Learning in a geometric model of place cell firing

Following Hartley et al. (Hartley et al. ( 2000 ) Hippocampus 10:369–379), we present a simple feed‐forward model of place cell (PC) firing predicated on neocortical information regarding the environmental geometry surrounding the animal. Incorporating the idea of boundaries with distinct sensory qualities, we show that synaptic plasticity mediated by a BCM‐like rule (Bienenstock et al. ( 1982 ) J Neurosci 2:32–48) produces PCs that encode position relative to specific extended landmarks. In an unchanging environment the model is shown to undergo an initial phase of learning, resulting in the formation of stable place fields. In familiar environments, perturbation of environmental cues produces graded changes in the firing rate and position of place fields. Model simulations are compared favorably with three sets of experimental data: (1) Results published by Barry et al. (Barry et al. ( 2006 ) Rev Neurosci 17:71–97) showing the slow disappearance of duplicate place fields produced when a barrier is placed into a familiar environment. (2) Rivard et al.'s (Rivard et al. ( 2004 ) J Gen Physiol 124:9–25) study showing a graded response in PC firing such that fields near to a centrally placed object encode space relative to the object, whereas more distant fields respond to the surrounding environment. (3) Fenton et al.'s (Fenton et al. ( 2000a ) J Gen Physiol 116:191–209) observation that inconsistent rotation of cue cards produces parametric changes in place field positions. The merits of the model are discussed in terms of its extensibility and biological plausibility. © 2007 Wiley‐Liss, Inc.

[1]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[3]  A. J. Hill First occurrence of hippocampal spatial firing in a new environment , 1978, Experimental Neurology.

[4]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  D. Zipser,et al.  Biologically plausible models of place recognition and goal location , 1986 .

[6]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Lucien T. Thompson,et al.  Persistence, reticence, and opportunism of place-field activity in hippocampal neurons , 1989 .

[9]  B. McNaughton,et al.  Cortical-hippocampal interactions and cognitive mapping: A hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing , 1989 .

[10]  Y. Miyashita,et al.  Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  B. McNaughton,et al.  Hebb-Marr networks and the neurobiological representation of action in space. , 1990 .

[14]  E. Bostock,et al.  Experience‐dependent modifications of hippocampal place cell firing , 1991, Hippocampus.

[15]  Patricia E. Sharp,et al.  Computer simulation of hippocampal place cells , 1991, Psychobiology.

[16]  Taketoshi Ono,et al.  Place recognition responses of neurons in monkey hippocampus , 1991, Neuroscience Letters.

[17]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[18]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Michael Recce,et al.  A model of hippocampal function , 1994, Neural Networks.

[20]  Bruce L. McNaughton,et al.  A Model of the Neural Basis of the Rat's Sense of Direction , 1994, NIPS.

[21]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

[22]  J. O’Keefe,et al.  Neuronal computations underlying the firing of place cells and their role in navigation , 1996, Hippocampus.

[23]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[24]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  A S Etienne,et al.  Path integration in mammals and its interaction with visual landmarks. , 1996, The Journal of experimental biology.

[26]  K M Gothard,et al.  Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues , 1996, The Journal of Neuroscience.

[27]  C Kentros,et al.  Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. , 1998, Science.

[28]  B. McNaughton,et al.  Spatial Firing Properties of Hippocampal CA1 Populations in an Environment Containing Two Visually Identical Regions , 1998, The Journal of Neuroscience.

[29]  P E Sharp,et al.  Subicular place cells expand or contract their spatial firing pattern to fit the size of the environment in an open field but not in the presence of barriers: comparison with hippocampal place cells. , 1999, Behavioral neuroscience.

[30]  David S. Touretzky,et al.  Synaptic learning models of map separation in the hippocampus , 2000, Neurocomputing.

[31]  P. Dayan,et al.  The Involvement of Recurrent Connections in Area CA3 in Establishing the Properties of Place Fields: a Model , 2000, The Journal of Neuroscience.

[32]  Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli , 2000, The Journal of general physiology.

[33]  E. Save,et al.  Contribution of multiple sensory information to place field stability in hippocampal place cells , 2000, Hippocampus.

[34]  J. O’Keefe,et al.  Modeling place fields in terms of the cortical inputs to the hippocampus , 2000, Hippocampus.

[35]  André A. Fenton,et al.  Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli , 2000, The Journal of general physiology.

[36]  Neil Burgess,et al.  Orientational and Geometric Determinants of Place and Head-direction , 2001, NIPS.

[37]  Tom Hartley,et al.  What can the hippocampal representation of environmental geometry tell us about Hebbian learning? , 2002, Biological Cybernetics.

[38]  M. Quirk,et al.  Requirement for Hippocampal CA3 NMDA Receptors in Associative Memory Recall , 2002, Science.

[39]  E. Rolls,et al.  A unified model of spatial and episodic memory , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[40]  Thomas J. Wills,et al.  Long-term plasticity in hippocampal place-cell representation of environmental geometry , 2002, Nature.

[41]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[42]  Kathryn J Jeffery,et al.  Heterogeneous Modulation of Place Cell Firing by Changes in Context , 2003, The Journal of Neuroscience.

[43]  Eric R Kandel,et al.  The long-term stability of new hippocampal place fields requires new protein synthesis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  R. Muller,et al.  Representation of Objects in Space by Two Classes of Hippocampal Pyramidal Cells , 2004, The Journal of general physiology.

[45]  J. O’Keefe,et al.  Hippocampal place units in the freely moving rat: Why they fire where they fire , 1978, Experimental Brain Research.

[46]  Neil Burgess,et al.  Abrupt shift in hippocampal place cell representation from square-like to circle-like in a morph box , 2004 .

[47]  N. Burgess,et al.  Geometric determinants of human spatial memory , 2004, Cognition.

[48]  A. Treves,et al.  Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1 , 2004, Science.

[49]  Robert U Muller,et al.  Deforming the hippocampal map , 2005, Hippocampus.

[50]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[51]  B Poucet,et al.  Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment , 2005, Hippocampus.

[52]  J. O’Keefe,et al.  Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells , 2005, Hippocampus.

[53]  J. Erichsen,et al.  Representing the Richness of Avian Spatial Cognition: Properties of a Lateralized Homing Pigeon Hippocampus , 2006, Reviews in the neurosciences.

[54]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

[55]  K. Jeffery,et al.  The Boundary Vector Cell Model of Place Cell Firing and Spatial Memory , 2006, Reviews in the neurosciences.

[56]  J. O’Keefe,et al.  An oscillatory interference model of grid cell firing , 2007, Hippocampus.

[57]  N. Ulanovsky,et al.  Hippocampal cellular and network activity in freely moving echolocating bats , 2007, Nature Neuroscience.