The cellular representation of temperature across the somatosensory thalamus.

Although distinct thalamic nuclei encode sensory information for almost all sensory modalities, the existence of a thalamic representation of temperature with a role in thermal perception remains unclear. To address this, we performed high-density electrophysiological recordings across the entire forelimb somatosensory thalamus in awake mice, and identified an anterior and a posterior representation of temperature that spans three thalamic nuclei. We found that these parallel representations show fundamental differences in the cellular encoding of temperature which reflects their cortical output targets. While the anterior representation encodes cool only and the posterior both cool and warm; in both representations cool was more densely represented and showed shorter latency, more transient responses as compared to warm. Moreover, thalamic inactivation showed a major role in thermal perception. Our comprehensive dataset identifies the thalamus as a key structure in thermal processing and highlights a novel posterior pathway in the thalamic representation of warm and cool.

Thermosensory thalamus: parallel processing across model organisms.

The thalamus acts as an interface between the periphery and the cortex, with nearly every sensory modality processing information in the thalamocortical circuit. Despite well-established thalamic nuclei for visual, auditory, and tactile modalities, the key thalamic nuclei responsible for innocuous thermosensation remains under debate. Thermosensory information is first transduced by thermoreceptors located in the skin and then processed in the spinal cord. Temperature information is then transmitted to the brain through multiple spinal projection pathways including the spinothalamic tract and the spinoparabrachial tract. While there are fundamental studies of thermal transduction via thermosensitive channels in primary sensory afferents, thermal representation in the spinal projection neurons, and encoding of temperature in the primary cortical targets, comparatively little is known about the intermediate stage of processing in the thalamus. Multiple thalamic nuclei have been implicated in thermal encoding, each with a corresponding cortical target, but without a consensus on the role of each pathway. Here, we review a combination of anatomy, physiology, and behavioral studies across multiple animal models to characterize the thalamic representation of temperature in two proposed thermosensory information streams.

Brain-wide connectivity map of mouse thermosensory cortices.

In the thermal system, skin cooling is represented in the primary somatosensory cortex (S1) and the posterior insular cortex (pIC). Whether S1 and pIC are nodes in anatomically separate or overlapping thermal sensorimotor pathways is unclear, as the brain-wide connectivity of the thermal system has not been mapped. We address this using functionally targeted, dual injections of anterograde viruses or retrograde tracers into the forelimb representation of S1 (fS1) and pIC (fpIC). Our data show that inputs to fS1 and fpIC originate from separate neuronal populations, supporting the existence of parallel input pathways. Outputs from fS1 and fpIC are more widespread than their inputs, sharing a number of cortical and subcortical targets. While, axonal projections were separable, they were more overlapping than the clusters of input cells. In both fS1 and fpIC circuits, there was a high degree of reciprocal connectivity with thalamic and cortical regions, but unidirectional output to the midbrain and hindbrain. Notably, fpIC showed connectivity with regions associated with thermal processing. Together, these data indicate that cutaneous thermal information is routed to the cortex via parallel circuits and is forwarded to overlapping downstream regions for the binding of somatosensory percepts and integration with ongoing behavior.