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      Thalamic state control of cortical paired-pulse dynamics

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          Abstract

          For the first time, we have been able to utilize optogenetic modulation of thalamic firing modes combined with optical imaging of cortex in the rat vibrissa system to directly test the role of thalamic state in shaping cortical response properties.

          Abstract

          Sensory stimulation drives complex interactions across neural circuits as information is encoded and then transmitted from one brain region to the next. In the highly interconnected thalamocortical circuit, these complex interactions elicit repeatable neural dynamics in response to temporal patterns of stimuli that provide insight into the circuit properties that generated them. Here, using a combination of in vivo voltage-sensitive dye (VSD) imaging of cortex, single-unit recording in thalamus, and optogenetics to manipulate thalamic state in the rodent vibrissa pathway, we probed the thalamocortical circuit with simple temporal patterns of stimuli delivered either to the whiskers on the face (sensory stimulation) or to the thalamus directly via electrical or optogenetic inputs (artificial stimulation). VSD imaging of cortex in response to whisker stimulation revealed classical suppressive dynamics, while artificial stimulation of thalamus produced an additional facilitation dynamic in cortex not observed with sensory stimulation. Thalamic neurons showed enhanced bursting activity in response to artificial stimulation, suggesting that bursting dynamics may underlie the facilitation mechanism we observed in cortex. To test this experimentally, we directly depolarized the thalamus, using optogenetic modulation of the firing activity to shift from a burst to a tonic mode. In the optogenetically depolarized thalamic state, the cortical facilitation dynamic was completely abolished. Together, the results obtained here from simple probes suggest that thalamic state, and ultimately thalamic bursting, may play a key role in shaping more complex stimulus-evoked dynamics in the thalamocortical pathway.

          NEW & NOTEWORTHY For the first time, we have been able to utilize optogenetic modulation of thalamic firing modes combined with optical imaging of cortex in the rat vibrissa system to directly test the role of thalamic state in shaping cortical response properties.

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          Author and article information

          Journal
          J Neurophysiol
          J. Neurophysiol
          jn
          jn
          JN
          Journal of Neurophysiology
          American Physiological Society (Bethesda, MD )
          0022-3077
          1522-1598
          19 October 2016
          1 January 2017
          1 January 2018
          : 117
          : 1
          : 163-177
          Affiliations
          Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Georgia
          Author notes
          Address for reprint requests and other correspondence: G. B. Stanley, Coulter Dept. of Biomedical Engineering, Georgia Inst. of Technology and Emory Univ., 313 Ferst Dr., Atlanta, GA 30332 (e-mail: garrett.stanley@ 123456bme.gatech.edu ).
          Author information
          http://orcid.org/0000-0003-2039-7706
          Article
          PMC5209547 PMC5209547 5209547 JN-00415-2016
          10.1152/jn.00415.2016
          5209547
          27760816
          41e510ec-0f8d-44b9-a579-8251a7e9edd9
          Copyright © 2017 the American Physiological Society
          History
          : 26 May 2016
          : 15 October 2016
          Funding
          Funded by: http://doi.org/10.13039/100000065 HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
          Award ID: R01NS48285
          Award ID: R01NS085447
          Award ID: F31NS089412
          Funded by: http://doi.org/10.13039/100000084 NSF | Directorate for Engineering (ENG)
          Funded by: http://doi.org/10.13039/100000026 HHS | NIH | National Institute on Drug Abuse (NIDA)
          Award ID: T90DA032466
          Categories
          Research Article
          Neural Circuits

          vibrissa,thalamic state,optogenetics,dynamics,cortical activation

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