Fast modulation of visual perception by basal forebrain cholinergic neurons

The basal forebrain provides the primary source of cholinergic input to the cortex, and it has a crucial function in promoting wakefulness and arousal. However, whether rapid changes in basal forebrain neuron spiking in awake animals can dynamically influence sensory perception is unclear. Here we s...

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Main Authors: Pinto, Lucas, Estandian, Daniel, Xu, Min, Lee, Seung-Hee, Feng, Guoping, Dan, Yang, Goard, Michael J., Kwan, Alex C., Harrison, Thomas C.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: Nature Publishing Group 2016
Online Access:http://hdl.handle.net/1721.1/102414
https://orcid.org/0000-0002-8021-277X
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author Pinto, Lucas
Estandian, Daniel
Xu, Min
Lee, Seung-Hee
Feng, Guoping
Dan, Yang
Goard, Michael J.
Kwan, Alex C.
Harrison, Thomas C.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Pinto, Lucas
Estandian, Daniel
Xu, Min
Lee, Seung-Hee
Feng, Guoping
Dan, Yang
Goard, Michael J.
Kwan, Alex C.
Harrison, Thomas C.
author_sort Pinto, Lucas
collection MIT
description The basal forebrain provides the primary source of cholinergic input to the cortex, and it has a crucial function in promoting wakefulness and arousal. However, whether rapid changes in basal forebrain neuron spiking in awake animals can dynamically influence sensory perception is unclear. Here we show that basal forebrain cholinergic neurons rapidly regulate cortical activity and visual perception in awake, behaving mice. Optogenetic activation of the cholinergic neurons or their V1 axon terminals improved performance of a visual discrimination task on a trial-by-trial basis. In V1, basal forebrain activation enhanced visual responses and desynchronized neuronal spiking; these changes could partly account for the behavioral improvement. Conversely, optogenetic basal forebrain inactivation decreased behavioral performance, synchronized cortical activity and impaired visual responses, indicating the importance of cholinergic activity in normal visual processing. These results underscore the causal role of basal forebrain cholinergic neurons in fast, bidirectional modulation of cortical processing and sensory perception.
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spelling mit-1721.1/1024142022-10-03T07:26:19Z Fast modulation of visual perception by basal forebrain cholinergic neurons Pinto, Lucas Estandian, Daniel Xu, Min Lee, Seung-Hee Feng, Guoping Dan, Yang Goard, Michael J. Kwan, Alex C. Harrison, Thomas C. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Picower Institute for Learning and Memory Goard, Michael J. Feng, Guoping The basal forebrain provides the primary source of cholinergic input to the cortex, and it has a crucial function in promoting wakefulness and arousal. However, whether rapid changes in basal forebrain neuron spiking in awake animals can dynamically influence sensory perception is unclear. Here we show that basal forebrain cholinergic neurons rapidly regulate cortical activity and visual perception in awake, behaving mice. Optogenetic activation of the cholinergic neurons or their V1 axon terminals improved performance of a visual discrimination task on a trial-by-trial basis. In V1, basal forebrain activation enhanced visual responses and desynchronized neuronal spiking; these changes could partly account for the behavioral improvement. Conversely, optogenetic basal forebrain inactivation decreased behavioral performance, synchronized cortical activity and impaired visual responses, indicating the importance of cholinergic activity in normal visual processing. These results underscore the causal role of basal forebrain cholinergic neurons in fast, bidirectional modulation of cortical processing and sensory perception. National Institute of Mental Health (U.S.) (Grant RC1-MH088434) National Institute of Neurological Disorders and Stroke (U.S.) (Ruth L. Kirschstein National Research Service Award F31NS059258) 2016-05-05T00:30:35Z 2016-05-05T00:30:35Z 2013-10 2013-04 Article http://purl.org/eprint/type/JournalArticle 1097-6256 1546-1726 http://hdl.handle.net/1721.1/102414 Pinto, Lucas, Michael J Goard, Daniel Estandian, Min Xu, Alex C Kwan, Seung-Hee Lee, Thomas C Harrison, Guoping Feng, and Yang Dan. “Fast Modulation of Visual Perception by Basal Forebrain Cholinergic Neurons.” Nature Neuroscience 16, no. 12 (October 27, 2013): 1857–63. https://orcid.org/0000-0002-8021-277X en_US http://dx.doi.org/10.1038/nn.3552 Nature Neuroscience 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 Pinto, Lucas
Estandian, Daniel
Xu, Min
Lee, Seung-Hee
Feng, Guoping
Dan, Yang
Goard, Michael J.
Kwan, Alex C.
Harrison, Thomas C.
Fast modulation of visual perception by basal forebrain cholinergic neurons
title Fast modulation of visual perception by basal forebrain cholinergic neurons
title_full Fast modulation of visual perception by basal forebrain cholinergic neurons
title_fullStr Fast modulation of visual perception by basal forebrain cholinergic neurons
title_full_unstemmed Fast modulation of visual perception by basal forebrain cholinergic neurons
title_short Fast modulation of visual perception by basal forebrain cholinergic neurons
title_sort fast modulation of visual perception by basal forebrain cholinergic neurons
url http://hdl.handle.net/1721.1/102414
https://orcid.org/0000-0002-8021-277X
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