TRPV1-Lineage Somatosensory Fibers Communicate with Taste Neurons in the Mouse Parabrachial Nucleus

Abstract

Trigeminal neurons convey somatosensory information from craniofacial tissues. In mouse brain, ascending projections from medullary trigeminal neurons arrive at taste neurons in the parabrachial (PB) nucleus, suggesting that taste neurons participate in somatosensory processing. However, the cell types that support this convergence were undefined. Using Cre-directed optogenetics and in vivo neurophysiology in anesthetized mice of both sexes, here we studied whether transient receptor potential vanilloid 1 (TRPV1)-lineage nociceptive and thermosensory fibers are primary neurons that drive trigeminal circuits reaching PB taste cells. We monitored spiking activity in individual PB neurons during photoexcitation of the terminals of TRPV1-lineage fibers arriving at the dorsal trigeminal nucleus caudalis, which relays orofacial somatosensory messages to the PB area. We also recorded PB neural responses to oral delivery of taste, chemesthetic, and thermal stimuli. We found that optical excitation of TRPV1-lineage fibers elicited responses in traditionally defined taste neurons in lateral PB nuclei. The tuning of neurons across diverse tastes associated with their sensitivity to TRPV1-lineage fiber stimulation, which only sparingly engaged neurons oriented to preferred tastes like sucrose. Moreover, neurons responsive to photostimulation of TRPV1-lineage afferents showed strong responses to temperature including noxious heat, which predominantly excited PB bitter taste cells. Multivariate and machine learning analyses revealed the PB confluence of TRPV1-lineage signals with taste captured sensory valence information shared across aversive gustatory, nociceptive, and thermal stimuli. Our results reveal that TRPV1-lineage fibers, which have defined roles in thermosensation and pain, communicate with PB taste neurons. This multisensory convergence supports dependencies between gustatory and somatosensory hedonic representations in the brain.

SIGNIFICANCE STATEMENT The parabrachial (PB) nucleus participates in autonomic and integrative neural processing for diverse sensory modalities. We recently found in mice that trigeminal neurons supplying craniofacial somatosensation project to PB neurons sensitive to tastes. Here, we show that trigeminal projections to PB gustatory cells are driven by a genetic class of thermosensory and nociceptive fiber. Input from these fibers was associated with PB neural sensitivity to aversive oral temperatures and tastes and supported a multimodal neural representation of sensory valence across gustatory, nociceptive, and thermal stimuli. These results reveal gustation and somatosensation to be only components of a larger PB code that captures sensory value. Defining this circuit has implications for understanding the neural representation of taste, temperature, and also pain-related phenomena.