Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1

The hippocampus has differentiated into an extensively connected recurrent stage (CA3) followed by a feed-forward stage (CA1). We examined the function of this structural differentiation by determining how cell ensembles in rat CA3 and CA1 generate representations of rooms with common spatial elements. In CA3, distinct subsets of pyramidal cells were activated in each room, regardless of the similarity of the testing enclosure. In CA1, the activated populations overlapped, and the overlap increased in similar enclosures. After exposure to a novel room, ensemble activity developed slower in CA3 than CA1, suggesting that the representations emerged independently.

[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]  R. Hirsh The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

[3]  L. Jarrard,et al.  Role of interference in retention by rats with hippocampal lesions. , 1975, Journal of comparative and physiological psychology.

[4]  James L Olds,et al.  Effects of context manipulation on memory and reversal learning in rats with hippocampal lesions. , 1978, Journal of comparative and physiological psychology.

[5]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

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

[8]  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.

[9]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[10]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[11]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[12]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[13]  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.

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

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

[16]  M. Gabriel,et al.  Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits , 1996, Journal of Neuroscience.

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

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

[19]  Patricia E. Sharp,et al.  Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: Comparison with hippocampal place cells , 1997, Behavioural Brain Research.

[20]  Alcino J. Silva,et al.  The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. , 1998, Behavioral neuroscience.

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

[22]  Heikki Tanila,et al.  Hippocampal place cells can develop distinct representations of two visually identical environments , 1999, Hippocampus.

[23]  Paul E. Gilbert,et al.  Testing neural network models of memory with behavioral experiments , 2000, Current Opinion in Neurobiology.

[24]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

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

[26]  Greg D. Gale,et al.  Hippocampus and contextual fear conditioning: Recent controversies and advances , 2001, Hippocampus.

[27]  S. Mizumori,et al.  Context-specific spatial representations by lateral septal cells , 2002, Neuroscience.

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

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

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

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

[32]  A. Treves Computational constraints between retrieving the past and predicting the future, and the CA3‐CA1 differentiation , 2004, Hippocampus.

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

[34]  J. Guzowski,et al.  Differences in Hippocampal Neuronal Population Responses to Modifications of an Environmental Context: Evidence for Distinct, Yet Complementary, Functions of CA3 and CA1 Ensembles , 2004, The Journal of Neuroscience.