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Activation of specific interneurons improves V1 feature selectivity and visual perception

Lee, Seung-Hee and Kwan, Alex C. and Zhang, Siyu and Phoumthipphavong, Victoria and Flannery, John G. and Masmanidis, Sotiris C. and Taniguchi, Hiroki and Huang, Z. Josh and Zhang, Feng and Boyden, Edward S. and Deisseroth, Karl and Dan, Yang (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature, 488 (7411). pp. 379-383. ISSN 0028-0836. PMCID PMC3435450. doi:10.1038/nature11312.

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Inhibitory interneurons are essential components of the neural circuits underlying various brain functions. In the neocortex, a large diversity of GABA (γ-aminobutyric acid) interneurons has been identified on the basis of their morphology, molecular markers, biophysical properties and innervation pattern. However, how the activity of each subtype of interneurons contributes to sensory processing remains unclear. Here we show that optogenetic activation of parvalbumin-positive (PV^+) interneurons in the mouse primary visual cortex (V1) sharpens neuronal feature selectivity and improves perceptual discrimination. Using multichannel recording with silicon probes and channelrhodopsin-2 (ChR2)-mediated optical activation, we found that increased spiking of PV^+ interneurons markedly sharpened orientation tuning and enhanced direction selectivity of nearby neurons. These effects were caused by the activation of inhibitory neurons rather than a decreased spiking of excitatory neurons, as archaerhodopsin-3 (Arch)-mediated optical silencing of calcium/calmodulin-dependent protein kinase IIα (CAMKIIα)-positive excitatory neurons caused no significant change in V1 stimulus selectivity. Moreover, the improved selectivity specifically required PV^+ neuron activation, as activating somatostatin or vasointestinal peptide interneurons had no significant effect. Notably, PV+ neuron activation in awake mice caused a significant improvement in their orientation discrimination, mirroring the sharpened V1 orientation tuning. Together, these results provide the first demonstration that visual coding and perception can be improved by increased spiking of a specific subtype of cortical inhibitory interneurons.

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Additional Information:© 2012 Macmillan Publishers Limited. Received 18 May 2011; accepted 11 June 2012; published online 8 August 2012. We thank M. Goard, L. Pinto, M. Xu and M. Viesel for help with experimental setup, A. Kaluszka for help with data analysis and H. Alitto and M. Poo for discussion and comments on the manuscript. This work was supported by National Institutes of Health grants R01 EY018861 and PN2 EY018241 and National Science Foundation grant 22250400-42533. Author Contributions: S.-H.L. and Y.D. conceived and designed the experiments. S.-H.L. performed and organized all the experiments. A.C.K. developed the head-fixed awake mouse preparation and behavioural task setup. S.Z. performed whole-cell recording experiments. V.P. performed some of the virus injection and head-plate implant surgeries. J.G.F. supported viral vector preparation. S.C.M. manufactured silicon probe (type II). H.T. and Z.J.H. generated SOM-Cre and VIP-Cre mouse lines. E.S.B. generated the Arch–eGFP viral vector. F.Z. and K.D. developed the ChR2–eYFP viral vector. S.-H.L., A.K. and Y.D. analysed the data. S.-H.L. and Y.D. wrote the manuscript. All authors discussed the results and commented on the manuscript.
Funding AgencyGrant Number
NIHR01 EY018861
NIHPN2 EY018241
Subject Keywords:Neuroscience; Animal behaviour; Physiology
Issue or Number:7411
PubMed Central ID:PMC3435450
Record Number:CaltechAUTHORS:20120913-113130000
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:34065
Deposited By: Jason Perez
Deposited On:13 Sep 2012 21:22
Last Modified:09 Nov 2021 23:06

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