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New Research, Sensory and Motor Systems

Different inhibitory interneuron cell classes make distinct contributions to visual contrast perception

Jackson J. Cone, Megan D. Scantlen, Mark H. Histed and John H.R. Maunsell
eNeuro 26 February 2019, ENEURO.0337-18.2019; https://doi.org/10.1523/ENEURO.0337-18.2019
Jackson J. Cone
Department of Neurobiology, University of Chicago, Chicago, IL, USA
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Megan D. Scantlen
Department of Neurobiology, University of Chicago, Chicago, IL, USA
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Mark H. Histed
Unit on Neural Computation and Behavior, National Institute of Mental Health, Bethesda, MD, USA
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John H.R. Maunsell
Department of Neurobiology, University of Chicago, Chicago, IL, USA
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Abstract

While recent work has revealed how different inhibitory interneurons influence responses of cortical neurons to sensory stimuli, little is known about their distinct contributions to sensory perception. Here, we optogenetically activated different genetically defined interneurons (parvalbumin (PV), somatostatin (SST), vasoactive intestinal peptide (VIP)) in visual cortex (V1) of mice working at threshold in a contrast increment detection task. The visual stimulus was paired with optogenetic stimulation to assess how enhancing V1 inhibitory neuron activity during visual processing altered task performance. PV or SST activation impaired, while VIP stimulation improved, contrast increment detection. The impairment produced by PV or SST activation persisted over several weeks of testing. In contrast, mice learned to reliably detect VIP activation in the absence of any natural visual stimulus. Thus, different inhibitory signals make distinct contributions to visual contrast perception.

Significance Statement Inhibitory interneurons are diverse and influence sensory responses through multiple mechanisms. Currently there is little consensus on how different inhibitory signals affect sensory perception. Here, we investigated how genetically defined interneuron subclasses (parvalbumin (PV), somatostatin (SST), and vasoactive intestinal peptide (VIP)) influence visual contrast perception. Mice were trained to work at threshold in a visual contrast detection task and interneuron activity was enhanced using ChannelRhodopsin-2 on a subset of trials. Different interneuron classes influenced perception in distinct ways. PV and SST stimulation impaired, whereas VIP stimulation improved visual contrast perception. With training, mice learned to perceive VIP activation in the absence of natural visual stimulation. These data highlight how different inhibitory signals affect the transformation of sensory-evoked responses into percepts.

  • inhibition
  • interneurons
  • mouse
  • psychophysics
  • vision
  • visual contrast

Footnotes

  • Authors report no conflict of interest.

  • This work was supported by NIH Grant U01-NS090576 (JHRM) and an Arnold O. Beckman Postdoctoral Fellowship from the Arnold and Mabel Beckman Foundation (JJC).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Different inhibitory interneuron cell classes make distinct contributions to visual contrast perception
Jackson J. Cone, Megan D. Scantlen, Mark H. Histed, John H.R. Maunsell
eNeuro 26 February 2019, ENEURO.0337-18.2019; DOI: 10.1523/ENEURO.0337-18.2019

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Different inhibitory interneuron cell classes make distinct contributions to visual contrast perception
Jackson J. Cone, Megan D. Scantlen, Mark H. Histed, John H.R. Maunsell
eNeuro 26 February 2019, ENEURO.0337-18.2019; DOI: 10.1523/ENEURO.0337-18.2019
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Keywords

  • inhibition
  • interneurons
  • mouse
  • psychophysics
  • vision
  • visual contrast

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