Sensory Afferents Use Different Coding Strategies for Heat and Cold

Abstract

Primary afferents transduce environmental stimuli into electrical activity that is transmitted centrally to be decoded into corresponding sensations. However, it remains unknown how afferent populations encode different somatosensory inputs. To address this, we performed two-photon Ca imaging from thousands of dorsal root ganglion (DRG) neurons in anesthetized mice while applying mechanical and thermal stimuli to hind paws. We found that approximately half of all neurons are polymodal and that heat and cold are encoded very differently. As temperature increases, more heating-sensitive neurons are activated, and most individual neurons respond more strongly, consistent with graded coding at population and single-neuron levels, respectively. In contrast, most cooling-sensitive neurons respond in an ungraded fashion, inconsistent with graded coding and suggesting combinatorial coding, based on which neurons are co-activated. Although individual neurons may respond to multiple stimuli, our results show that different stimuli activate distinct combinations of diversely tuned neurons, enabling rich population-level coding.

Oral thermosensing by murine trigeminal neurons: modulation by capsaicin, menthol, and mustard oil

“…Namely, capsaicin and AITC sensitize nociceptors and warm-responding neurons and menthol attenuates responses mainly in cool thermoreceptors. Our data are also consistent with the notion that neural coding of oral thermosensations can be explained by population coding, as postulated for cutaneous thermosensitivity (Ma, 2012;Wang et al 2018). Abstracts of these findings have been published (Leijon et al 2016(Leijon et al , 2017(Leijon et al , 2018.…”

“…Population coding of oral thermosensing might explain the conflicting data regarding orosensitivity to cool and warm in human subjects; if orosensory thermal input is sensed by the combined population of afferent thermosensory trigeminal neurons, thermal sensations would be expected to be highly dependent on the subset of neurons activated the sizes and locations of the subsets of thermosensitive afferent neurons likely varied from laboratory to laboratory. Extensive data from imaging thermal responses in dorsal root ganglion neurons that innervate the hindpaws in mice came to the same conclusion, namely that cutaneous temperature is signalled by population coding (Wang et al 2018). These conclusions support earlier interpretations of thermoreception coding (Ma, 2012).…”

“…1E and F). Similar responses have been recorded from cutaneous cool thermoreceptors (Wang et al 2018). Cooling-sensitive responses were distributed among Types I and II cool neurons, with a greater proportion found in Type I (rapidly adapting) cool neurons (88 and 34 neurons, respectively).…”

“…As in B, grey lines show data for 6 representative neurons and dark line is best fit sigmoidal curve for all neurons. Note that some LT cool respond best (are 'tuned') to a specific temperature between 6 and 32°C, a phenomenon previously seen in recordings from cutaneous and trigeminal cool thermosensors (Madrid et al 2006;Bautista et al 2007;Wang et al 2018). J Physiol 597.7 Thermosensitive neurons had characteristic responses to the chemesthetic compounds.…”

“…2C). Neurons similarly tuned to specific temperatures were also reported for cool thermoreceptors innervating the mouse hindpaw (Wang et al 2018). Figure 3A summarizes the distribution of the different types of oral thermosensitive trigeminal neurons.…”