PRIMARY AFFERENT PLASTICITY FOLLOWING PARTIAL DENERVATION OF THE TRIGEMINAL BRAIN-STEM NUCLEAR-COMPLEX IN THE POSTNATAL RAT

Although interaxonal competition is believed to be an essential compon ent of the normal development of numerous mammalian neuronal populatio ns, there is considerable debate regarding the role of competition in the development and maintenance of the somatic sensory system. The res ults of recent investigations suggest that trigeminal primary afferent s may compete for target territory in the brainstem, but it is unclear whether these interactions continue after birth. The present study ex plored this important issue by examining the response of individual tr igeminal primary afferent neurons to partial denervation of the trigem inal brainstem nuclear complex at early postnatal ages. We utilized in tracellular recording and HRP injection techniques to label primary af ferent central terminal arbors in rats that sustained electrocautery o f 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 u ndamaged B or D row vibrissae while 14 supplied lesioned vibrissae. Qu alitative and quantitative analyses revealed that the arbors associate d with undamaged afferents were enlarged (mean arbor area of 13512 +/- 790.67 mu m(2) vs normal area of 6130 +/- 214 mu m(2)) and were orien ted toward the adjacent (partially denervated) territory. There was no significant change in the size of the lesioned afferent arbor area. T he perimeter of the lesioned afferent arbors was increased, however, s uggesting that the arbor shape had changed. This was confirmed with a form factor calculation that indicated that the circularity of the arb ors associated with lesioned vibrissae was significantly reduced. Thus , while the arbors of undamaged afferents were enlarged and oriented i n the direction of the partially denervated territory, the lesioned af ferent arbors were not enlarged but assumed a flattened/elongate morph ology within their appropriate row. The lesion-induced increase in the size of the undamaged afferent arbors was not associated with an incr ease in the number of bouton-like fiber swellings. The density of bout ons was only 25% the value seen in normal animals. Thus, while the are a supplied by the undamaged afferent arbors increased, there was no ev idence that the absolute amount of terminal arbor was similarly increa sed (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 consiste nt with prior suggestions that trigeminal primary afferents utilize so me form of competitive interaction(s) to establish their final form an d disposition. This competition would appear to continue into early po stnatal periods. It appears, however, that undamaged trigeminal primar y afferents are most likely to expand their central terminal arbors in to adjacent partially denervated territory if the denervation is exten sive and includes more than one row of mystacial vibrissae.