Mouse parabrachial neurons signal a relationship between bitter taste and nociceptive stimuli

Abstract

Taste and somatosensation both partly mediate protective behaviors. Bitter taste guides avoidance of ingestion of toxins while pain sensations, such as noxious heat, signal adverse conditions to ward off harm. Although brain pathways for taste and somatosensation are typically studied independently, prior data suggest they intersect, potentially reflecting their common protective role. To investigate this, we applied electrophysiologic and optogenetic techniques in anesthetized mice of both sexes to evaluate relationships between oral somatosensory and taste activity in the parabrachial nucleus (PbN), implicated for roles in gustation and pain. Spikes were recorded from taste-active PbN neurons tested with oral delivery of thermal and chemesthetic stimuli, including agonists of nocisensitive transient receptor potential (TRP) ion channels on somatosensory fibers. Gustatory neurons were also tested to follow electrical pulse stimulation of an oral somatosensory region of the spinal trigeminal subnucleus caudalis (Vc), which projects to the PbN. Neurons composed classic taste groups, including sodium, electrolyte, appetitive, or bitter oriented cells. Across groups, most neurons spiked to Vc pulse stimulation, implying trigeminal projections reach PbN gustatory neurons. Among such cells, agonists of nocisensitive TRP channels, including mustard oil, capsaicin, and noxious heat, were discovered to predominantly activate PbN bitter taste neurons tuned to the bitters quinine and cycloheximide. Such neurons populated the lateral PbN. Further, PbN bitter taste neurons showed suppressed oral nociceptive activity during optogenetic-assisted inhibition of the Vc, implying convergent trigeminal input contributed to such activity. Our results imply a novel role for PbN gustatory cells in crossmodal signaling related to protection.