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Intervening inhibition underlies simple-cell receptive field structure in visual cortex

Nature Neuroscience volume 13, pages 89–96 (2010)Cite this article

Abstract

Synaptic inputs underlying spike receptive fields are important for understanding mechanisms of neuronal processing. Using whole-cell voltage-clamp recordings from neurons in mouse primary visual cortex, we examined the spatial patterns of their excitatory and inhibitory synaptic inputs evoked by On and Off stimuli. Neurons with either segregated or overlapped On/Off spike subfields had substantial overlaps between all the four synaptic subfields. The segregated receptive-field structures were generated by the integration of excitation and inhibition with a stereotypic 'overlap-but-mismatched' pattern: the peaks of excitatory On/Off subfields were separated and flanked colocalized peaks of inhibitory On/Off subfields. The small mismatch of excitation/inhibition led to an asymmetric inhibitory shaping of On/Off spatial tunings, resulting in a great enhancement of their distinctiveness. Thus, slightly separated On/Off excitation, together with intervening inhibition, can create simple-cell receptive-field structure and the dichotomy of receptive-field structures may arise from a fine-tuning of the spatial arrangement of synaptic inputs.

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Figure 1: Membrane potential (Vm) responses underlying SRF and ORF structures in layer 2/3 of the mouse V1.
Figure 2: Synaptic subfields examined by voltage-clamp recordings.
Figure 3: Grouping of cells on the basis of the structure of synaptic subfields.
Figure 4: Summary of the spatial relationships between synaptic subfields.
Figure 5: The inhibitory mechanism for the generation of the SRF structure.
Figure 6

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Acknowledgements

We thank A. Sampath and D. Li for their helpful suggestions. This work was supported by grants to H.W.T. from the US National Institutes of Health (EY018718 and EY019049) and The Karl Kirchgessner Foundation. L.I.Z. is supported by the Searle Scholar Program, the Klingenstein Foundation, and the David and Lucile Packard Foundation.

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Authors and Affiliations

  1. Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA

    Bao-hua Liu, Pingyang Li, Yujiao J Sun, Ya-tang Li, Li I Zhang & Huizhong Whit Tao

  2. Department of Physiology and Biophysics, Keck School of Medicine, University of Southern California, Los Angeles, California, USA

    Li I Zhang

  3. Department of Cell and Neurobiology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA

    Huizhong Whit Tao

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Correspondence to Li I Zhang or Huizhong Whit Tao.

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Liu, Bh., Li, P., Sun, Y. et al. Intervening inhibition underlies simple-cell receptive field structure in visual cortex. Nat Neurosci 13, 89–96 (2010). https://doi.org/10.1038/nn.2443

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