Determination of thermosensory pathways required for behavioural thermoregulation

Abstract

Thermoregulatory behavior, represented by cold‐ and warm‐seeking behaviors in hot and cold environments, respectively, is utilized by animals to choose an optimal thermal environment. This voluntary behavior helps involuntary autonomous thermoregulatory mechanisms efficiently maintain body core temperature. Although many thermoregulatory behaviors are dependent on environmental temperature information transmitted from skin thermoreceptors to the brain, the afferent mechanism of the thermosensory transmission for behavioral thermoregulation has been unknown. In this study, we first examined the involvement of the well‐known spinothalamocortical thermosensory pathway in behavioral thermoregulation. The rat spinothalamocortical pathway was ablated by bilateral lesions of the ventral posteromedial and ventral posterolateral thalamic nuclei (VPM/VPL), a thalamic area receiving most thermal somatosensory signals from the spinal cord. The functional ablation of this pathway was confirmed with elimination of skin temperature‐dependent electroencephalographic responses recorded from the primary somatosensory cortex. To measure behavioral thermoregulation, we performed a two‐floor thermal plate preference test, in which control rats preferred a 28°C plate to a 15°C (cold) or 38°C (hot) plate, displaying cold‐ and heat‐avoidance thermoregulatory behaviors. Of note, the lesions of the VPM/VPL did not affect the thermoregulatory behaviors, indicating that the spinothalamocortical pathway is not involved in behavioral thermoregulation. We next investigated whether the lateral parabrachial nucleus (LPB), which mediates thermosensory signaling for autonomous thermoregulation, plays a role in behavioral thermoregulation. Inhibition of neurons in the LPB with bilateral nanoinjections of muscimol eliminated the cold‐ and heat‐avoidance thermoregulatory behaviors. These results indicate that an LPB‐mediated afferent pathway, but not the spinothalamocortical pathway, transmits the cutaneous thermosensory neural signals required for behavioral thermoregulation. This finding may contribute to future understanding of the central circuit mechanisms for the generation of thermal comfort and discomfort underlying thermoregulatory behavior.Support or Funding InformationFunding from Nagoya University School of Medicine (TY); KAKENHI, MEXT of Japan 16H05128 & 15H05932 (KN)