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

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

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    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 ? 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 ? oscillations in connexin36 knockout mice; without such gap junction blockade, ? 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 ? oscillations. We construct a network model of an experimental ? oscillation, known to be regulated by both types of electrical coupling. In our model, axonal electrical coupling is required for the ? oscillation to occur at all; interneuron dendritic gap junctions exert a modulatory effect.

    Original languageEnglish
    Pages (from-to)1370-1374
    Number of pages5
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume100
    Issue number3
    Early online date13 Jan 2003
    DOIs
    Publication statusPublished - 4 Feb 2003

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    Pyramidal Cells
    Interneurons
    Gap Junctions
    Knockout Mice
    Pharmacology
    Kainic Acid
    Dendrites
    Axons
    Hippocampus
    Theoretical Models
    connexin 36

    Cite this

    Traub, Roger D. ; Pais, Isabel ; Bibbig, Andrea ; LeBeau, Fiona E. N. ; Buhl, Eberhard H. ; Hormuzdi, Sheriar G. ; Monyer, Hannah ; Whittington, Miles A. / Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. In: Proceedings of the National Academy of Sciences of the United States of America. 2003 ; Vol. 100, No. 3. pp. 1370-1374.
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    Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. / Traub, Roger D.; Pais, Isabel; Bibbig, Andrea; LeBeau, Fiona E. N.; Buhl, Eberhard H.; Hormuzdi, Sheriar G.; Monyer, Hannah; Whittington, Miles A.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 100, No. 3, 04.02.2003, p. 1370-1374.

    Research output: Contribution to journalArticle

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    AU - Traub, Roger D.

    AU - Pais, Isabel

    AU - Bibbig, Andrea

    AU - LeBeau, Fiona E. N.

    AU - Buhl, Eberhard H.

    AU - Hormuzdi, Sheriar G.

    AU - Monyer, Hannah

    AU - Whittington, Miles A.

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    N2 - 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 ? 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 ? oscillations in connexin36 knockout mice; without such gap junction blockade, ? 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 ? oscillations. We construct a network model of an experimental ? oscillation, known to be regulated by both types of electrical coupling. In our model, axonal electrical coupling is required for the ? oscillation to occur at all; interneuron dendritic gap junctions exert a modulatory effect.

    AB - 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 ? 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 ? oscillations in connexin36 knockout mice; without such gap junction blockade, ? 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 ? oscillations. We construct a network model of an experimental ? oscillation, known to be regulated by both types of electrical coupling. In our model, axonal electrical coupling is required for the ? oscillation to occur at all; interneuron dendritic gap junctions exert a modulatory effect.

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