Literature DB >> 12525690

Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations.

Roger D Traub1, Isabel Pais, Andrea Bibbig, Fiona E N LeBeau, Eberhard H Buhl, Sheriar G Hormuzdi, Hannah Monyer, Miles A Whittington.   

Abstract

Electrical coupling between pyramidal cell axons, and between interneuron dendrites, have both been described in the hippocampus. What are the functional roles of the two types of coupling? Interneuron gap junctions enhance synchrony of gamma oscillations (25-70 Hz) in isolated interneuron networks and also in networks containing both interneurons and principal cells, as shown in mice with a knockout of the neuronal (primarily interneuronal) connexin36. We have recently shown that pharmacological gap junction blockade abolishes kainate-induced gamma oscillations in connexin36 knockout mice; without such gap junction blockade, gamma oscillations do occur in the knockout mice, albeit at reduced power compared with wild-type mice. As interneuronal dendritic electrical coupling is almost absent in the knockout mice, these pharmacological data indicate a role of axonal electrical coupling in generating the gamma oscillations. We construct a network model of an experimental gamma oscillation, known to be regulated by both types of electrical coupling. In our model, axonal electrical coupling is required for the gamma oscillation to occur at all; interneuron dendritic gap junctions exert a modulatory effect.

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Year:  2003        PMID: 12525690      PMCID: PMC298779          DOI: 10.1073/pnas.0337529100

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  29 in total

1.  Two networks of electrically coupled inhibitory neurons in neocortex.

Authors:  J R Gibson; M Beierlein; B W Connors
Journal:  Nature       Date:  1999-11-04       Impact factor: 49.962

2.  High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions.

Authors:  R D Traub; D Schmitz; J G Jefferys; A Draguhn
Journal:  Neuroscience       Date:  1999       Impact factor: 3.590

3.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons.

Authors:  G Tamás; E H Buhl; A Lörincz; P Somogyi
Journal:  Nat Neurosci       Date:  2000-04       Impact factor: 24.884

4.  Electrical coupling and excitatory synaptic transmission between rhythmogenic respiratory neurons in the preBötzinger complex.

Authors:  J C Rekling; X M Shao; J L Feldman
Journal:  J Neurosci       Date:  2000-12-01       Impact factor: 6.167

5.  A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro.

Authors:  R D Traub; A Bibbig; A Fisahn; F E LeBeau; M A Whittington; E H Buhl
Journal:  Eur J Neurosci       Date:  2000-11       Impact factor: 3.386

6.  Connexin expression in electrically coupled postnatal rat brain neurons.

Authors:  L Venance; A Rozov; M Blatow; N Burnashev; D Feldmeyer; H Monyer
Journal:  Proc Natl Acad Sci U S A       Date:  2000-08-29       Impact factor: 11.205

7.  A network of fast-spiking cells in the neocortex connected by electrical synapses.

Authors:  M Galarreta; S Hestrin
Journal:  Nature       Date:  1999-11-04       Impact factor: 49.962

8.  Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons.

Authors:  A Semyanov; D M Kullmann
Journal:  Nat Neurosci       Date:  2001-07       Impact factor: 24.884

9.  Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36.

Authors:  M R Deans; J R Gibson; C Sellitto; B W Connors; D L Paul
Journal:  Neuron       Date:  2001-08-16       Impact factor: 17.173

10.  Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization.

Authors:  C Bou-Flores; A J Berger
Journal:  J Neurophysiol       Date:  2001-04       Impact factor: 2.714

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  41 in total

1.  Network recruitment to coherent oscillations in a hippocampal computer model.

Authors:  William C Stacey; Abba Krieger; Brian Litt
Journal:  J Neurophysiol       Date:  2011-01-27       Impact factor: 2.714

2.  GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations.

Authors:  R D Traub; M O Cunningham; T Gloveli; F E N LeBeau; A Bibbig; E H Buhl; M A Whittington
Journal:  Proc Natl Acad Sci U S A       Date:  2003-09-05       Impact factor: 11.205

3.  A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro.

Authors:  Mark O Cunningham; Miles A Whittington; Andrea Bibbig; Anita Roopun; Fiona E N LeBeau; Angelika Vogt; Hannah Monyer; Eberhard H Buhl; Roger D Traub
Journal:  Proc Natl Acad Sci U S A       Date:  2004-04-21       Impact factor: 11.205

4.  Mechanisms of very fast oscillations in networks of axons coupled by gap junctions.

Authors:  Erin Munro; Christoph Börgers
Journal:  J Comput Neurosci       Date:  2010-04-13       Impact factor: 1.621

Review 5.  Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back.

Authors:  Edward O Mann; Catrin A Radcliffe; Ole Paulsen
Journal:  J Physiol       Date:  2004-11-11       Impact factor: 5.182

6.  The role of distal dendritic gap junctions in synchronization of mitral cell axonal output.

Authors:  M Migliore; M L Hines; Gordon M Shepherd
Journal:  J Comput Neurosci       Date:  2005 Mar-Apr       Impact factor: 1.621

Review 7.  Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model.

Authors:  Roger D Traub; Andrea Bibbig; Fiona E N LeBeau; Mark O Cunningham; Miles A Whittington
Journal:  J Physiol       Date:  2004-10-15       Impact factor: 5.182

Review 8.  Kainate receptors and rhythmic activity in neuronal networks: hippocampal gamma oscillations as a tool.

Authors:  André Fisahn
Journal:  J Physiol       Date:  2004-10-28       Impact factor: 5.182

9.  Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex.

Authors:  Anna Simon; Szabolcs Oláh; Gábor Molnár; János Szabadics; Gábor Tamás
Journal:  J Neurosci       Date:  2005-07-06       Impact factor: 6.167

10.  Pannexins, a family of gap junction proteins expressed in brain.

Authors:  Roberto Bruzzone; Sheriar G Hormuzdi; Michael T Barbe; Anne Herb; Hannah Monyer
Journal:  Proc Natl Acad Sci U S A       Date:  2003-11-03       Impact factor: 11.205

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