Recovery of functional response in the nucleus of the solitary tract after peripheral gustatory nerve crush and regeneration.

Abstract

Single-unit recording and transganglionic tracing techniques were used to assess the properties of, and inputs to, neurons within the rostral nucleus of the solitary tract (NST) after peripheral gustatory nerve injury and regeneration in adult hamsters (Mesocricetus auratus). Tastant-evoked responses were recorded from 43 neurons in animals in which the ipsilateral chorda tympani (CT) nerve was crushed 8 wk earlier (experimental animals) and from 46 neurons in unlesioned control animals. The 89 neurons were separated into three functional clusters named according to the best stimulus for neurons in the cluster: S, sucrose; N, sodium acetate; and H, HCl or KCl. Stimulus-evoked spike rates across all stimuli were 35.4 +/- 4.4% lower in the experimental hamsters. The largest difference in evoked spike rates occurred for neurons in the H cluster, in which the response to KCl also was delayed relative to normal responses. The response of S-cluster units to sucrose and saccharin was also lower in the experimental animals. The mean response rate and the time course of response of neurons in the N cluster did not differ between the two groups. For each cluster, the spontaneous rates and mean response profiles across eight stimuli were very similar in the experimental and control animals, and the breadth of tuning hardly differed. In both groups, Na+ responses in the N cluster were amiloride sensitive, and responses to the water rinse after stimulation with HCl were common in the S cluster. At 8-20 wk after nerve crush, biotinylated dextran tracing of the CT nerve revealed that the regenerated CT fibers did not sprout outside the normal terminal zone in the NST, but the density of the central terminal fibers was 36.9 +/- 6.35% lower than normal. After CT nerve crush and regeneration, the overall reduction in taste-evoked spike rates in NST neurons is likely a consequence of this change in terminal fibers; this in turn likely results from the known reduction in CT fibers regenerating past the crush site. In the face of this reduction, the normal taste-evoked spike rate in N-cluster neurons requires explanation. The observed recovery of normal specificity could be mediated by a restoration of specific connections by primary afferent fibers peripherally and centrally or by central compensatory mechanisms.