Long-Range GABAergic Connections Distributed throughout the Neocortex and their Possible Function

Features and functions of long-range GABAergic projection neurons in the developing cerebral cortex have been reported previously, although until now their significance in the adult cerebral cortex has remained uncertain. The septo-hippocampal circuit is one exception – in this system, long-range mature GABAergic projection neurons have been well analyzed and their contribution to the generation of theta-oscillatory behavior in the hippocampus has been documented. To have a clue to the function of the GABAergic projection neurons in the neocortex, we view how the long-range GABAergic projections are integrated in the cortico-cortical, cortico-fugal, and afferent projections in the cerebral cortex. Then, we consider the possibility that the GABAergic projection neurons are involved in the generation, modification, and/or synchronization of oscillations in mature neocortical neuron activity. When markers that identify the GABAergic projection neurons are examined in anatomical and developmental studies, it is clear that neuronal NO synthetase (nNOS)-immunoreactivity can readily identify GABAergic projection neurons. GABAergic projection neurons account for 0.5% of the neocortical GABAergic neurons. To elucidate the role of the GABAergic projection neurons in the neocortex, it will be necessary to clarify the network constructed by nNOS-positive GABAergic projection neurons and their postsynaptic targets. Thus, our long-range goals will be to label and manipulate (including deleting) the GABAergic projection neurons using genetic tools driven by a nNOS promoter. We recognize that this may be a complex endeavor, as most excitatory neurons in the murine neocortex express nNOS transiently. Nevertheless, additional studies characterizing long-range GABAergic projection neurons will have great value to the overall understanding of mature cortical function.

[1]  A. Waisman,et al.  A novel in vivo inducible dendritic cell ablation model in mice. , 2010, Biochemical and biophysical research communications.

[2]  Heiko J Luhmann,et al.  The subplate and early cortical circuits. , 2010, Annual review of neuroscience.

[3]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[4]  I. Módy,et al.  Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons , 2009, Nature Neuroscience.

[5]  Y. Yanagawa,et al.  Two Separate Subtypes of Early Non-Subplate Projection Neurons in the Developing Cerebral Cortex of Rodents , 2009, Frontiers in neuroanatomy.

[6]  Shigeyoshi Higo,et al.  Subtypes of GABAergic Neurons Project Axons in the Neocortex , 2009, Front. Neuroanat..

[7]  S. Jinno.  Structural Organization of Long-Range GABAergic Projection System of the Hippocampus , 2009, Front. Neuroanat..

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

[9]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[10]  Michael Z. Lin,et al.  Characterization of engineered channelrhodopsin variants with improved properties and kinetics. , 2009, Biophysical journal.

[11]  K. Deisseroth,et al.  eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications , 2008, Brain cell biology.

[12]  Y. Kawaguchi,et al.  Two distinct activity patterns of fast-spiking interneurons during neocortical UP states , 2008, Proceedings of the National Academy of Sciences.

[13]  Kathleen S Rockland,et al.  Long‐distance corticocortical GABAergic neurons in the adult monkey white and gray matter , 2007, The Journal of comparative neurology.

[14]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[15]  Sébastien Vigneau,et al.  Multiple origins of Cajal-Retzius cells at the borders of the developing pallium , 2005, Nature Neuroscience.

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

[17]  M. Fabri,et al.  Glutamic acid decarboxylase immunoreactivity in callosal projecting neurons of cat and rat somatic sensory areas , 2004, Neuroscience.

[18]  J. Rossier,et al.  Cortical GABA Interneurons in Neurovascular Coupling: Relays for Subcortical Vasoactive Pathways , 2004, The Journal of Neuroscience.

[19]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[20]  T. Kosaka,et al.  Parvalbumin is expressed in glutamatergic and GABAergic corticostriatal pathway in mice , 2004, The Journal of comparative neurology.

[21]  T. Kaneko,et al.  GABAergic basal forebrain neurons that express receptor for neurokinin B and send axons to the cerebral cortex , 2004, The Journal of comparative neurology.

[22]  S. Nakanishi,et al.  Generation of Reelin-Positive Marginal Zone Cells from the Caudomedial Wall of Telencephalic Vesicles , 2004, The Journal of Neuroscience.

[23]  T. Kaneko,et al.  Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse , 2003, The Journal of comparative neurology.

[24]  S. Kalinichenko,et al.  Subcortical White Matter Interstitial Cells: Their Connections, Neurochemical Specialization, and Role in the Histogenesis of the Cortex , 2003, Neuroscience and Behavioral Physiology.

[25]  B. Clancy,et al.  Structure and projections of white matter neurons in the postnatal rat visual cortex , 2001, The Journal of comparative neurology.

[26]  D. Javitt,et al.  Nitric oxide synthase interneurons in the monkey cerebral cortex are subsets of the somatostatin, neuropeptide Y, and calbindin cells , 2000, Brain Research.

[27]  Roger D. Traub,et al.  A Model of High-Frequency Ripples in the Hippocampus Based on Synaptic Coupling Plus Axon–Axon Gap Junctions between Pyramidal Neurons , 2000, The Journal of Neuroscience.

[28]  J. Stone,et al.  Major glutamatergic projection from subplate into visual cortex during development , 1998, The Journal of comparative neurology.

[29]  A. Fairén,et al.  Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex , 1998, The Journal of comparative neurology.

[30]  M. Moskowitz,et al.  Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo , 1998, Neuroscience.

[31]  N. Tamamaki,et al.  Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone , 1997, The Journal of Neuroscience.

[32]  Leyuan Shi,et al.  Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. , 1997, Science.

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

[34]  A. Burkhalter,et al.  Three distinct families of GABAergic neurons in rat visual cortex. , 1997, Cerebral cortex.

[35]  R. Baughman,et al.  GABAergic Transcallosal Neurons in Developing Rat Neocortex , 1997, The European journal of neuroscience.

[36]  T. Freund,et al.  Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. , 1997, The Journal of physiology.

[37]  Floris G. Wouterlood,et al.  GABAergic Presubicular Projections to the Medial Entorhinal Cortex of the Rat , 1997, The Journal of Neuroscience.

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

[39]  A. Keller,et al.  Intrinsic inhibitory pathways in mouse barrel cortex. , 1996, Neuroreport.

[40]  L. Garey,et al.  NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. , 1996, Cerebral cortex.

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

[42]  P A Salin,et al.  Electrophysiological mapping of GABAA receptor-mediated inhibition in adult rat somatosensory cortex. , 1996, Journal of neurophysiology.

[43]  W. Singer,et al.  Integrator or coincidence detector? The role of the cortical neuron revisited , 1996, Trends in Neurosciences.

[44]  Y. Gonchar,et al.  GABA-immunopositive neurons in rat neocortex with contralateral projections to S-I , 1995, Brain Research.

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

[46]  P. Lowenstein,et al.  Neocortex provides direct synaptic input to interstitial neurons of the intermediate zone of kittens and white matter of cats: A light and electron microscopic study , 1994, The Journal of comparative neurology.

[47]  Y. Kubota,et al.  Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex , 1994, Brain Research.

[48]  K. Albus,et al.  The Topography of Tangential Inhibitory Connections in the Postnatally Developing and Mature Striate Cortex of the Cat , 1994, The European journal of neuroscience.

[49]  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.

[50]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[51]  A. Burkhalter,et al.  Organization of long-range inhibitory connections with rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  T. Freund,et al.  Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: Their immunoreactivity for GABA and projection to the medial septum , 1992, Neuroscience.

[53]  M. Marín‐Padilla,et al.  Neocortical Development , 1992, Journal of Cognitive Neuroscience.

[54]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[55]  A. Heynen,et al.  Induction of RSA-like oscillations in both the in-vitro and in-vivo hippocampus. , 1991, Neuroreport.

[56]  A. Peters,et al.  Transcallosal non‐pyramidal cell projections from visual cortex in the cat , 1990, The Journal of comparative neurology.

[57]  N. Mizuno,et al.  Direct projections of non-pyramidal neurons of Ammon's horn to the amygdala and the entorhinal cortex , 1990, Neuroscience Letters.

[58]  J K Chapin,et al.  A major direct GABAergic pathway from zona incerta to neocortex. , 1990, Science.

[59]  C. Shatz,et al.  Subplate neurons pioneer the first axon pathway from the cerebral cortex. , 1989, Science.

[60]  C. Shatz,et al.  The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  C. Shatz,et al.  Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population , 1989, The Journal of comparative neurology.

[62]  T. Freund,et al.  GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus , 1988, Nature.

[63]  A. Fairén,et al.  Transient GABA-like immunoreactive axons in the corpus callosum of perinatal rats , 1988, Neuroscience Letters.

[64]  R. Shigemoto,et al.  Direct projections of non-pyramidal neurons of Ammon's horn to the supramammillary region in the cat , 1988, Brain Research.

[65]  R Porter,et al.  Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. , 1988, The Journal of physiology.

[66]  Yasuo Kawaguchi,et al.  Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin , 1987, Brain Research.

[67]  G. V. Goddard,et al.  Septohippocampal and commissural pathways antagonistically control inhibitory interneurons in the dentate gyrus , 1987, Brain Research.

[68]  C. Shatz,et al.  Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons , 1987, Nature.

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

[70]  K. Fujimori,et al.  Intermediate zone and intermediate zone neurons. Do IZ neurons acts as pioneers for layer V neurons in rats? , 1997, Developmental neuroscience.

[71]  L. Garey,et al.  Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. , 1997, Journal fur Hirnforschung.

[72]  Nobuaki Tamamaki,et al.  Intermediate Zone and Intermediate Zone Neurons , 1997 .

[73]  M. Fabri,et al.  Glutamate decarboxylase immunoreactivity in corticocortical projecting neurons of rat somatic sensory cortex. , 1996, Neuroscience.

[74]  Carla J. Shatz,et al.  The Role of the Subplate in the Development of the Mammalian Telencephalon , 1988 .

[75]  A. Peters,et al.  Development and maturation of cerebral cortex , 1988 .