceptive stimuli. Both, e.g., intero- and exteroceptive brain
ever is beyond the scope of this paper (see Northoff, 2004, 2012b; regions, should then also be closely linked to each other in terms
Northoff and Bermpohl, 2004; Northoff et al., 2006). of anatomical, i.e., structural and functional connectivity.
Finally, the here proposed neuronal mechanisms underlying Human brain imaging data show strong involvement of the
especially the subjective nature of emotions may be relevant for VMPFC and other aCMS in emotional feelings. These regions can
consciousness in general. The yet to be specified and defined be characterized by strong convergence between intero- and exte-
neuronal mechanisms underlying rest-stimulus interaction are roceptive inputs as well as of both with the brain’s high intrinsic
assumed to be central for the subjective component. If so they must activity, its resting state activity. This presupposes what I describe
be regarded necessary of consciousness in general that is essentially as the neural-intero-exteroceptive relational mode of neural cod-
defined as subjective. Even if not sufficient by themselves as neural ing rather than interoceptive-based translational neural coding
correlates of consciousness (NCC), specific yet unknown ways of (see also Northoff, 2012a). In short I assume relational coding to
rest-stimulus interaction must then be regarded a necessary or be the predominant neural code that allows to link emotions to
predisposing condition of consciousness. One may consequently brain, body, and environment. Emotions and emotional feelings
want to speak of neural predispositions of consciousness (NPC) may then be considered, metaphorically speaking, the bridge or
as distinguished from the NCC (see Northoff, 2012b). glue between brain, body, and environment.
The intrinsic linkage between brain, body, and environment
CONCLUSION accounts for the subjective and affective nature of emotional feel-
The often favored James–Lange theory and many current neu- ings. By being processed in the brain relative to its intrinsic activity
roscientific approaches that consider feeling as mere perception (at least in the human brain as it is designed) emotions cannot
of bodily changes and thus as “embodied” may be extended by avoid becoming subjective and affective. The subjective and affec-
considering the crucial role of the environment in directly con- tive components must therefore be regarded intrinsic to and thus
stituting emotional feelings. I therefore suggested in this paper defining features of emotions. As such emotions and emotional
to complement the embodied concept of emotional feelings by a feeling may be considered paradigmatic cases of consciousness
relational concept that assumes emotional feelings to be consti- in general which in the current neuroscientific and philosophical
tuted by the brain-body-environment relationship. The relational debate is rather often neglected (see also Northoff, 2012b).
concept assumes that the environment and the brain itself have
not only instrumental and thus indirect impact on emotional feel- ACKNOWLEDGMENTS
ings via the body but also a direct, e.g., non-instrumental and thus I am thankful to Jaak Panksepp, Peter Goldie, and Aaron Ben-Ze’ev
constitutional role in constituting emotional feelings. for stimulating discussions about the philosophy of emotions as
The present paper focuses on whether such relational con- well as the reviewers and editors for helpful comments. Financial
cept of emotional feelings is compatible with current empirical support is acknowledged from CIHR, EJLB-CIHR, Michael Smith
data on the neuroscience of emotion processing. If the relational Foundation, and HDRF-ISAN.

REFERENCES Ben-Ze’ev, A. (1993). The Perceptual Colombetti, G. (2008). “Emotion, Craig, A. D. (2004). Human feelings:
Alcaro, A., Panksepp, J., Witczak, J., System – A Philosophical and Psycho- sense-making and enaction,” in why are some more aware than oth-
Hayes, D. J., and Northoff, G. logical Perspective. New York: Peter Enaction: Towards A New Paradigm ers? Trends Cogn. Sci. (Regul. Ed.) 8,
(2010). Is subcortical-cortical mid- Lang Publishing Inc. for Cognitive Science, eds J. Stewart, 239–241.
line activity in depression mediated Ben-Ze’ev, A. (2000). The Subtlety of O. Gapenne, and E. Di Paolo (Cam- Craig, A. D. (2005). Forebrain emo-
by glutamate and GABA? A cross- Emotions. Cambridge, MA: MIT bridge, MA: MIT Press), 134–150. tional asymmetry: a neuroanatom-
species translational approach. Neu- Press. Colombetti, G., and Thompson, E. ical basis? Trends Cogn. Sci. (Regul.
rosci. Biobehav. Rev. 34, 592–605. Block, N. (1996). How can we find the (2005). Enacting emotional inter- Ed.) 9, 566–571.
Barbas, H. (2000). Complementary neural correlate of consciousness? pretations with feeling. Behav. Brain Craig, A. D. (2009). How do you feel
roles of prefrontal cortical regions in Trends Neurosci. 19, 456–459. Sci. 28, 200–201. now? The anterior insula and human
cognition, memory, and emotion in Carmichael, S. T., and Price, J. L. (1996). Colombetti, G., and Thompson, E. awareness. Nat. Rev. Neurosci. 10,
primates. Adv. Neurol. 84, 87–110. Connectional networks within the (2007). “The feeling body: towards 59–70.
Barbas, H. (2004). Dead tissue, living orbital and medial prefrontal cor- an enactive approach to emotion,” in Craig, A. D. (2010). The sentient self.
ideas: facts and theory from neu- tex of macaque monkeys. J. Comp. Body in Mind, Mind in Body: Devel- Brain Struct. Funct. 214, 563–577.
roanatomy. Cortex 40, 205–206. Neurol. 371, 179–207. opmental Perspectives on Embodi- Craig, A. D. (2011). Significance of the
Bechara, A. (2004). The role of emo- Chalmers, D. J. (1995). The puzzle of ment and Consciousness, eds W. F. insula for the evolution of human
tion in decision-making: evidence conscious experience. Sci. Am. 273, Overton, U. Müller, and J. Newman awareness of feelings from the body.
from neurological patients with 80–86. (New York: Lawrence Erlbaum), 86– Ann. N. Y. Acad. Sci. 1225, 72–82.
orbitofrontal damage. Brain Cogn. Ciaramidaro, A., Adenzato, M., Enrici, 98. Critchley, H. D. (2005). Neural mech-
55, 30–40. I., Erk, S., Pia, L., Bara, B. G., and Craig, A. D. (2002). How do you feel? anisms of autonomic, affective, and
Bechara, A., and Naqvi, N. (2004). Lis- Walter, H. (2007). The intentional Interoception: the sense of the phys- cognitive intergration. J. Comp. Neu-
tening to your heart: interoceptive network: how the brain reads vari- iological condition of the body. Nat. rol. 493, 154–166.
awareness as a gateway to feeling. eties of intentions. Neuropsychologia Rev. Neurosci. 3, 656–666. Critchley, H. D., Wiems, S. W., Rot-
Nat. Neurosci. 7, 102–103. 45, 3105–3113. Craig, A. D. (2003). Interoception: the shtein, P., Oehman, A., and Dolan, R.
Bennett, M. R., and Hacker, P. (2003). Colombetti, G. (2005). Appraising sense of the physiological condition J. (2004). Neural systems supporting
Philosophical Foundations of Neuro- valence. J. Conscious. Stud. 12, of the body. Curr. Opin. Neurobiol. interoceptive awareness. Nat. Neu-
science. Oxford: Blackwell. 103–126. 13, 500–505. rosci. 7, 189–195.

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 14

Northoff Emotion and consciousness

Damasio, A. (2003). Feelings of emo- neuroanatomy of the human Northoff, G., Wiebking, C., Feinberg, information analysis. J. Cogn. Neu-
tion and the self. Ann. N. Y. Acad. orbitofrontal cortex: evidence T., and Panksepp, J. (2011). The rosci. 11, 300–311.
Sci. 1001, 253–261. from neuroimaging and neu- “resting-state hypothesis” of major Russell, J. A. (2003). Core affect and
Damasio, A. R. (1999). The Feeling of ropsychology. Prog. Neurobiol. 72, depressive disorder-a translational the psychological construction of
What Happens: Body and Emotion 341–372. subcortical-cortical framework for a emotion. Psychol. Rev. 110, 145–172.
in the Making of Consciousness. New Kripke, S. (1972). “Naming and system disorder. Neurosci. Biobehav. [Review].
York: Harcourt Brace. necessity,” in Semantics of Natural Rev. 35, 1929–1945. Schachter, S., and Singer, J. E. (1962).
Damasio, A. R. (2010). Self Comes to Language, 2nd Edn, eds D. David- Ongur, D., and Price, J. L. (2000). The Cognitive, social, and physiologi-
Mind: Constructing the Conscious son and G. Harman (Dordrecht: organization of networks within the cal determinants of emotional state.
Brain. New York: Harcourt Brace. Reidel Publishing Company), orbital and medial prefrontal cortex Psychol. Rev. 69, 379–399.
Ellis, R. D. (2005). Curious Emotions: 253–355. of rats, monkeys and humans. Cereb. Schilbach, L., Bzdok, D., Timmermans,
Roots of Consciousness and Personal- LeDoux, J. E. (2002). Synaptic Self: How Cortex 10, 206–219. B., Fox, P. T., Laird, A. R., Vogeley,
ity in Motivated Action. New York: Our Brains Become Who We Are. New Panksepp, J. (1998). Affective Neuro- K., and Eickhoff, S. B. (2012). Intro-
John Benjamin Publisher. York: Viking. science: The Foundations of Human spective minds: using ALE meta-
Eryilmaz, H., Van De Ville, D., Schwartz, Nagai, Y., Critchley, H. D., Featherstone, and Animal Emotions. New York: analyses to study commonalities in
S., and Vuilleumier, P. (2011). E., Trimble, M. R., and Dolan, R. J. Oxford University Press. the neural correlates of emotional
Impact of transient emotions on (2004). Activity in ventromedial pre- Panksepp, J. (2005). Affective con- processing, social & unconstrained
functional connectivity during sub- frontal cortex covaries with sympa- sciousness: core emotional feelings cognition. PLoS ONE 7, e30920.
sequent resting state: a wavelet cor- thetic skin conductance level: a phys- in animals and humans. Conscious. doi:10.1371/journal.pone.0030920
relation approach. Neuroimage 54, iological account of a “default mode” Cogn. 14, 30–80. Schore, A. N. (2003). Affect Regulation
2481–2491. of brain function. Neuroimage 22, Panksepp, J. (2010). Affective con- and the Repair of the Self. New York:
Farb, N. A., Segal, Z. V., and Anderson, 243–251. sciousness in animals: perspectives W.W. Norton.
A. K. (2012). Attentional modula- Niedenthal, P. M. (2007). Embodying on dimensional and primary process Solomon, R. C. (2004). Thinking About
tion of primary interoceptive and emotion. Science 316, 1002–1005. emotion approaches. Proc. Biol. Sci. Feeling. Contemporary Philosophers
exteroceptive cortices. Cereb. Cortex [Review]. 277, 2905–2907. on Emotions. New York: Oxford Uni-
[Epub ahead of print]. Niedenthal, P. M., Barsalou, L. W., Phan, K. L., Wager, T., Taylor, S. F., versity Press.
Fliessbach, K., Weber, B., Trautner, P., Winkielman, P., Krauth-Gruber, S., and Liberzon, I. (2002). Functional Sreenivas, S., Boehm, S. G., and Linden,
Dohmen, T., Sunde, U., Elger, C. and Ric, F. (2005). Embodiment neuroanatomy of emotion: a meta- D. E. (2012). Emotional faces and
E., and Falk, A. (2007). Social com- in attitudes, social perception, and analysis of emotion activation stud- the default mode network. Neurosci.
parison affects reward-related brain emotion. Pers. Soc. Psychol. Rev. 9, ies in PET and fMRI. Neuroimage 16, Lett. 506, 229–234.
activity in the human ventral stria- 184–211. [Review]. 331–348. Tsuchiya, N., and Adolphs, R. (2007).
tum. Science 318, 1305. Northoff, G. (2004). Why do we need Pollatos, O., Kirsch,W., and Schandry, R. Emotion and consciousness. Trends
Goldie, P. (2000). The Emotions: A Philo- a philosophy of the brain? Trends (2005). On the relationship between Cogn. Sci. (Regul. Ed.) 11, 158–167.
sophical Exploration. Oxford: Oxford Cogn. Sci. (Regul. Ed.) 8, 484–485. interoceptive awareness, emotional Veer, I. M., Oei, N. Y., Spinhoven,
University Press. Northoff, G. (2011). Neuropsychoanaly- experience and brain processes. P., van Buchem, M. A., Elzinga,
Grimm, S., Schmidt, C. F., Bermpohl, sis in Practice. Brain Self and Objects. Brain Res. Cogn. Brain Res. 25, B. M., and Rombouts, S. A.
F., Heinzel, A., Dahlem, Y., Wyss, Oxford: Oxford University Press. 948–962. (2011). Beyond acute social stress:
M., Hell, D., Boesiger, P., Boeker, Northoff, G. (2012a). Unlocking the Pollatos, O., Herbert, B. M., Matthias, increased functional connectivity
H., and Northoff, G. (2006). Segre- Brain. Vol. I: Coding. Oxford: Oxford E., and Schandry, R. (2007a). Heart between amygdala and cortical mid-
gated neural representation of dis- University Press. rate response after emotional picture line structures. Neuroimage 57,
tinct emotion dimensions in the pre- Northoff, G. (2012b). Unlocking the presentation is modulated by intero- 1534–1541.
frontal cortex-an fMRI study. Neu- Brain. Volume II: Consciousness. ceptive awareness. Int. J. Psychophys- Wicker, B., Keysers, C., Plailly, J., Royet,
roimage 30, 325–340. Oxford: Oxford University Press. iol. 63, 117–124. J. P., Gallese, V., and Rizzolatti, G.
Herbert, B. M., Herbert, C., and Pol- Northoff, G., and Bermpohl, F. (2004). Pollatos, O., Traut-Mattausch, E., (2003). Both of us disgusted in My
latos, O. (2011). On the relation- Cortical midline structures and the Schroeder, H., and Schandry, R. insula: the common neural basis of
ship between interoceptive aware- self. Trends Cogn. Sci. (Regul. Ed.) 8, (2007b). Interoceptive awareness seeing and feeling disgust. Neuron
ness and alexithymia: is interocep- 102–107. mediates the relationship between 40, 655–664.
tive awareness related to emotional Northoff, G., Heinzel, A., de Greck, M., anxiety and the intensity of unpleas- Wiebking, C., de Greck, M., Dun-
awareness? J. Pers. 79, 1149–1175. Bermpohl, F., Dobrowolny, H., and ant feelings. J. Anxiety Disord. 21, can, N. W., Heinzel, A., Tempel-
Hurley, S. (1998). Consciousness in Panksepp, J. (2006). Self-referential 931–943. mann, C., and Northoff, G. (2011).
Action. Cambridge, MA: Harvard processing in our brain – a meta- Price, J. L. (1999). Prefrontal cortical Are emotions associated with activ-
University Press. analysis of imaging studies on the networks related to visceral function ity during rest or interoception?
Hurliman, E., Nagode, J. C., and Pardo, self. Neuroimage 31, 440–457. and mood. Ann. N. Y. Acad. Sci. 877, An exploratory fMRI study in
J. V. (2005). Double dissociation Northoff, G., and Musholt, K. (2006). 383–396. healthy subjects. Neurosci. Lett. 491,
of exteroceptive and interoceptive How can searle avoid property Dual- Ratcliffe, M. J. (2005). The feeling 87–92.
feedback systems in the orbitofrontal ism? Epistemic-ontological infer- of being. J. Conscious. Stud. 12, Zajonc, R. (2000). “Feeling and think-
and ventromedial prefrontal cor- ence and autoepistemic limitation. 43–60. ing: closing the debate over the
tex of humans. J. Neurosci. 25, Philos. Psychol. 19, 1–17. Ratcliffe, M. J. (2008). Feelings of Being: independence of affect,” in Feeling
4641–4648. Northoff, G., and Qin, P. (2011). How Phenomenology, Psychiatry and the and Thinking: The Role of Affect in
James, W. (1884). What is an emotion? can the brain’s resting state gener- Sense of Reality. Oxford: Oxford Uni- Social Cognition, ed. J. Forgas (Cam-
Mind 9, 185–205. ate adutiroy hallucinations? A rest- versity Press. bridge: Cambridge University Press),
Kringelbach, M. L. (2005). The human ing state hypothesis. Schizophr. Res. Rolls, E. T. (2000). The orbitofrontal 45–65.
orbitofrontal cortex: linking reward 127, 202–214. cortex and reward. Cereb. Cortex 10, Zajonc, R. B. (1998). “Emotions,” in The
to hedonic experience. Nat. Rev. Northoff, G., Qin, P., and Nakao, T. 284–294. Handbook of Social Psychology, Vol.
Neurosci. 6, 691–702. [Review]. (2010). Rest-stimulus interaction in Rolls, E. T., Tovee, M. J., and Panz- 1, eds D. Gilbert, S. T. Fiske, and
Kringelbach, M. L., and Rolls, the brain. A review. Trends Neurosci. eri, S. (1999). The neurophysiol- G. Lindzey (Boston: McGraw-Hills),
E. T. (2004). The functional 33, 277–284. [Review]. ogy of backward visual masking: 591–632.

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 15

Northoff Emotion and consciousness

Conflict of Interest Statement: The Received: 19 March 2012; paper pend- approach. Front. Psychology 3:303. doi: the terms of the Creative Com-
author declares that the research ing published: 25 April 2012; accepted: 02 10.3389/fpsyg.2012.00303 mons Attribution License, which per-
was conducted in the absence August 2012; published online: 31 August This article was submitted to Frontiers in mits use, distribution and reproduction
of any commercial or financial 2012. Emotion Science, a specialty of Frontiers in other forums, provided the original
relationships that could be con- Citation: Northoff G (2012) From in Psychology. authors and source are credited and sub-
strued as a potential conflict of emotions to consciousness – a neuro- Copyright © 2012 Northoff. This is ject to any copyright notices concerning
interest. phenomenal and neuro-relational an open-access article distributed under any third-party graphics etc.

Frontiers in Psychology | Emotion Science August 2012 | Volume 3 | Article 303 | 16

Northoff Emotion and consciousness

APPENDIX
GLOSSARIUM
Coding: Formal measure according to which stimuli are encoded
into neural activity.
Consciousness: Subjective experience characterized by “what
it is like” and a point of view. Referring here mainly to phe-
nomenal consciousness as distinguished from access or reflective
consciousness.
Embeddedness: Constitutional (as distinguished from mere
modulatory) dependence of consciousness and emotional feeling
on the (social) environment.
Embodiment: Constitutional (as distinguished from mere
modulatory) dependence of consciousness and emotional feeling
on the body and its sensorimotor functions.
Exteroceptive stimuli: Input into the brain from the environ-
ment.
Interoceptive stimuli: Input into the brain from the own body.
Neural stimuli: Input into the brain from other regions and
time points within the brain itself.
Non-affective-affective transformation: Processes that underlie
FIGURE A1 | The figure illustrates schematically the relevant midline
the assignment of affect to a primarily non-affective stimulus that regions in the cortex. The image is a sagittal slice of the brain take in its
thereby becomes transformed into an affective stimulus. midline. MOPFC, medial orbitofrontal cortex; VMPFC, ventromedial
Objective-subjective transformation: Processes that underlie prefrontal cortex; DMPFC, dorsomedial prefrontal cortex; PACC, perigenual
the assignment of subjectivity to a primarily objective stimulus anterior cingulate cortex; SACC, supragenual anterior cingulate cortex; PCC,
posterior cingulate cortex; RSC, retrosplenial cortex; MPC, medial parietal
that thereby becomes transformed into a subjective stimulus.
cortex.
Relational coding: Coding of different stimuli in relation to
each other into neural activity in the brain.
Resting state: The state of the brain in the absence of any spe- Rest-intero interaction: Interaction of the brain’s resting state
cific stimulus from outside the brain as from the body or the activity with interoceptive stimuli from the own body.
environment. Rest-stimulus interaction: Term for the interaction of intero-
Rest–rest interaction: Changes in neural activity in the resting ceptive and/or exteroceptive stimuli with the brain’s resting state
state. These changes may occur between different regions and/or activity.
across time as fluctuations in the spontaneous activity of the brain. Translational coding: Coding of each stimulus by itself into
Rest-extero interaction: Interaction of the brain’s resting state neural activity in the brain with subsequent translation of the
activity with exteroceptive stimuli from the environment. different neural activities into each other.

www.frontiersin.org August 2012 | Volume 3 | Article 303 | 17