State-Dependent Architecture of Thalamic Reticular Subnetworks

Behavioral state is known to influence interactions between thalamus and cortex, which are important for sensation, action, and cognition. The thalamic reticular nucleus (TRN) is hypothesized to regulate thalamo-cortical interactions, but the underlying functional architecture of this process and it...

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Main Authors: Halassa, Michael M., Chen, Zhe, Wimmer, Ralf D., Brunetti, Philip M., Zhao, Shengli, Zikopoulos, Basilis, Wang, Fan, Brown, Emery N., Wilson, Matthew A., Halassa, Michael M., Wimmer, Ralf D., Brunetti, Philip M., Brown, Emery N., Wilson, Matthew A.
Other Authors: Harvard University--MIT Division of Health Sciences and Technology
Format: Article
Language:en_US
Published: Elsevier 2016
Online Access:http://hdl.handle.net/1721.1/102340
https://orcid.org/0000-0003-2668-7819
https://orcid.org/0000-0001-7149-3584
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author Halassa, Michael M.
Chen, Zhe
Wimmer, Ralf D.
Brunetti, Philip M.
Zhao, Shengli
Zikopoulos, Basilis
Wang, Fan
Brown, Emery N.
Wilson, Matthew A.
Halassa, Michael M.
Wimmer, Ralf D.
Brunetti, Philip M.
Brown, Emery N.
Wilson, Matthew A.
author2 Harvard University--MIT Division of Health Sciences and Technology
author_facet Harvard University--MIT Division of Health Sciences and Technology
Halassa, Michael M.
Chen, Zhe
Wimmer, Ralf D.
Brunetti, Philip M.
Zhao, Shengli
Zikopoulos, Basilis
Wang, Fan
Brown, Emery N.
Wilson, Matthew A.
Halassa, Michael M.
Wimmer, Ralf D.
Brunetti, Philip M.
Brown, Emery N.
Wilson, Matthew A.
author_sort Halassa, Michael M.
collection MIT
description Behavioral state is known to influence interactions between thalamus and cortex, which are important for sensation, action, and cognition. The thalamic reticular nucleus (TRN) is hypothesized to regulate thalamo-cortical interactions, but the underlying functional architecture of this process and its state dependence are unknown. By combining the first TRN ensemble recording with psychophysics and connectivity-based optogenetic tagging, we found reticular circuits to be composed of distinct subnetworks. While activity of limbic-projecting TRN neurons positively correlates with arousal, sensory-projecting neurons participate in spindles and show elevated synchrony by slow waves during sleep. Sensory-projecting neurons are suppressed by attentional states, demonstrating that their gating of thalamo-cortical interactions is matched to behavioral state. Bidirectional manipulation of attentional performance was achieved through subnetwork-specific optogenetic stimulation. Together, our findings provide evidence for differential inhibition of thalamic nuclei across brain states, where the TRN separately controls external sensory and internal limbic processing facilitating normal cognitive function.
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spelling mit-1721.1/1023402022-09-30T12:03:24Z State-Dependent Architecture of Thalamic Reticular Subnetworks Halassa, Michael M. Chen, Zhe Wimmer, Ralf D. Brunetti, Philip M. Zhao, Shengli Zikopoulos, Basilis Wang, Fan Brown, Emery N. Wilson, Matthew A. Halassa, Michael M. Wimmer, Ralf D. Brunetti, Philip M. Brown, Emery N. Wilson, Matthew A. Harvard University--MIT Division of Health Sciences and Technology Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Picower Institute for Learning and Memory Halassa, Michael M. Wimmer, Ralf D. Brunetti, Philip M. Brown, Emery N. Wilson, Matthew A. Behavioral state is known to influence interactions between thalamus and cortex, which are important for sensation, action, and cognition. The thalamic reticular nucleus (TRN) is hypothesized to regulate thalamo-cortical interactions, but the underlying functional architecture of this process and its state dependence are unknown. By combining the first TRN ensemble recording with psychophysics and connectivity-based optogenetic tagging, we found reticular circuits to be composed of distinct subnetworks. While activity of limbic-projecting TRN neurons positively correlates with arousal, sensory-projecting neurons participate in spindles and show elevated synchrony by slow waves during sleep. Sensory-projecting neurons are suppressed by attentional states, demonstrating that their gating of thalamo-cortical interactions is matched to behavioral state. Bidirectional manipulation of attentional performance was achieved through subnetwork-specific optogenetic stimulation. Together, our findings provide evidence for differential inhibition of thalamic nuclei across brain states, where the TRN separately controls external sensory and internal limbic processing facilitating normal cognitive function. National Institute of Neurological Disorders and Stroke (U.S.) (NIH Pathway to Independence Career Award K99 NS 078115) Brain & Behavior Research Foundation (Young Investigator Award) National Institutes of Health (U.S.) ( Transformative R01 Award TR01-GM10498) National Institutes of Health (U.S.) (Grant R01-MH061976) 2016-04-29T20:24:28Z 2016-04-29T20:24:28Z 2014-08 2014-05 Article http://purl.org/eprint/type/JournalArticle 00928674 http://hdl.handle.net/1721.1/102340 Halassa, Michael M., Zhe Chen, Ralf D. Wimmer, Philip M. Brunetti, Shengli Zhao, Basilis Zikopoulos, Fan Wang, Emery N. Brown, and Matthew A. Wilson. “State-Dependent Architecture of Thalamic Reticular Subnetworks.” Cell 158, no. 4 (August 2014): 808–821. https://orcid.org/0000-0003-2668-7819 https://orcid.org/0000-0001-7149-3584 en_US http://dx.doi.org/10.1016/j.cell.2014.06.025 Cell Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier PMC
spellingShingle Halassa, Michael M.
Chen, Zhe
Wimmer, Ralf D.
Brunetti, Philip M.
Zhao, Shengli
Zikopoulos, Basilis
Wang, Fan
Brown, Emery N.
Wilson, Matthew A.
Halassa, Michael M.
Wimmer, Ralf D.
Brunetti, Philip M.
Brown, Emery N.
Wilson, Matthew A.
State-Dependent Architecture of Thalamic Reticular Subnetworks
title State-Dependent Architecture of Thalamic Reticular Subnetworks
title_full State-Dependent Architecture of Thalamic Reticular Subnetworks
title_fullStr State-Dependent Architecture of Thalamic Reticular Subnetworks
title_full_unstemmed State-Dependent Architecture of Thalamic Reticular Subnetworks
title_short State-Dependent Architecture of Thalamic Reticular Subnetworks
title_sort state dependent architecture of thalamic reticular subnetworks
url http://hdl.handle.net/1721.1/102340
https://orcid.org/0000-0003-2668-7819
https://orcid.org/0000-0001-7149-3584
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