EXPRESS: Stimulation of spinal afferents from skin activates parabrachial neurons that respond to taste

The parabrachial (PB) nucleus participates in neural coding for diverse sensory modalities, including nociception and taste. Recent neurophysiological studies identified a subpopulation of PB neurons that responds to both gustatory and oral nociceptive (trigeminal) stimuli. These taste-integrative neurons populate PB subnuclei that receive somatosensory input from bodily skin supplied by spinal afferents. Yet whether spinal sensory input can excite these cells was unexplored. Here, we applied electrophysiological and optogenetic techniques in anesthetized TRPV1;Ai32 mice, which support transdermal photoexcitation of cutaneous TRPV1-lineage thermo-nociceptive fibers, to study if spinal sensory stimulation could engage taste-active PB cells. Action potentials were monitored in isolated PB neurons during oral application of diverse taste and chemesthetic stimuli, oral thermal stimulation using temperature-controlled water, and pinch of the hindpaw and tail. In some cases, photostimulation was applied to pinch-sensitive receptive fields to optogenetically excite bodily TRPV1-lineage fibers. Analysis of 94 PB neurons identified 35 cells (37.2%) that responded to more than one stimulus modality, including 10 taste-excited neurons that also fired impulses to noxious oral chemesthetic (trigeminal) stimuli, oral thermal input, and hindpaw/tail pinch. Such neurons could also respond to photoexcitation of TRPV1-lineage afferents innervating body extremities and frequently displayed bitter-oriented (aversive) taste response profiles. These data suggest that spinal afferent input, including pain-related neural messages from skin, converges onto taste-active PB neurons. These neurons would be misclassified as unimodal "taste" cells under traditional methods but display multisensory response repertoires that agree with involvement of PB circuits in sensory-affective processing.