Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex

Electrical synapses contribute to the generation of synchronous activity in neuronal networks. Several types of cortical GABAergic neurons acting via postsynaptic GABAA receptors also form electrical synapses with interneurons of the same class, suggesting that synchronization through gap junctions could be limited to homogenous interneuron populations. Neurogliaform cells elicit combined GABAA and GABAB receptor-mediated postsynaptic responses in cortical pyramidal cells, but it is not clear whether neurogliaform cells are involved in networks linked by electrical coupling. We recorded from pairs, triplets, and quadruplets of cortical neurons in layers 2 and 3 of rat somatosensory cortex (postnatal day 20-35). Neurogliaform cells eliciting slow IPSPs on pyramidal cells also triggered divergent electrical coupling potentials on interneurons. Neurogliaform cells were electrically coupled to other neurogliaform cells, basket cells, regular-spiking nonpyramidal cells, to an axoaxonic cell, and to various unclassified interneurons showing diverse firing patterns and morphology. Electrical interactions were mediated by one or two electron microscopically verified gap junctions linking the somatodendritic domain of the coupled cells. Our results suggest that neurogliaform cells have a unique position in the cortical circuit. Apart from eliciting combined GABAA and GABAB receptor-mediated inhibition on pyramidal cells, neurogliaform cells establish electrical synapses and link multiple networks formed by gap junctions restricted to a particular class of interneuron. Widespread electrical connections might enable neurogliaform cells to monitor the activity of different interneurons acting on GABAA receptors at various regions of target cells.

[1]  K. Willecke,et al.  Expression and functions of neuronal gap junctions , 2005, Nature Reviews Neuroscience.

[2]  P. Somogyi,et al.  Input and frequency‐specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin , 2004, The European journal of neuroscience.

[3]  B. Ermentrout,et al.  Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. L. Schnapf,et al.  Electrical coupling between red and green cones in primate retina , 2004, Nature Neuroscience.

[5]  M. Bennett,et al.  Electrical Coupling and Neuronal Synchronization in the Mammalian Brain , 2004, Neuron.

[6]  Eun-Jin Lee,et al.  The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina , 2003, The European journal of neuroscience.

[7]  T. Kosaka,et al.  Ultrastructural study of gap junctions between dendrites of parvalbumin-containing GABAergic neurons in various neocortical areas of the adult rat , 2003, Neuroscience.

[8]  M. Whittington,et al.  A Novel Network of Multipolar Bursting Interneurons Generates Theta Frequency Oscillations in Neocortex , 2003, Neuron.

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

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

[11]  Hannah Monyer,et al.  Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  S. Hestrin,et al.  Synaptic Interactions of Late-Spiking Neocortical Neurons in Layer 1 , 2003, The Journal of Neuroscience.

[13]  Michael A Long,et al.  Rhythmicity without Synchrony in the Electrically Uncoupled Inferior Olive , 2002, The Journal of Neuroscience.

[14]  Edward N Pugh,et al.  Connexin36 Forms Synapses Essential for Night Vision , 2002, Neuron.

[15]  B. Connors,et al.  The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex , 2002, The Journal of Neuroscience.

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

[17]  B. Connors,et al.  Synchronous Activity of Inhibitory Networks in Neocortex Requires Electrical Synapses Containing Connexin36 , 2001, Neuron.

[18]  R. Weiler,et al.  Visual Transmission Deficits in Mice with Targeted Disruption of the Gap Junction Gene Connexin36 , 2001, The Journal of Neuroscience.

[19]  G. Tamás,et al.  β and γ Frequency Synchronization by Dendritic GABAergic Synapses and Gap Junctions in a Network of Cortical Interneurons , 2001, The Journal of Neuroscience.

[20]  S. Hestrin,et al.  Electrical synapses between Gaba-Releasing interneurons , 2001, Nature Reviews Neuroscience.

[21]  D. Feldmeyer,et al.  Connexin expression in electrically coupled postnatal rat brain neurons. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Carson C. Chow,et al.  Dynamics of Spiking Neurons with Electrical Coupling , 2000, Neural Computation.

[23]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[25]  Marla B Feller,et al.  Neurotransmitters and gap junctions in developing neural circuits , 2000, Brain Research Reviews.

[26]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[27]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[28]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[29]  A. Destexhe,et al.  Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices , 1999, Neuroscience.

[30]  P. Calabresi,et al.  Morphological and functional study of dwarf neurons in the rat striatum , 1998, The European journal of neuroscience.

[31]  Maria V. Sanchez-Vives,et al.  Functional dynamics of GABAergic inhibition in the thalamus. , 1997, Science.

[32]  Y. Kubota,et al.  GABAergic cell subtypes and their synaptic connections in rat frontal cortex. , 1997, Cerebral cortex.

[33]  T. Wiesel.  Neural Mechanisms of Visual Perception , 1997 .

[34]  M. C. Angulo,et al.  Molecular and Physiological Diversity of Cortical Nonpyramidal Cells , 1997, The Journal of Neuroscience.

[35]  P. Somogyi,et al.  Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. , 1997, The Journal of physiology.

[36]  S. Hestrin,et al.  Morphology and Physiology of Cortical Neurons in Layer I , 1996, The Journal of Neuroscience.

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

[38]  Y. Kawaguchi.  Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  I. Mody,et al.  Bridging the cleft at GABA synapses in the brain , 1994, Trends in Neurosciences.

[40]  J. Rinzel,et al.  Rhythmogenic effects of weak electrotonic coupling in neuronal models. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[41]  P. Somogyi,et al.  Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. , 1990, Brain : a journal of neurology.

[42]  B W Connors,et al.  Carbon dioxide sensitivity of dye coupling among glia and neurons of the neocortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  P. Schwartzkroin,et al.  Electrotonic and dye coupling in hippocampal CA1 pyramidal cells in vitro , 1982, Neuroscience.

[44]  M. Gutnick,et al.  Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. , 1981, Science.

[45]  P. Somogyi.  A specific ‘axo-axonal’ interneuron in the visual cortex of the rat , 1977, Brain Research.

[46]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[47]  M. Arbib,et al.  Conceptual models of neural organization. , 1974, Neurosciences Research Program bulletin.

[48]  J. Sloper,et al.  Gap junctions between dendrites in the primate neocortex. , 1972, Brain research.

[49]  F. Valverde.  Short axon neuronal subsystems in the visual cortex of the monkey. , 1971, The International journal of neuroscience.