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Visual input evokes transient and strong shunting inhibition in visual cortical neurons

Nature volume 393, pages 369–373 (1998)Cite this article

Abstract

The function and nature of inhibition of neurons in the visual cortex have been the focus of both experimental and theoretical investigations1,2,3,4,5,6,7. There are two ways in which inhibition can suppress synaptic excitation2,8. In hyperpolarizing inhibition, negative and positive currents sum linearly to produce a net change in membrane potential. In contrast, shunting inhibition acts nonlinearly by causing an increase in membrane conductance; this divides the amplitude of the excitatory response. Visually evoked changes in membrane conductance have been reported to be nonsignificant or weak, supporting the hyperpolarization mode of inhibition3,9,10,11,12. Here we present a new approach to studying inhibition that is based on in vivo whole-cell voltage clamping. This technique allows the continuous measurement of conductance dynamics during visual activation. We show, in neurons of cat primary visual cortex, that the response to optimally orientated flashed bars can increase the somatic input conductance to more than three times that of the resting state. The short latency of the visually evoked peak of conductance, and its apparent reversal potential suggest a dominant contribution from γ-aminobutyric acid ((GABA)A) receptor-mediated synapses. We propose that nonlinear shunting inhibition may act during the initial stage of visual cortical processing, setting the balance between opponent ‘On’ and ‘Off’ responses in different locations of the visual receptive field.

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Figure 1: The visually evoked relative change in input conductance ΔGin(t) and its apparent reversal potential Erev(t) are derived from the current waveforms measured by two to four voltage-clamp protocols, illustrated here for the subthreshold response of an end-stopped simple cell to an Off transition of a flashing bar (full response is shown in Fig. 2e , cell 4, position 8).
Figure 2: Response–plane receptive field maps based on spike activity (peri-stimulus histograms, PSTHs, left column), voltage (centre) and conductance (right) measurements.
Figure 3: Relationships between amplitude, latency and apparent reversal potential of the maximum values of relative ΔGin(t).
Figure 4: Phase plots of relative ΔGin(t) versus Erev(t) for positions in the receptive fields (indicated in corner of each graph) eliciting the largest conductance or spike responses.

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Acknowledgements

We thank V. Bringuier and F. Chavane for help with some experiments; N. Gazeres, T. Bal, K. Grant, R. Kado, P.-M. Lledo, N. Ropert and D. Shulz for comments; and G. Sadoc and L. Glaeser for software assistance. This work was supported by HFSP and GIS Cognisciences grants (to Y.F.). L.J.B.G. was funded by fellowships from the CNRS and Foundations Philippe and Fyssen.

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  1. Equipe Cognisciences, Institut Alfred Fessard, CNRS, Avenue de la Terrasse, 91198, Gif sur Yvette, France

    Lyle J. Borg-Graham, Cyril Monier & Yves Frégnac

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  1. Lyle J. Borg-Graham
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Correspondence to Yves Frégnac.

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Borg-Graham, L., Monier, C. & Frégnac, Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393, 369–373 (1998). https://doi.org/10.1038/30735

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