Altered taste responses in adult NST after neonatal chorda tympani denervation

Anatomic and behavioral changes have been observed in the taste system after peripheral deafferentation, but their physiological consequences remain unknown. Interestingly, a recent behavioral study suggested that peripheral denervation could induce central plasticity. After neonatal chorda tympani (CT) transection, adult rats demonstrated a marked preference for a normally avoided salt, NH(4)Cl. In the present study, taste responses were recorded from the nucleus of the solitary tract (NST) in similarly CT-denervated rats to investigate a physiological basis for this behavioral phenomenon. We hypothesized that alterations in functional connectivity of remaining afferent nerves might underlie the behavioral change. Specifically, if NST neurons formerly activated by sodium-selective CT fibers were instead driven by more broadly tuned glossopharyngeal (GL) afferents, neural coding of salt responses would be altered. Such a change should be accompanied by a shift in orotopic representation and increased NH(4)Cl responses. This hypothesis was not supported. After CT denervation, orotopy was unaltered, NH(4)Cl responsiveness declined, and no other changes occurred that could simply explain the behavioral effects. Indeed, the most pronounced consequence of CT denervation was a 68% reduction in NaCl responses, supporting previous evidence for a critical role of this nerve in coding sodium salts. In addition, we found "reorganizational" changes similar to, albeit smaller than, those observed in other sensory systems after deafferentation. There was a trend for increased responses elicited by stimulation of receptor subpopulations innervated by the GL and greater superficial petrosal nerves. In addition, the spontaneous rate of nasoincisor duct-responsive cells increased significantly. This effect on spontaneous rate is opposite to that produced by CT anesthesia, suggesting that acute versus chronic denervation may affect central taste neurons differently. In conclusion, the taste system at the medullary level seems more resistant to large-scale plasticity than other sensory systems, but nevertheless reacts to lost afferent input. Because the most robust plastic changes have been documented at cortical levels in other sensory pathways, the substrate for the behavioral effect of neonatal CT transection may be located more centrally in the gustatory system.