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Spatial navigation and causal analysis in a brain-based device modeling cortical-hippocampal interactions

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Abstract

We describe Darwin X, a physical device that interacts with a real environment, whose behavior is guided by a simulated nervous system incorporating aspects of the detailed anatomy and physiology of the hippocampus and its surrounding regions. This brain-based device integrates cues from its environment and solves a spatial memory task. The responses of simulated neuronal units in the hippocampal areas during its exploratory behavior are comparable to place cells in the rodent hippocampus and emerged by associating sensory cues during exploration. To identify different functional hippocampal pathways and their influence on behavior, we employed a time series analysis that distinguishes causal interactions within and between simulated hippocampal and neocortical regions while the device is engaged in a spatial memory task. Our analysis identified different functional pathways within the neural simulation and prompts novel predictions about the influence of the perforant path, the trisynaptic loop and hippocampal-cortical interactions on place cell activity and behavior during navigation. Moreover, this causal time series analysis may be useful in analyzing networks in general.

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References

  • Akaike, H. (1974) A new look at the statistical model identification. IEEE Trans. Automat. Control 19, 716–723.

    Article  Google Scholar 

  • Almassy, N., Edelman, G. M., and Sporns, O. (1998) Behavioral constraints in the development of neuronal properties: a cortical model embedded in a real-world device. Cereb. Cortex 8, 346–361.

    Article  PubMed  CAS  Google Scholar 

  • Amaral, D.G., Ishizuka, N., and Claiborne, B. (1990) Neurons, numbers and the hippocampal network. In: Progress in Brain Research. Ottersen, O.P. (ed.) ElsevierScience, Amsterdam, pp. 1–11.

    Google Scholar 

  • Arleo, A. and Gerstner, W. (2000) Modeling rodent head-direction cells and place cells for spatial learning in bio-mimetic robotics. Paper presented at: From Animals to Animats 6: Proceedings of the Sixth International Conference on Simulation of Adaptive Behavior, MIT Press, Paris, France.

    Google Scholar 

  • Aston-Jones, G. and Bloom, F. E. (1981) Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J. Neurosci. 1, 887–900.

    PubMed  CAS  Google Scholar 

  • Bachelder, I. A. and Waxman, A. M. (1995) A view-based neurocomputational system for relational map-making and navigation in visual environments. Auton. Syst. 16, 267–289.

    Article  Google Scholar 

  • Battaglia, F. P., Sutherland, G. R., and McNaughton, B. L. (2004) Local sensory cues and place cell directionality: Additional evidence of prospective coding in the hippocampus. J. Neurosci. 24, 4541–4550.

    Article  PubMed  CAS  Google Scholar 

  • Bernard, C. and Wheal, H. V. (1994) Model of local connectivity patterns in CA3 and CA1 areas of the hippocampus. Hippocampus 4, 497–529.

    Article  PubMed  CAS  Google Scholar 

  • Bernasconi, C. and Konig, P. (1999) On the directionality of cortical interactions studied by structural analysis of electrophysiological recordings. Biol. Cybern. 81, 199–210.

    Article  PubMed  CAS  Google Scholar 

  • Bienenstock, E. L., Cooper, L. N., and Munro, P. W. (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32–48.

    PubMed  CAS  Google Scholar 

  • Blum, K. I. and Abbott, L. F. (1996) A model of spatial map formation in the hippocampus of the rat. Neural Comput. 8, 85–93.

    Article  PubMed  CAS  Google Scholar 

  • Boudjellaba, B., Dufour, J.-M., and Roy, R. (1992) Testing causality between two vextors in multivariate ARMA models. J. Am. Stat. Assoc. 87, 1082–1090.

    Article  Google Scholar 

  • Brovelli, A., Ding, M., Ledberg, A., Chen, Y., Nakamura, R., and Bressler, S. L. (2004) Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc. Natl. Acad. Sci. USA 101, 9849–9854.

    Article  PubMed  CAS  Google Scholar 

  • Brun, V. H., Otnass, M. K., Molden, S., et al. (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243–2246.

    Article  PubMed  CAS  Google Scholar 

  • Burgess, N., Donnett, J. G., Jeffery, K. J., and O’Keefe, J. (1997) Robotic and Neural Simulation of the Hippocampus and Rat Navigation. Biol. Sci. 352, 1535–1543.

    Article  CAS  Google Scholar 

  • Chavarriaga, R., Strösslin, T., Sheynikhovich, D., and Gerstner, W. (2005) A computational model of parallel navigation systems in rodents. Neuroinformatics 3(3), in press.

  • Edelman, G. M. (1987) Neural Darwinism: The Theory of Neuronal Group Selection. Basic Books, Inc., New York.

    Google Scholar 

  • Edelman, G. M., Reeke, G. N., Gall, W. E., Tononi, G., Williams, D., and Sporns, O. (1992) Synthetic neural modeling applied to a real-world artifact. Proc. Natl. Acad. Sci. USA 89, 7267–7271.

    Article  PubMed  CAS  Google Scholar 

  • Farah, M. (1994) Neuropsychological inference with an interactive brain: A critique of the locality assumption. Behav. Brain Sci. 17, 43–61.

    Article  Google Scholar 

  • Ferbinteanu, J. and Shapiro, M. L. (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227–1239.

    Article  PubMed  CAS  Google Scholar 

  • Floreano, D. and Mondada, F. (1998) Evolutionary neurocontrollers for autonomous mobile robots. Neural Netw. 11, 1461–1478.

    Article  PubMed  Google Scholar 

  • Foster, D. J., Morris, R. G., and Dayan, P. (2000) A model of hippocampally dependent navigation, using the temporal difference learning rule. Hippocampus 10, 1–16.

    Article  PubMed  CAS  Google Scholar 

  • Frank, L. M., Brown, E. N., and Wilson, M. (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178.

    Article  PubMed  CAS  Google Scholar 

  • Freund, T. F. and Buzsaki, G. (1996) Interneurons of the hippocampus. Hippocampus 6, 347–470.

    Article  PubMed  CAS  Google Scholar 

  • Gaussier, P., Revel, A., Banquet, J. P., and Babeau, V. (2002) From view cells and place cells to cognitive map learning: processing stages of the hippocampal system. Biol. Cybern. 86, 15–28.

    Article  PubMed  CAS  Google Scholar 

  • Granger, C. W. J. (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37, 424–438.

    Article  Google Scholar 

  • Griffiths, D., Dickinson, A., and Clayton, N. (1999) Episodic memory: what can animals remember about their past? Trends Cogn. Sci. 3, 74–80.

    Article  PubMed  Google Scholar 

  • Grossberg, S. (1999) The link between brain learning, attention, and consciousness. Conscious Cogn. 8, 1–44.

    Article  PubMed  CAS  Google Scholar 

  • Hasselmo, M. E., Bodelon, C., and Wyble, B. P. (2002a). A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 14, 793–817.

    Article  PubMed  Google Scholar 

  • Hasselmo, M. E., Hay, J., Ilyn, M., and Gorchetchnikov, A. (2002b). Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw. 15, 689–707.

    Article  PubMed  Google Scholar 

  • Ijspeert, A. J., Crespi, A., and Cabelguen, J.-M. (2005) Towards a salamander robot: applying neurobiological principles to the control of locomotion in robots. Neuroinformatics 3(3), in press.

  • Kaminski, M., Ding, M., Truccolo, W. A., and Bressler, S. L. (2001) Evaluating causal relations in neural systems: granger causality, directed transfer function and statistical assessment of significance. Biol. Cybern. 85, 145–157.

    Article  PubMed  CAS  Google Scholar 

  • Keinan, A., Sandbank, B., Hilgetag, C. C., Meilijson, I., and Ruppin, E. (2004) Fair attribution of functional contribution in artificial and biological networks. Neural Comput. 16, 1887–1915.

    Article  PubMed  Google Scholar 

  • Kotter, R. and Stephan, K. E. (2003) Network participation indices: characterizing component roles for information processing in neural networks. Neural Netw. 16, 1261–1275.

    Article  PubMed  Google Scholar 

  • Krichmar, J. L. and Edelman, G. M. (2002) Machine psychology: autonomous behavior, perceptual categorization and conditioning in a brain-based device. Cereb. Cortex 12, 818–830.

    Article  PubMed  Google Scholar 

  • Krichmar, J. L., Nitz, D. A., Gally, J. A., and Edelman, G. M. (2005) Characterizing functional hippocampal pathways in a brain-based device as it solves a spatial memory task. Proc. Natl. Acad. Sci. USA 102, 2111–2116.

    Article  PubMed  CAS  Google Scholar 

  • Kubie, J. L., Muller, R. U., and Bostock, E. (1990) Spatial firing properties of hippocampal theta cells. J. Neurosci. 10, 1110–1123.

    PubMed  CAS  Google Scholar 

  • Lavenex, P. and Amaral, D. G. (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10, 420–430.

    Article  PubMed  CAS  Google Scholar 

  • Liang, H., Ding, M., Nakamura, R., and Bressler, S. L. (2000) Causal influences in primate cerebral cortex during visual pattern discrimination. Neuroreport 11, 2875–2880.

    Article  PubMed  CAS  Google Scholar 

  • Mataric, M. J. (1991) Navigating with a rat brain: A neurobiologically-inspired model for robot spatial representation. In: From Animals to Animats. Meyer, J. A. and Wilson, S. W. (eds.) MIT Press, Cambridge, MA, pp. 169–175.

    Google Scholar 

  • Milford, M. J., Wyeth, G. F., and Prasser, D. (2004) RatSLAM: A Hippocampal Model for Simultaneous Localization and Mapping. Paper presented at: Proceedings of the 2004 IEEE International Conference on Robotics & Automation, New Orleans, LA.

  • Mogenson, G. and Nielsen, M. (1984) Neuropharmacological evidence to suggest that the nucleus accumbens and subpllidal region contributes to exploratory locomotion. Behav. Neural Biol. 42, 52–60.

    Article  PubMed  CAS  Google Scholar 

  • Montague, P. R., Dayan, P., and Sejnowski, T. J. (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci. 16, 1936–1947.

    PubMed  CAS  Google Scholar 

  • Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47–60.

    Article  PubMed  CAS  Google Scholar 

  • Muller, R. U., Ranck, J. B., Jr., and Taube, J. S. (1996) Head direction cells: properties and functional significance. Curr. Opin. Neurobiol. 6, 196–206.

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe, J. and Dostrovsky, J. (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175.

    Article  PubMed  CAS  Google Scholar 

  • Pearl, J. (1999) Causality: Models, reasoning, and inference. Cambridge University Press, Cambridge.

    Google Scholar 

  • Pfeifer, R. and Scheier, C. (1997) Sensory-motor coordination: The metaphor and beyond. Robot. Auton. Syst. 20, 157–178.

    Article  Google Scholar 

  • Recce, M. and Harris, K. D. (1996) Memory for places: a navigational model in support of Marr’s theory of hippocampal function. Hippocampus 6, 735–748.

    Article  PubMed  CAS  Google Scholar 

  • Redish, A. D., Touretzky, D., and Wan, H. S. (1993) Neural representation of space using sinusoidal arrays. Neural Comput. 5, 869–884.

    Google Scholar 

  • Reeke, G. N., Sporns, O., and Edelman, G. M. (1990) Synthetic neural modeling: The “Darwin” series of recognition automata. Proc. IEEE 78, 1498–1530.

    Article  Google Scholar 

  • Samsonovich, A. and McNaughton, B. L. (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900–5920.

    PubMed  CAS  Google Scholar 

  • Schultz, W., Dayan, P., and Montague, P. R. (1997) A neural substrate of prediction and reward. Science 275, 1593–1599.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz, G. (1978) Estimating the dimension of a model. Ann. Stat. 5, 461–464.

    Google Scholar 

  • Scoville, W. B. and Milner, B. (1957) Loss of recent memory after bilateral hippocampal lesions. J. Neurochem. 20, 11–21.

    CAS  Google Scholar 

  • Seth, A. K. Causal connectivity analysis of evolved neural networks during behavior. Netw.: Comput. Neural Syst., in press.

  • Seth, A. K., McKinstry, J. L., Edelman, G. M., and Krichmar, J. L. (2004a). Spatiotemporal processing of whisker input supports texture discrimination by a brain-based device. In: Animals to Animats 8: Proceedings of the Eighth International Conference on the Simulation of Adaptive Behavior. Meyer, J. A. (ed.) MIT Press, Cambridge, MA, pp. 130–139.

    Google Scholar 

  • Seth, A. K., McKinstry, J. L., Edelman, G. M., and Krichmar, J. L. (2004b). Visual Binding Through Reentrant Connectivity and Dynamic Synchronization in a Brain-based Device. Cereb. Cortex 14, 1185–1199.

    Article  PubMed  Google Scholar 

  • Shapiro, M. L. and Hetherington, P. A. (1993) A Simple Network Simulates Hippocampal Place Fields: Parametric Analyses and Physiological Predictions. Behav. Neurosci. 107, 34–50.

    Article  PubMed  CAS  Google Scholar 

  • Skaggs, W. E., McNaughton, B. L., Wilson, M. A., and Barnes, C. A. (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149–172.

    Article  PubMed  CAS  Google Scholar 

  • Sporns, O. and Alexander, W. H. (2002) Neuromodulation and plasticity in an autonomous robot. Neural Netw. 15, 761–774.

    Article  PubMed  Google Scholar 

  • Sporns, O., Almassy, N., and Edelman, G. M. (2000) Plasticity in value systems and its role in adaptive behavior. Adapt. Behav. 8, 129–148.

    Article  Google Scholar 

  • Stewart, M. and Fox, S. E. (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci. 13, 163–168.

    Article  PubMed  CAS  Google Scholar 

  • Sutton, R. S. and Barto, A. G. (1990) Time-derivative models of pavlovian reinforcement. In: Learning and Computational Neuroscience: Foundations of Adaptive Networks, Moore, J. (ed.) MIT Press, Cambridge, MA, pp. 497–537.

    Google Scholar 

  • Taube, J. S. (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog. Neurobiol. 55, 225–256.

    Article  PubMed  CAS  Google Scholar 

  • Thierry, A. M., Gioanni, Y., Degenetais, E., and Glowinski, J. (2000) Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 10, 411–419.

    Article  PubMed  CAS  Google Scholar 

  • Tononi, G. and Sporns, O. (2003) Measuring information integration. BMC Neurosci. 4, 31.

    Article  PubMed  Google Scholar 

  • Treves, A. (2004) Learning to predict through adaptation. Neuroinformatics 2, 361–366.

    Article  PubMed  Google Scholar 

  • Treves, A. and Rolls, E. T. (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374–391.

    Article  PubMed  CAS  Google Scholar 

  • Tulving, E. (1972) Episodic and semantic memory. In: Organisation of Memory. Donaldson, W. (ed.) Academic Press, New York, pp. 381–403.

    Google Scholar 

  • Uchibe, E. and Doya, K. (2004) Competitive-Cooperative-Concurrent Reinforcement Learning with Importance Sampling. In: Animals to Animats 8: Proceedings of the Eighth International Conference on the Simulation of Adaptive Behavior. Schaal, S., Ijspeert, A., Billard, A., Vijayakumar, S., Hallam, J., and Meyer, J. A. (eds.) MIT Press, Cambridge, MA.

    Google Scholar 

  • Ungerleider, L. and Mishkin, M. (1982) Two cortical visual systems. In: Analysis of Visual Behavior, R. Mansfield (ed.) MIT Press, Cambridge, MA, pp. 549–586.

    Google Scholar 

  • Ungerleider, L. G., and Haxby, J. V. (1994) ‘What’ and ‘where’ in the human brain. Curr. Opin. Neurobiol. 4, 157–165.

    Article  PubMed  CAS  Google Scholar 

  • Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van Paesschen, W., and Mishkin, M. (1997) Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380.

    Article  PubMed  CAS  Google Scholar 

  • Weng, J. (2004) Developmental robots: Theory and experiments. Int. J. Humanoid Robot. 1, 199–236.

    Article  Google Scholar 

  • Witter, M. P., Naber, P. A., van Haeften, T., et al. (2000a). Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10, 398–410.

    Article  PubMed  CAS  Google Scholar 

  • Witter, M. P., Wouterlood, F. G., Naber, P. A., and Van Haeften, T. (2000b). Anatomical organization of the parahippocampal-hippocampal network. Ann. NY Acad. Sci. 911, 1–24.

    Article  PubMed  CAS  Google Scholar 

  • Wray, J. and Edelman, G. M. (1996) A model of color vision based on cortical reentry. Cereb. Cortex 6, 701–716.

    Article  PubMed  CAS  Google Scholar 

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  1. The Neurosciences Institute, 10640 John J. Hopkins Drive, 92121, San Diego, CA, USA

    Jeffrey L. Krichmar, Anil K. Seth, Douglas A. Nitz, Jason G. Fleischer & Gerald M. Edelman

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  1. Jeffrey L. Krichmar
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  2. Anil K. Seth
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  4. Jason G. Fleischer
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  5. Gerald M. Edelman
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Correspondence to Jeffrey L. Krichmar.

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Krichmar, J.L., Seth, A.K., Nitz, D.A. et al. Spatial navigation and causal analysis in a brain-based device modeling cortical-hippocampal interactions. Neuroinform 3, 197–221 (2005). https://doi.org/10.1385/NI:3:3:197

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