Thalamic state influences timing precision in the thalamocortical circuit
AbstractSensory signals from the outside world are transduced at the periphery, passing through thalamus before reaching cortex, ultimately giving rise to the sensory representations that enable us to perceive the world. The thalamocortical circuit is particularly sensitive to the temporal precision of thalamic spiking due to highly convergent synaptic connectivity. Thalamic neurons can exhibit burst and tonic modes of firing that strongly influence timing within the thalamus. The impact of these changes in thalamic state on sensory encoding in the cortex, however, remains unclear. Here, we investigated the role of thalamic state on timing in the thalamocortical circuit of the vibrissa pathway in the anesthetized rat. We optogenetically hyperpolarized thalamus while recording single unit activity in both thalamus and cortex. Tonic spike triggered analysis revealed temporally precise thalamic spiking that was locked to white-noise sensory stimuli, while thalamic burst spiking was associated with a loss in stimulus-locked temporal precision. These thalamic state dependent changes propagated to cortex such that the cortical timing precision was diminished during the hyperpolarized (burst biased) thalamic state. While still sensory driven, the cortical neurons became significantly less precisely locked to the white-noise stimulus. The results here suggest that tonic thalamic spiking is more temporally precise than burst firing, which leads to distinct differences in sensory information representation at the level of both the thalamus and the cortex, as assessed using spike triggered analysis. This difference in spike timing precision enables a dynamic encoding scheme for sensory information as a function of thalamic state.New and NoteworthyThe majority of sensory signals are transmitted through the thalamus. There is growing evidence of complex thalamic gating through coordinated firing modes that have a strong impact on cortical sensory representations. Optogenetic hyperpolarization of thalamus pushed it into burst firing that disrupted precise time-locked sensory signaling, with a direct impact on the downstream cortical encoding, setting the stage for a timing-based thalamic gate of sensory signaling.
