Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations

In the cerebral cortex, diverse types of neurons form intricate circuits and cooperate in time for the processing and storage of information. Recent advances reveal a spatiotemporal division of labor in cortical circuits, as exemplified in the CA1 hippocampal area. In particular, distinct GABAergic (γ-aminobutyric acid–releasing) cell types subdivide the surface of pyramidal cells and act in discrete time windows, either on the same or on different subcellular compartments. They also interact with glutamatergic pyramidal cell inputs in a domain-specific manner and support synaptic temporal dynamics, network oscillations, selection of cell assemblies, and the implementation of brain states. The spatiotemporal specializations in cortical circuits reveal that cellular diversity and temporal dynamics coemerged during evolution, providing a basis for cognitive behavior.

[1]  J. O’Keefe.  Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[2]  P. Somogyi,et al.  A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells , 1983, Brain Research.

[3]  J. Lund,et al.  Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics , 1993, The Journal of comparative neurology.

[4]  M. Deschenes,et al.  Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. , 1993, Journal of neurophysiology.

[5]  Z. Borhegyi,et al.  Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  G. Buzsáki,et al.  Inhibitory CA1-CA3-hilar region feedback in the hippocampus. , 1994, Science.

[7]  G. Buzsáki,et al.  Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells , 1995, Hippocampus.

[8]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  T. Freund,et al.  Interneurons Containing Calretinin Are Specialized to Control Other Interneurons in the Rat Hippocampus , 1996, The Journal of Neuroscience.

[10]  L. Acsády,et al.  Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus , 1996, Neuroscience.

[11]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[12]  I. Módy,et al.  Synaptic Communication among Hippocampal Interneurons: Properties of Spontaneous IPSCs in Morphologically Identified Cells , 1997, The Journal of Neuroscience.

[13]  A. Thomson,et al.  Facilitating pyramid to horizontal oriens‐alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus , 1998, The Journal of physiology.

[14]  György Buzsáki,et al.  Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo , 1998, The European journal of neuroscience.

[15]  J. Deuchars,et al.  CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices , 1998, The Journal of physiology.

[16]  Ken Mackie,et al.  Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA Release from Axon Terminals of Specific Hippocampal Interneurons , 1999, The Journal of Neuroscience.

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

[18]  L. Acsády,et al.  Medial septal and median raphe innervation of vasoactive intestinal polypeptide-containing interneurons in the hippocampus , 1999, Neuroscience.

[19]  U. Stäubli,et al.  Recognition Memory Correlates of Hippocampal Theta Cells , 2001, The Journal of Neuroscience.

[20]  Alex M Thomson,et al.  Physiological and morphological diversity of immunocytochemically defined parvalbumin‐ and cholecystokinin‐positive interneurones in CA1 of the adult rat hippocampus , 2002, The Journal of comparative neurology.

[21]  R. Miles,et al.  On the Origin of Interictal Activity in Human Temporal Lobe Epilepsy in Vitro , 2002, Science.

[22]  G. Buzsáki,et al.  Hippocampal Pyramidal Cell–Interneuron Spike Transmission Is Frequency Dependent and Responsible for Place Modulation of Interneuron Discharge , 2002, The Journal of Neuroscience.

[23]  G. Tamás,et al.  Identified Sources and Targets of Slow Inhibition in the Neocortex , 2003, Science.

[24]  P. Jonas,et al.  Kv3 Potassium Conductance is Necessary and Kinetically Optimized for High-Frequency Action Potential Generation in Hippocampal Interneurons , 2003, The Journal of Neuroscience.

[25]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[26]  O. Paulsen,et al.  Spike Timing of Distinct Types of GABAergic Interneuron during Hippocampal Gamma Oscillations In Vitro , 2004, The Journal of Neuroscience.

[27]  Z. Borhegyi,et al.  Phase Segregation of Medial Septal GABAergic Neurons during Hippocampal Theta Activity , 2004, The Journal of Neuroscience.

[28]  Massimo Scanziani,et al.  Routing of spike series by dynamic circuits in the hippocampus , 2004, Nature.

[29]  P. Somogyi,et al.  Input and frequency‐specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin , 2004, European Journal of Neuroscience.

[30]  P. Somogyi,et al.  Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo , 2004, Nature Neuroscience.

[31]  H. Markram,et al.  Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit , 2004, The Journal of physiology.

[32]  P. Somogyi,et al.  Properties of horizontal axo‐axonic cells in stratum oriens of the hippocampal CA1 area of rats in vitro , 2004, Hippocampus.

[33]  Michel Le Van Quyen,et al.  Epileptogenic Actions of GABA and Fast Oscillations in the Developing Hippocampus , 2005, Neuron.

[34]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

[35]  Hannah Monyer,et al.  Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro , 2005, The Journal of physiology.

[36]  Z. Nusser,et al.  Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses , 2005, The Journal of Neuroscience.

[37]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[38]  A. Tsalenko,et al.  Marek's disease virus Meq transforms chicken cells via the v-Jun transcriptional cascade: a converging transforming pathway for avian oncoviruses. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Marco Capogna,et al.  Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area , 2005, The Journal of Neuroscience.

[40]  Hannah Monyer,et al.  Transient depression of excitatory synapses on interneurons contributes to epileptiform bursts during gamma oscillations in the mouse hippocampal slice. , 2005, Journal of neurophysiology.

[41]  Jozsef Csicsvari,et al.  Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations , 2005, The Journal of Neuroscience.

[42]  Stefan Hefft,et al.  Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron–principal neuron synapse , 2005, Nature Neuroscience.

[43]  F. Fujiyama,et al.  Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex , 2005, The European journal of neuroscience.

[44]  Viktor Varga,et al.  Serotonergic neuron diversity: identification of raphe neurons with discharges time-locked to the hippocampal theta rhythm. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[45]  L. Swanson,et al.  Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat , 2006, The Journal of comparative neurology.

[46]  Andrew P Maurer,et al.  Phase Precession in Hippocampal Interneurons Showing Strong Functional Coupling to Individual Pyramidal Cells , 2006, The Journal of Neuroscience.

[47]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[48]  C. McBain,et al.  Cell type‐specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones , 2006, The Journal of physiology.

[49]  Robert A Pearce,et al.  Active and Passive Membrane Properties and Intrinsic Kinetics Shape Synaptic Inhibition in Hippocampal CA1 Pyramidal Neurons , 2006, The Journal of Neuroscience.

[50]  T. Hökfelt,et al.  Characterization of neuropeptide Y2 receptor protein expression in the mouse brain. I. Distribution in cell bodies and nerve terminals , 2006, The Journal of comparative neurology.

[51]  G. Tamás,et al.  Excitatory Effect of GABAergic Axo-Axonic Cells in Cortical Microcircuits , 2006, Science.

[52]  S. Nelson,et al.  Molecular taxonomy of major neuronal classes in the adult mouse forebrain , 2006, Nature Neuroscience.

[53]  A. Sampson,et al.  Regional specificity of chandelier neuron axon terminal alterations in schizophrenia , 2006, Neuroscience.

[54]  Christophe Bernard,et al.  Interneurons targeting similar layers receive synaptic inputs with similar kinetics , 2006, Hippocampus.

[55]  Massimo Scanziani,et al.  Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells , 2006, Nature Neuroscience.

[56]  P. Somogyi,et al.  Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus , 2007, The Journal of Neuroscience.

[57]  Pablo Fuentealba,et al.  Cell Type-Specific Tuning of Hippocampal Interneuron Firing during Gamma Oscillations In Vivo , 2007, The Journal of Neuroscience.

[58]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[59]  Douglas A Nitz,et al.  Discrete place fields of hippocampal formation interneurons. , 2007, Journal of neurophysiology.

[60]  I. Soltesz,et al.  Cell type–specific gating of perisomatic inhibition by cholecystokinin , 2007, Nature Neuroscience.

[61]  Fiona E. N. LeBeau,et al.  Recruitment of Parvalbumin-Positive Interneurons Determines Hippocampal Function and Associated Behavior , 2007, Neuron.

[62]  M. Wilson,et al.  Spatial selectivity and theta phase precession in CA1 interneurons , 2007, Hippocampus.

[63]  György Buzsáki,et al.  Hippocampal place cell assemblies are speed-controlled oscillators , 2007, Proceedings of the National Academy of Sciences.

[64]  N. Spruston,et al.  Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus , 2008, The Journal of comparative neurology.

[65]  M. Brecht,et al.  Behavioural report of single neuron stimulation in somatosensory cortex , 2008, Nature.

[66]  Jozsef Csicsvari,et al.  Ivy Cells: A Population of Nitric-Oxide-Producing, Slow-Spiking GABAergic Neurons and Their Involvement in Hippocampal Network Activity , 2008, Neuron.