Thalamic bursting and the role of timing and synchrony in thalamocortical signaling in the awake mouse

The thalamus controls transmission of sensory signals from periphery to cortex, ultimately shaping perception. Despite this significant role, dynamic thalamic gating and the consequences for downstream cortical sensory representations have not been well studied in the awake brain. We optogenetically...

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Published inNeuron (Cambridge, Mass.) Vol. 110; no. 17; pp. 2836 - 2853.e8
Main Authors Borden, Peter Y., Wright, Nathaniel C., Morrissette, Arthur E., Jaeger, Dieter, Haider, Bilal, Stanley, Garrett B.
Format Journal Article
LanguageEnglish
Published Elsevier Inc 07.09.2022
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Summary:The thalamus controls transmission of sensory signals from periphery to cortex, ultimately shaping perception. Despite this significant role, dynamic thalamic gating and the consequences for downstream cortical sensory representations have not been well studied in the awake brain. We optogenetically modulated the ventro-posterior-medial thalamus in the vibrissa pathway of the awake mouse and measured spiking activity in the thalamus and activity in primary somatosensory cortex (S1) using extracellular electrophysiology and genetically encoded voltage imaging. Thalamic hyperpolarization significantly enhanced thalamic sensory-evoked bursting; however, surprisingly, the S1 cortical response was not amplified, but instead, timing precision was significantly increased, spatial activation more focused, and there was an increased synchronization of cortical inhibitory neurons. A thalamocortical network model implicates the modulation of precise timing of feedforward thalamic population spiking, presenting a highly sensitive, timing-based gating of sensory signaling to the cortex. •Optogenetic thalamic hyperpolarization enhances thalamic sensory-evoked bursting•S1 cortical responses are not amplified•Thalamic bursting increases S1 timing precision and synchrony•A highly sensitive, timing-based gating of sensory signaling to cortex It has long been proposed that the thalamus serves as a dynamic gate for control of sensory signaling to cortex through switching between tonic and burst firing modes. Using optogenetic manipulation in the awake mouse, Borden et al. demonstrate a thalamic burst-driven, timing-based gating of sensory signaling to the cortex.
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Author Contributions: PYB, NCW, and GBS conceptualized the study. PYB and NCW conducted the investigation, including performing the experiments, curating the data, and conducting the formal analysis. PYB, NCW, and GBS wrote the original draft. DJ, BH, and AEM contributed to writing of the original draft and review/editing.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2022.06.008