Thalamic state controls timing and synchronization of primary somatosensory cortical representations in the awake mouse

Abstract

SummaryThe 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 at the level of primary somatosensory cortex (S1) using extracellular electrophysiology and genetically encoded voltage imaging. Thalamic hyperpolarization significantly amplified thalamic sensory-evoked spiking through enhanced bursting, yet 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 precise timing of feedforward thalamic spiking, and timing-sensitive engagement of synaptic depression, presenting a highly sensitive, state-dependent timing-based gating of sensory signaling to cortex.