Organization of cell assemblies in the hippocampus

Neurons can produce action potentials with high temporal precision. A fundamental issue is whether, and how, this capability is used in information processing. According to the ‘cell assembly’ hypothesis, transient synchrony of anatomically distributed groups of neurons underlies processing of both external sensory input and internal cognitive mechanisms. Accordingly, neuron populations should be arranged into groups whose synchrony exceeds that predicted by common modulation by sensory input. Here we find that the spike times of hippocampal pyramidal cells can be predicted more accurately by using the spike times of simultaneously recorded neurons in addition to the animals location in space. This improvement remained when the spatial prediction was refined with a spatially dependent theta phase modulation. The time window in which spike times are best predicted from simultaneous peer activity is 10–30 ms, suggesting that cell assemblies are synchronized at this timescale. Because this temporal window matches the membrane time constant of pyramidal neurons, the period of the hippocampal gamma oscillation and the time window for synaptic plasticity, we propose that cooperative activity at this timescale is optimal for information transmission and storage in cortical circuits.

[1]  C. Waddington.  Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[2]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

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

[4]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[5]  W. Scharloo,et al.  Canalization: Genetic and Developmental Aspects , 1991 .

[6]  N. Spruston,et al.  Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. , 1992, Journal of neurophysiology.

[7]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

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

[9]  M. Wong-Riley,et al.  Primate Visual Cortex , 1994 .

[10]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[11]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[12]  S. Stearns,et al.  The differential genetic and environmental canalization of fitness components in Drosophila melanogaster , 1995 .

[13]  J E Lisman,et al.  Storage of 7 +/- 2 short-term memories in oscillatory subcycles , 1995, Science.

[14]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[15]  A. Wagner.  DOES EVOLUTIONARY PLASTICITY EVOLVE? , 1996, Evolution; international journal of organic evolution.

[16]  G. Wagner,et al.  A POPULATION GENETIC THEORY OF CANALIZATION , 1997, Evolution; international journal of organic evolution.

[17]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[18]  R. Muller,et al.  Place cell discharge is extremely variable during individual passes of the rat through the firing field. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  T. Albright,et al.  Efficient Discrimination of Temporal Patterns by Motion-Sensitive Neurons in Primate Visual Cortex , 1998, Neuron.

[20]  S. Rice.  THE EVOLUTION OF CANALIZATION AND THE BREAKING OF VON BAER'S LAWS: MODELING THE EVOLUTION OF DEVELOPMENT WITH EPISTASIS , 1998, Evolution; international journal of organic evolution.

[21]  E N Brown,et al.  A Statistical Paradigm for Neural Spike Train Decoding Applied to Position Prediction from Ensemble Firing Patterns of Rat Hippocampal Place Cells , 1998, The Journal of Neuroscience.

[22]  A. Cossins.  Cryptic clues revealed , 1998, Nature.

[23]  S. Lindquist,et al.  Hsp90 as a capacitor for morphological evolution , 1998, Nature.

[24]  G. Wagner,et al.  Is Hsp90 a regulator of evolvability? , 1999, The Journal of experimental zoology.

[25]  R. G. Morris.  D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949 , 1999, Brain Research Bulletin.

[26]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[27]  A. McLaren.  Too late for the midwife toad: stress, variability and Hsp90. , 1999, Trends in genetics : TIG.

[28]  J. Seger,et al.  Cause and effect in evolution , 1999, Nature.

[29]  Ronald W. Davis,et al.  Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. , 1999, Science.

[30]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[31]  M. Quirk,et al.  Interaction between spike waveform classification and temporal sequence detection , 1999, Journal of Neuroscience Methods.

[32]  J. Lisman,et al.  Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. , 2000, Journal of neurophysiology.

[33]  R. Reid,et al.  Low Response Variability in Simultaneously Recorded Retinal, Thalamic, and Cortical Neurons , 2000, Neuron.

[34]  Yudong D. He,et al.  Functional Discovery via a Compendium of Expression Profiles , 2000, Cell.

[35]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[36]  Garth A. Gibson,et al.  Canalization in evolutionary genetics: a stabilizing theory? , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  A. Zador,et al.  Neural representation and the cortical code. , 2000, Annual review of neuroscience.

[38]  S. Rutherford,et al.  From genotype to phenotype: buffering mechanisms and the storage of genetic information , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[39]  D. Tautz.  A genetic uncertainty problem. , 2000, Trends in genetics : TIG.

[40]  G. Wagner,et al.  Modeling the evolution of genetic architecture: A continuum of alleles model with pairwise AxA epistasis. , 2000, Journal of theoretical biology.

[41]  G Buzsáki,et al.  Behavior-Dependent States of the Hippocampal Network Affect Functional Clustering of Neurons , 2001, The Journal of Neuroscience.

[42]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[43]  G. Buzsáki,et al.  Temporal Interaction between Single Spikes and Complex Spike Bursts in Hippocampal Pyramidal Cells , 2001, Neuron.

[44]  B. McNaughton,et al.  Independence of Firing Correlates of Anatomically Proximate Hippocampal Pyramidal Cells , 2001, The Journal of Neuroscience.

[45]  A K Kreiter,et al.  Synchronization and assembly formation in the visual cortex. , 2001, Progress in brain research.

[46]  G. Wagner,et al.  Modeling genetic architecture: a multilinear theory of gene interaction. , 2001, Theoretical population biology.

[47]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[48]  A. Bergman,et al.  Waddington's canalization revisited: Developmental stability and evolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  T. Mitchell-Olds,et al.  Chaperones as Buffering Agents? , 2002, Science.

[50]  R. Reid,et al.  Precise Firing Events Are Conserved across Neurons , 2002, The Journal of Neuroscience.

[51]  S. Lindquist,et al.  Hsp90 as a capacitor of phenotypic variation , 2002, Nature.

[52]  Colin D. Meiklejohn,et al.  A single mode of canalization , 2002 .

[53]  A. Barabasi,et al.  Hierarchical Organization of Modularity in Metabolic Networks , 2002, Science.

[54]  D. Featherstone,et al.  Wrestling with pleiotropy: genomic and topological analysis of the yeast gene expression network. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[55]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

[56]  M. Pigliucci.  Developmental genetics: Buffer zone , 2002, Nature.

[57]  Ronald W. Davis,et al.  Functional profiling of the Saccharomyces cerevisiae genome , 2002, Nature.

[58]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[59]  Richard J. Edwards,et al.  Transiently beneficial insertions could maintain mobile DNA sequences in variable environments. , 2003, Molecular biology and evolution.