The cellular coding of temperature in the mammalian cortex

Abstract

Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm (Blix, 1882; Filingeri, 2016; Vriens et al., 2014). Unlike other modalities, however, the cortical encoding of temperature remains mysterious, with very few cortical neurons reported that respond to non-painful temperature and the presence of a thermal cortex is debated (Bokiniec et al., 2018; Craig et al., 2000; Hellon et al., 1973; Milenkovic et al., 2014; Tsuboi et al., 1993). Using widefield and two-photon calcium imaging in the mouse forepaw system, here we identify cortical neurons that respond to cooling and/or warming with distinct spatial and temporal response properties. Surprisingly, we observed a representation of cool, but not warm, in the primary somatosensory cortex, but cool and warm in the posterior insular cortex (pIC). The representation of thermal information in pIC is robust, somatotopicallyarranged and reversible manipulations show a profound impact on thermal perception. Intriguingly, despite being positioned along the same one-dimensional sensory axis, the encoding of cool and warm is distinct, both in highly- and broadly- tuned neurons. Together, our results show that pIC contains the primary cortical representation of skin temperature and may help explain how the thermal system generates sensations of cool and warm.