Multiple origins of the cortical gamma rhythm

Gamma rhythms (30–80 Hz) are a near‐ubiquitous feature of neuronal population activity in mammalian cortices. Their dynamic properties permit the synchronization of neuronal responses to sensory input within spatially distributed networks, transient formation of local neuronal “cell assemblies,” and coherent response patterns essential for intercortical regional communication. Each of these phenomena form part of a working hypothesis for cognitive function in cortex. All forms of physiological gamma rhythm are inhibition based, being characterized by rhythmic trains of inhibitory postsynaptic potentials in populations of principal neurons. It is these repeating periods of relative enhancement and attenuation of the responsivity of major cell groups in cortex that provides a temporal structure shared across many millions of neurons. However, when considering the origins of these repeating trains of inhibitory events considerable divergence is seen depending on cortical region studied and mode of activation of gamma rhythm generating networks. Here, we review the evidence for involvement of multiple subtypes of interneuron and focus on different modes of activation of these cells. We conclude that most massively parallel brain regions have different mechanisms of gamma rhythm generation, that different mechanisms have distinct functional correlates, and that switching between different local modes of gamma generation may be an effective way to direct cortical communication streams. Finally, we suggest that developmental disruption of the endophenotype for certain subsets of gamma‐generating interneuron may underlie cognitive deficit in psychiatric illness. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 71: 92–106, 2011

[1]  E. Adrian Olfactory reactions in the brain of the hedgehog , 1942, The Journal of physiology.

[2]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Wong,et al.  Excitatory synaptic responses mediated by GABAA receptors in the hippocampus , 1991, Science.

[4]  R. Miles,et al.  Metabotropic glutamate receptors mediate a post‐tetanic excitation of guinea‐pig hippocampal inhibitory neurones. , 1993, The Journal of physiology.

[5]  K. Reinikainen,et al.  Selective attention enhances the auditory 40-Hz transient response in humans , 1993, Nature.

[6]  G. Buzsáki,et al.  Hippocampal CA1 interneurons: an in vivo intracellular labeling study , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[8]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[9]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[10]  B. Rudy,et al.  Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[12]  C. McBain,et al.  The hyperpolarization‐activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens‐alveus interneurones. , 1996, The Journal of physiology.

[13]  R. Traub,et al.  Neuronal networks for induced ‘40 Hz’ rhythms , 1996, Trends in Neurosciences.

[14]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[15]  R. Traub,et al.  A mechanism for generation of long-range synchronous fast oscillations in the cortex , 1996, Nature.

[16]  P. Somogyi,et al.  Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus , 1996, Hippocampus.

[17]  G. Buzsáki,et al.  Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. , 1996, The Journal of physiology.

[18]  R. Traub,et al.  Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice , 1997 .

[19]  R. Traub,et al.  Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. , 1997, The Journal of physiology.

[20]  M. Whittington,et al.  Gamma frequency oscillations gate temporally coded afferent inputs in the rat hippocampal slice , 1998, Neuroscience Letters.

[21]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[22]  R. Miles,et al.  How Many Subtypes of Inhibitory Cells in the Hippocampus? , 1998, Neuron.

[23]  Tomoyuki Takano,et al.  Characterization of developmental changes in EEG‐gamma band activity during childhood using the autoregressive model , 1998, Acta paediatrica Japonica : Overseas edition.

[24]  G. Collingridge,et al.  The GluR5 subtype of kainate receptor regulates excitatory synaptic transmission in areas CA1 and CA3 of the rat hippocampus , 1998, Neuropharmacology.

[25]  P. Sokoloff,et al.  A rat G protein‐coupled receptor selectively expressed in myelin‐forming cells , 1998, The European journal of neuroscience.

[26]  P. Somogyi,et al.  Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat , 1998, The Journal of Neuroscience.

[27]  R. Traub,et al.  Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro , 1998, Nature.

[28]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[29]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Wei Yang Lu,et al.  G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors , 1999, Nature Neuroscience.

[31]  Y Yarom,et al.  Electrotonic Coupling Interacts with Intrinsic Properties to Generate Synchronized Activity in Cerebellar Networks of Inhibitory Interneurons , 1999, The Journal of Neuroscience.

[32]  J. A. Payne,et al.  The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation , 1999, Nature.

[33]  R. Traub,et al.  Inhibition-based rhythms: experimental and mathematical observations on network dynamics. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[34]  Y. Yarom,et al.  Resonance, oscillation and the intrinsic frequency preferences of neurons , 2000, Trends in Neurosciences.

[35]  Takaichi Fukuda,et al.  The dual network of GABAergic interneurons linked by both chemical and electrical synapses: a possible infrastructure of the cerebral cortex , 2000, Neuroscience Research.

[36]  J. White,et al.  Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  F. G. Pike,et al.  Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents , 2000, The Journal of physiology.

[39]  A. Thomson Facilitation, augmentation and potentiation at central synapses , 2000, Trends in Neurosciences.

[40]  P. Somogyi,et al.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons , 2000, Nature Neuroscience.

[41]  J. Weiner,et al.  Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Fiona E. N. LeBeau,et al.  A model of gamma‐frequency network oscillations induced in the rat CA3 region by carbachol in vitro , 2000, The European journal of neuroscience.

[43]  D. Kullmann,et al.  Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons , 2001, Nature Neuroscience.

[44]  Fiona E. N. LeBeau,et al.  Differential Expression of Synaptic and Nonsynaptic Mechanisms Underlying Stimulus-Induced Gamma Oscillations In Vitro , 2001, The Journal of Neuroscience.

[45]  R. Traub,et al.  Axo-Axonal Coupling A Novel Mechanism for Ultrafast Neuronal Communication , 2001, Neuron.

[46]  Miles A. Whittington,et al.  Impaired Electrical Signaling Disrupts Gamma Frequency Oscillations in Connexin 36-Deficient Mice , 2001, Neuron.

[47]  Roger A. Nicoll,et al.  Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors , 2001, Neuropharmacology.

[48]  J. Wess,et al.  Muscarinic Induction of Hippocampal Gamma Oscillations Requires Coupling of the M1 Receptor to Two Mixed Cation Currents , 2002, Neuron.

[49]  G. Buzsáki,et al.  Correlated Bursts of Activity in the Neonatal Hippocampus in Vivo , 2002, Science.

[50]  Miles A Whittington,et al.  Fast network oscillations induced by potassium transients in the rat hippocampus in vitro , 2002, The Journal of physiology.

[51]  J. White,et al.  Frequency selectivity of layer II stellate cells in the medial entorhinal cortex. , 2002, Journal of neurophysiology.

[52]  D. Lewis,et al.  Postnatal development of parvalbumin‐ and GABA transporter‐immunoreactive axon terminals in monkey prefrontal cortex , 2002, The Journal of comparative neurology.

[53]  Fiona E. N. LeBeau,et al.  A Model of Atropine‐Resistant Theta Oscillations in Rat Hippocampal Area CA1 , 2002, The Journal of physiology.

[54]  M. Frotscher,et al.  Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Hannah Monyer,et al.  Sharp wave-like activity in the hippocampus in vitro in mice lacking the gap junction protein connexin 36. , 2003, Journal of neurophysiology.

[56]  Miles A Whittington,et al.  Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro , 2003, Trends in Neurosciences.

[57]  Fiona E. N. LeBeau,et al.  GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Kenneth D Harris,et al.  Selective Impairment of Hippocampal Gamma Oscillations in Connexin-36 Knock-Out Mouse In Vivo , 2003, The Journal of Neuroscience.

[59]  A. Kovács,et al.  Loss of GABAergic neuronal phenotype in primary cerebellar cultures following blockade of glutamate reuptake , 2003, Brain Research.

[60]  M. Whittington,et al.  Gamma Oscillations Induced by Kainate Receptor Activation in the Entorhinal Cortex In Vitro , 2003, The Journal of Neuroscience.

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

[62]  R. Traub,et al.  Fast rhythmic bursting can be induced in layer 2/3 cortical neurons by enhancing persistent Na+ conductance or by blocking BK channels. , 2003, Journal of neurophysiology.

[63]  S. Rivkees,et al.  Lysophosphatidic acid regulates the proliferation and migration of olfactory ensheathing cells in vitro , 2003, Glia.

[64]  R. Traub,et al.  Distinct Roles for the Kainate Receptor Subunits GluR5 and GluR6 in Kainate-Induced Hippocampal Gamma Oscillations , 2004, The Journal of Neuroscience.

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

[66]  O. Paulsen,et al.  Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices , 2004, Neuropharmacology.

[67]  Miles A Whittington,et al.  Coexistence of gamma and high‐frequency oscillations in rat medial entorhinal cortex in vitro , 2004, The Journal of physiology.

[68]  Roger D. Traub,et al.  Simulation of Gamma Rhythms in Networks of Interneurons and Pyramidal Cells , 1997, Journal of Computational Neuroscience.

[69]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[70]  T. Woo,et al.  Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. , 2004, Archives of general psychiatry.

[71]  P. Maldonado,et al.  Neuronal assembly dynamics in the rat auditory cortex during reorganization induced by intracortical microstimulation , 1996, Experimental Brain Research.

[72]  G. Buzsáki,et al.  Early motor activity drives spindle bursts in the developing somatosensory cortex , 2004, Nature.

[73]  Miles A Whittington,et al.  Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. , 2004, Annual review of neuroscience.

[74]  M. Frotscher,et al.  Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry , 2004, Anatomy and Embryology.

[75]  Hannah Monyer,et al.  A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[76]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

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

[78]  Jessica A. Cardin,et al.  Stimulus-dependent gamma (30-50 Hz) oscillations in simple and complex fast rhythmic bursting cells in primary visual cortex. , 2005, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  Miles A Whittington,et al.  Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model , 2005, The Journal of physiology.

[80]  A. Sampson,et al.  Relationship of Brain-Derived Neurotrophic Factor and Its Receptor TrkB to Altered Inhibitory Prefrontal Circuitry in Schizophrenia , 2005, The Journal of Neuroscience.

[81]  Edward O. Mann,et al.  Perisomatic Feedback Inhibition Underlies Cholinergically Induced Fast Network Oscillations in the Rat Hippocampus In Vitro , 2005, Neuron.

[82]  Jessica A. Cardin,et al.  Stimulus-Dependent γ (30-50 Hz) Oscillations in Simple and Complex Fast Rhythmic Bursting Cells in Primary Visual Cortex , 2005, The Journal of Neuroscience.

[83]  Fiona E. N. LeBeau,et al.  Region-Specific Reduction in Entorhinal Gamma Oscillations and Parvalbumin-Immunoreactive Neurons in Animal Models of Psychiatric Illness , 2006, The Journal of Neuroscience.

[84]  Miles A Whittington,et al.  A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex , 2006, Proceedings of the National Academy of Sciences.

[85]  T. Bártfai,et al.  A Specific Role for NR2A-Containing NMDA Receptors in the Maintenance of Parvalbumin and GAD67 Immunoreactivity in Cultured Interneurons , 2006, The Journal of Neuroscience.

[86]  Erwan Dupont,et al.  Rapid developmental switch in the mechanisms driving early cortical columnar networks , 2006, Nature.

[87]  S. Nakagawa,et al.  Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidine-induced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats , 2007, Psychopharmacology.

[88]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[89]  Patrick R Hof,et al.  Gap junctions on hippocampal mossy fiber axons demonstrated by thin-section electron microscopy and freeze–fracture replica immunogold labeling , 2007, Proceedings of the National Academy of Sciences.

[90]  R. Tyzio,et al.  Timing of the Developmental Switch in GABAA Mediated Signaling from Excitation to Inhibition in CA3 Rat Hippocampus Using Gramicidin Perforated Patch and Extracellular Recordings , 2007, Epilepsia.

[91]  Peter Somogyi,et al.  Anti-Hebbian Long-Term Potentiation in the Hippocampal Feedback Inhibitory Circuit , 2007, Science.

[92]  Li I. Zhang,et al.  Heterosynaptic Scaling of Developing GABAergic Synapses: Dependence on Glutamatergic Input and Developmental Stage , 2007, The Journal of Neuroscience.

[93]  Kevin L Quick,et al.  Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase , 2007, Science.

[94]  Kenneth M. Johnson,et al.  Postnatal Phencyclidine Administration Selectively Reduces Adult Cortical Parvalbumin-Containing Interneurons , 2008, Neuropsychopharmacology.

[95]  H. Haas,et al.  Carbenoxolone impairs LTP and blocks NMDA receptors in murine hippocampus , 2008, Neuropharmacology.

[96]  Steven J. Middleton,et al.  Model of very fast (> 75 Hz) network oscillations generated by electrical coupling between the proximal axons of cerebellar Purkinje cells , 2008, The European journal of neuroscience.

[97]  Jozsi Z. Jalics,et al.  NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex , 2008, Proceedings of the National Academy of Sciences.

[98]  Roger D. Traub,et al.  High-Frequency Network Oscillations in Cerebellar Cortex , 2008, Neuron.

[99]  Adriano B. L. Tort,et al.  Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons , 2009, Proceedings of the National Academy of Sciences.

[100]  A. Thiele,et al.  Attention – oscillations and neuropharmacology , 2009, The European journal of neuroscience.

[101]  J. Kauer,et al.  Presynaptic plasticity: targeted control of inhibitory networks , 2009, Current Opinion in Neurobiology.

[102]  Anthony A Grace,et al.  A Loss of Parvalbumin-Containing Interneurons Is Associated with Diminished Oscillatory Activity in an Animal Model of Schizophrenia , 2009, The Journal of Neuroscience.

[103]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[104]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[105]  Eugenio Rodriguez,et al.  The development of neural synchrony reflects late maturation and restructuring of functional networks in humans , 2009, Proceedings of the National Academy of Sciences.

[106]  Gustavo Deco,et al.  Stochastic dynamics as a principle of brain function , 2009, Progress in Neurobiology.

[107]  W. Singer,et al.  Stabilization of visual responses through cholinergic activation , 2010, Neuroscience.