Progressive Transformation of Hippocampal Neuronal Representations in “Morphed” Environments

Hippocampal neural codes for different, familiar environments are thought to reflect distinct attractor states, possibly implemented in the recurrent CA3 network. A defining property of an attractor network is its ability to undergo sharp and coherent transitions between pre-established (learned) representations when the inputs to the network are changed. To determine whether hippocampal neuronal ensembles exhibit such discontinuities, we recorded in CA3 and CA1 when a familiar square recording enclosure was morphed in quantifiable steps into a familiar circular enclosure while leaving other inputs constant. We observed a gradual noncoherent progression from the initial to the final network state. In CA3, the transformation was accompanied by significant hysteresis, resulting in more similar end states than when only square and circle were presented. These observations suggest that hippocampal cell assemblies are capable of incremental plastic deformation, with incongruous information being incorporated into pre-existing representations.

[1]  E. Rolls,et al.  Neural networks and brain function , 1998 .

[2]  M. Quirk,et al.  Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience , 2003, Neuron.

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

[4]  Neil Burgess,et al.  Attractor Dynamics in the Hippocampal Representation of the Local Environment , 2005, Science.

[5]  Daniel J. Amit,et al.  Modeling brain function: the world of attractor neural networks, 1st Edition , 1989 .

[6]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

[7]  M. Hasselmo,et al.  Encoding and retrieval in the CA3 region of the hippocampus: a model of theta-phase separation. , 2005, Journal of neurophysiology.

[8]  J. Knierim,et al.  Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3 , 2004, Nature.

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

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

[11]  B. McNaughton,et al.  Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. , 1998, Journal of neurophysiology.

[12]  H. Eichenbaum,et al.  Cues that hippocampal place cells encode: Dynamic and hierarchical representation of local and distal stimuli , 1997, Hippocampus.

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

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

[15]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  R. Muller,et al.  Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli , 2000, The Journal of general physiology.

[17]  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.

[18]  A. V. Lukashin,et al.  Modeling motor cortical operations by an attractor network of stochastic neurons , 1996, Biological Cybernetics.

[19]  V Paz-Villagrán,et al.  Independent coding of connected environments by place cells , 2004, The European journal of neuroscience.

[20]  O. Paulsen,et al.  A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity , 1998, Trends in Neurosciences.

[21]  E T Rolls,et al.  Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network , 1992, Hippocampus.

[22]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[24]  James J. Knierim,et al.  Ensemble Dynamics of Hippocampal Regions CA3 and CA1 , 2004, Neuron.

[25]  K. Jeffery,et al.  Preserved performance in a hippocampal‐dependent spatial task despite complete place cell remapping , 2003, Hippocampus.

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

[27]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[28]  J. Csicsvari,et al.  Organization of cell assemblies in the hippocampus , 2003, Nature.

[29]  M. Fyhn,et al.  Hippocampal Neurons Responding to First-Time Dislocation of a Target Object , 2002, Neuron.

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

[31]  T J Sejnowski,et al.  Learning viewpoint-invariant face representations from visual experience in an attractor network. , 1998, Network.

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

[33]  Edmund T. Rolls,et al.  What determines the capacity of autoassociative memories in the brain? Network , 1991 .

[34]  Alessandro Treves,et al.  Attractor neural networks storing multiple space representations: A model for hippocampal place fields , 1998, cond-mat/9807101.

[35]  A. Ainsworth,et al.  Glass-coated platinum-plated tungsten microelectrodes , 1972, Medical and biological engineering.

[36]  C. Giovanni Galizia,et al.  Odor-Driven Attractor Dynamics in the Antennal Lobe Allow for Simple and Rapid Olfactory Pattern Classification , 2004, Neural Computation.

[37]  M. Andersson,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005 .

[38]  B. McNaughton,et al.  Hippocampal synaptic enhancement and information storage within a distributed memory system , 1987, Trends in Neurosciences.

[39]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[40]  R. Wyttenbach,et al.  Categorical Perception of Sound Frequency by Crickets , 1996, Science.

[41]  John J. Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities , 1999 .

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

[43]  James J Knierim,et al.  Dynamic Interactions between Local Surface Cues, Distal Landmarks, and Intrinsic Circuitry in Hippocampal Place Cells , 2002, The Journal of Neuroscience.

[44]  M. Shapiro,et al.  Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. , 1997, Behavioral neuroscience.

[45]  M. Hasselmo,et al.  Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[47]  R. Muller,et al.  The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  Menno P. Witter,et al.  Place Cells and Place Recognition Maintained by Direct Entorhinal-Hippocampal Circuitry , 2002, Science.

[49]  Beata Jarosiewicz,et al.  Hippocampal Place Cells Are Not Controlled by Visual Input during the Small Irregular Activity State in the Rat , 2004, The Journal of Neuroscience.

[50]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[52]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[53]  James L. McClelland,et al.  Considerations arising from a complementary learning systems perspective on hippocampus and neocortex , 1996, Hippocampus.

[54]  S. Molden,et al.  Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task , 2001, The Journal of Neuroscience.