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Context-dependent and dynamic functional influence of corticothalamic pathways to first- and higher-order visual thalamus

View ORCID ProfileMegan A. Kirchgessner, View ORCID ProfileAlexis D. Franklin, View ORCID ProfileEdward M. Callaway
doi: https://doi.org/10.1101/738203
Megan A. Kirchgessner
aSystems Neurobiology Laboratories, Salk Institute for Biological Studies, La Jolla, CA 92037, USA
bNeurosciences Graduate Program, University of California San Diego, La Jolla, CA 92093, USA
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  • ORCID record for Megan A. Kirchgessner
Alexis D. Franklin
aSystems Neurobiology Laboratories, Salk Institute for Biological Studies, La Jolla, CA 92037, USA
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Edward M. Callaway
aSystems Neurobiology Laboratories, Salk Institute for Biological Studies, La Jolla, CA 92037, USA
bNeurosciences Graduate Program, University of California San Diego, La Jolla, CA 92093, USA
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  • For correspondence: callaway@salk.edu
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Abstract

Layer 6 (L6) is the sole purveyor of corticothalamic (CT) feedback to first-order thalamus and also sends projections to higher-order thalamus, yet how it engages the full corticothalamic circuit to contribute to sensory processing in an awake animal remains unknown. We sought to elucidate the functional impact of L6CT projections from primary visual cortex to visual thalamic nuclei dLGN (first-order) and pulvinar (higher-order) using optogenetics and extracellular electrophysiology in awake mice. While sustained L6CT photostimulation suppresses activity in both visual thalamic nuclei in vivo, moderate-frequency (10Hz) stimulation powerfully facilitates thalamic spiking. We show that each stimulation paradigm differentially influences the balance between monosynaptic excitatory and disynaptic inhibitory corticothalamic pathways to dLGN and pulvinar as well as the prevalence of burst versus tonic firing. Altogether, our results support a model in which L6CTs modulate first- and higher-order thalamus through parallel excitatory and inhibitory pathways that are highly dynamic and context-dependent.

Significance Layer 6 corticothalamic (L6CT) projections play important modulatory roles in thalamic processing, yet how this modulation is executed is unclear. While some studies suggest fundamentally inhibitory influence of L6CTs over first-order thalamus, potential complex, frequency-dependent effects have not been investigated in vivo. Moreover, how L6CTs affect higher-order nuclei in vivo has not been explored. This study utilizes various optogenetic manipulations of L6CTs with single-unit recordings from multiple thalamic nuclei in awake mice to address these questions. Our results illustrate similar effects of L6CTs on first- and higher-order visual thalamic nuclei, yet very different effects within-nucleus depending on how L6CTs are engaged. These findings suggest that L6CT modulation is not simply inhibitory by nature, but instead is dynamic and context-dependent.

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  • Additional analyses; revised Discussion

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 06, 2020.
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Context-dependent and dynamic functional influence of corticothalamic pathways to first- and higher-order visual thalamus
Megan A. Kirchgessner, Alexis D. Franklin, Edward M. Callaway
bioRxiv 738203; doi: https://doi.org/10.1101/738203
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Context-dependent and dynamic functional influence of corticothalamic pathways to first- and higher-order visual thalamus
Megan A. Kirchgessner, Alexis D. Franklin, Edward M. Callaway
bioRxiv 738203; doi: https://doi.org/10.1101/738203

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