Abstract
Sensory 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 weak white-noise sensory stimuli, whereas 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. Although still sensory driven, the cortical neurons became significantly less precisely locked to the weak white-noise stimulus. The results here suggests a state-dependent differential regulation of spike timing precision in the thalamus that could gate what signals are ultimately propagated to cortex.NEW & NOTEWORTHY The 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.
Highlights
Sensory thalamus plays a critical role in gating information flow from our sensors in the periphery to sensory cortex, shaping how we perceive the world
STASNR for all bSTA computed from all burst spikes while red circles indicate the STASNR for bSTA computed from only the first spike in the burst (p = 1e-6)
We found that the tonic spikes were well tuned to the spike triggered average (STA), as evidenced by the steep slope of the non-linearity while the burst spikes were not well tuned to the STA, as evidenced by the relatively flat non-linearity (Figure 2D)
Summary
Sensory thalamus plays a critical role in gating information flow from our sensors in the periphery to sensory cortex, shaping how we perceive the world. Arising from different mechanisms, these modulatory inputs have the net effect of altering the baseline membrane polarization level in the thalamus, which we refer to here as “thalamic state”, which plays an important role in determining the encoding properties of the thalamic neurons that serve as primary inputs to sensory cortex. Modulation of the baseline membrane potential in thalamic neurons enables distinct tonic and burst firing modes due to the hyperpolarization (Suzuki and Rogawski, 1989). In addition to their roles in thalamocortical oscillations (Steriade et al, 1993), it has long been posited that these two firing modes could be a mechanism for dynamically controlling information processing (Sherman 2001). It has been proposed that both burst and tonic spikes carry stimulus information (Reinagel et al, 1999), but the relationship between burst and tonic firing in representing temporal stimulus information in tactile encoding remains unclear
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