Activation of specific interneurons improves V1 feature selectivity and visual perception
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 p...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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Nature Publishing Group
2013
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| Online Access: | http://hdl.handle.net/1721.1/79761 https://orcid.org/0000-0002-0419-3351 |
| _version_ | 1826206961681563648 |
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| author | Lee, Seung-Hee Kwan, Alex C. Zhang, Siyu Phoumthipphavong, Victoria Flannery, John G. Masmanidis, Sotiris C. Taniguchi, Hiroki Huang, Z. Josh Zhang, Feng Deisseroth, Karl Dan, Yang Boyden, Edward |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Lee, Seung-Hee Kwan, Alex C. Zhang, Siyu Phoumthipphavong, Victoria Flannery, John G. Masmanidis, Sotiris C. Taniguchi, Hiroki Huang, Z. Josh Zhang, Feng Deisseroth, Karl Dan, Yang Boyden, Edward |
| author_sort | Lee, Seung-Hee |
| collection | MIT |
| description | 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 pattern1, 2, 3. 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 probes4, 5 and channelrhodopsin-2 (ChR2)-mediated optical activation6, 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 silencing7 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. |
| first_indexed | 2024-09-23T13:41:19Z |
| format | Article |
| id | mit-1721.1/79761 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T13:41:19Z |
| publishDate | 2013 |
| publisher | Nature Publishing Group |
| record_format | dspace |
| spelling | mit-1721.1/797612022-05-26T02:13:24Z Activation of specific interneurons improves V1 feature selectivity and visual perception Lee, Seung-Hee Kwan, Alex C. Zhang, Siyu Phoumthipphavong, Victoria Flannery, John G. Masmanidis, Sotiris C. Taniguchi, Hiroki Huang, Z. Josh Zhang, Feng Deisseroth, Karl Dan, Yang Boyden, Edward Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Massachusetts Institute of Technology. Media Laboratory Program in Media Arts and Sciences (Massachusetts Institute of Technology) Boyden, Edward Stuart 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 pattern1, 2, 3. 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 probes4, 5 and channelrhodopsin-2 (ChR2)-mediated optical activation6, 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 silencing7 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. 2013-08-01T19:52:05Z 2013-08-01T19:52:05Z 2012-08 2011-05 Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 http://hdl.handle.net/1721.1/79761 Lee, Seung-Hee, Alex C. Kwan, Siyu Zhang, et al. 2012 Activation of Specific Interneurons Improves V1 Feature Selectivity and Visual Perception. Nature 488(7411): 379–383. https://orcid.org/0000-0002-0419-3351 en_US http://dx.doi.org/10.1038/nature11312 Nature Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Nature Publishing Group PMC |
| spellingShingle | Lee, Seung-Hee Kwan, Alex C. Zhang, Siyu Phoumthipphavong, Victoria Flannery, John G. Masmanidis, Sotiris C. Taniguchi, Hiroki Huang, Z. Josh Zhang, Feng Deisseroth, Karl Dan, Yang Boyden, Edward Activation of specific interneurons improves V1 feature selectivity and visual perception |
| title | Activation of specific interneurons improves V1 feature selectivity and visual perception |
| title_full | Activation of specific interneurons improves V1 feature selectivity and visual perception |
| title_fullStr | Activation of specific interneurons improves V1 feature selectivity and visual perception |
| title_full_unstemmed | Activation of specific interneurons improves V1 feature selectivity and visual perception |
| title_short | Activation of specific interneurons improves V1 feature selectivity and visual perception |
| title_sort | activation of specific interneurons improves v1 feature selectivity and visual perception |
| url | http://hdl.handle.net/1721.1/79761 https://orcid.org/0000-0002-0419-3351 |
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