Primary afferent plasticity following partial denervation of the trigeminal brainstem nuclear complex in the postnatal rat

Abstract

Although interaxonal competition is believed to be an essential component of the normal development of numerous mammalian neuronal populations, there is considerable debate regarding the role of competition in the development and maintenance of the somatic sensory system. The results of recent investigations suggest that trigeminal primary afferents may compete for target territory in the brainstem, but it is unclear whether these interactions continue after birth. The present study explored this important issue by examining the response of individual trigeminal primary afferent neurons to partial denervation of the trigeminal brainstem nuclear complex at early postnatal ages. We utilized intracellular recording and HRP injection techniques to label primary afferent central terminal arbors in rats that sustained electrocautery of mystacial vibrissae in rows A, C, and E on the day of birth. A total of 42 low-threshold trigeminal primary afferent neurons were labeled in subnucleus interpolaris. Twenty-eight of these afferents supplied undamaged B or D row vibrissae while 14 supplied lesioned vibrissae. Qualitative and quantitative analyses revealed that the arbors associated with undamaged afferents were enlarged (mean arbor area of 13512 +/- 790.67 microns 2 vs normal area of 6130 +/- 214 microns 2) and were oriented toward the adjacent (partially denervated) territory. There was no significant change in the size of the lesioned afferent arbor area. The perimeter of the lesioned afferent arbors was increased, however, suggesting that the arbor shape had changed. This was confirmed with a form factor calculation that indicated that the circularity of the arbors associated with lesioned vibrissae was significantly reduced. Thus, while the arbors of undamaged afferents were enlarged and oriented in the direction of the partially denervated territory, the lesioned afferent arbors were not enlarged but assumed a flattened/elongate morphology within their appropriate row. The lesion-induced increase in the size of the undamaged afferent arbors was not associated with an increase in the number of bouton-like fiber swellings. The density of boutons was only 25% the value seen in normal animals. Thus, while the area supplied by the undamaged afferent arbors increased, there was no evidence that the absolute amount of terminal arbor was similarly increased (as would be the case if sprouting had occurred; see Renehan et al., 1989). We would therefore conclude that the undamaged afferents had undergone arbor expansion, but not sprouting. These data are consistent with prior suggestions that trigeminal primary afferents utilize some form of competitive interaction(s) to establish their final form and disposition. This competition would appear to continue into early postnatal periods.(ABSTRACT TRUNCATED AT 400 WORDS)