Primary Afferent Plasticity Following Partial Denervation of the Trigeminal Brainstem Nuclear Complex in the Postnatal Rat
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TheJournalof Neuroscience,February1994, 74(2): 721-739 Primary Afferent Plasticity following Partial Denervation of the Trigeminal Brainstem Nuclear Complex in the Postnatal Rat William E. Renehan,’ Robert S. Crissman,* and Mark F. Jacquin3 ‘Laboratory of Gastrointestinal, Gustatory and Somatic Sensation, Division of Gastroenterology, Henry Ford Hospital, Detroit, Michigan 48202, 2Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699, and 3Department of Anatomy and Neurobiology, St. Louis University, School of Medicine, St. Louis, Missouri 63104 Although interaxonal competition is believed to be an es- no evidence that the absolute amount of terminal arbor was sential component of the normal development of numerous similarly increased (as would be the case if sprouting had mammalian neuronal populations, there is considerable de- occurred; see Renehan et al., 1969). We would therefore bate regarding the role of competition in the development conclude that the undamaged afferents had undergone arbor and maintenance of the somatic sensory system. The results expansion, but not sprouting. These data are consistent with of recent investigations suggest that trigeminal primary af- prior suggestions that trigeminal primary afferents utilize ferents may compete for target territory in the brainstem, some form of competitive interaction(s) to establish their but it is unclear whether these interactions continu,e after final form and disposition. This competition would appear to birth. The present study explored this important issue by continue into early postnatal periods. It appears, however, examining the response of individual trigeminal primary af- that undamaged trigeminal primary afferents are most likely ferent neurons to partial denervation of the trigeminal brain- to expand their central terminal arbors into adjacent partially stem nuclear complex at early postnatal ages. We utilized denervated territory if the denervation is extensive and in- intracellular recording and HRP injection techniques to label cludes more than one row of mystacial vibrissae. primary afferent central terminal arbors in rats that sustained [Key words: development, competition, somatosensory electrocautery of mystacial vibrissae in rows A, C, and E on cortex, sensory system, intracellular recording, reorgani- the day of birth. A total of 42 low-threshold trigeminal primary za tion] afferent neurons were labeled in subnucleus interpolaris. Twenty-eight of these afferents supplied undamaged B or D There is a large body of evidence to support the contention that row vibrissae while 14 supplied lesioned vibrissae. Quali- the formation of neuronal pathways, including those pathways tative and quantitative analyses revealed that the arbors associatedwith sensory systems, is dependent on both genetic associated with undamaged afferents were enlarged (mean and epigenetic processes(for reviews, see Dodd and Jessell, arbor area of 135 12 Ifr 790.67 pm* vs normal area of 6 130 1988; Jacobson, 1991). The initial stagesof axon guidance are * 214 pm2) and were oriented toward the adjacent (partially most likely under genetic control. The final disposition of axons, denervated) territory. There was no significant change in the however, seemsto be sensitive to environmental influences. size of the lesioned afferent arbor area. The perimeter of Once vertebrate axons arrive in the vicinity oftheir final targets, the lesioned afferent arbors was increased, however, sug- they often form highly ordered projections within the target field. gesting that the arbor shape had changed. This was con- The mechanismsresponsible for the development and main- firmed with a form factor calculation that indicated that the tenance of these patterned projections are not understood. Ev- circularity of the arbors associated with lesioned vibrissae idence obtained in the visual system indicates that pattern for- was significantly reduced. Thus, while the arbors of undam- mation is precededby a period ofaxon arbor proliferation (Ferster aged afferents were enlarged and oriented in the direction and LeVay, 1978; Stretavan and Shatz, 1986; Naegele et al., of the partially denervated territory, the lesioned afferent 1988; Callaway and Katz, 1990, 1991; Jhaveri et al., 1991; arbors were not enlarged but assumed a flattened/elongate O’Leary, 1992), with the proliferating axons emitting collateral morphology within their appropriate row. The lesion-induced sprouts that may be widely distributed throughout the terminal increase in the size of the undamaged afferent arbors was region. Recent data suggestthat many of these sprouts synapse not associated with an increase in the number of bouton- on neurons in “inappropriate” territory (Campbell and Shatz, like fiber swellings. The density of boutons was only 25% 1992). Under normal circumstances,however, thesewidespread the value seen in normal animals. Thus, while the area sup- projections are not maintained. Driven by an unknown signal plied by the undamaged afferent arbors increased, there was (or multiple signals),the axons undergo a period of collateral elimination (seeO’Leary, 1992, for review). Thus, the incorrect collaterals are “pruned” from the axon arbor, resulting in the Received Mar. 3, 1993; revised July 19, 1993; accepted July 26, 1993. appropriate patterned projection. What causes this selective We thank Susan Stansel and Dana Randall for excellent technical assistance. elimination of axon terminals? Although a number of mecha- This work was supported by DE 07734 and DE 07662. nisms have been proposed to account for the selective main- Correspondence should be addressed to William E. Renehan, Ph.D., Laboratory of Gastrointestinal, Gustatory and Somatic Sensation, Division of Gastroenter- tenance of a given population of axons (for review, seeFraser, ology, Henry Ford Hospital, 2799 West Grand Boulevard, Detroit, MI 48202. 1989; Fraser and Perkel, 1990) it appearslikely that someform Copyright 0 1994 Society for Neuroscience 0270-6474/94/140721-19$05.00/O of competitive interaction(s) is fundamental to this process. 722 Renehan et al. - Trigeminal Primary Afferent Plasticity As discussed by Chiaia et al. (1992), interaxonal competition evidence of abnormal projections from mandibular or undam- has been implicated in the development of numerous neuronal aged ophthalmic-maxillary fibers in the rat. In the hamster, systems (for additional discussion, see Cotman et al., 1981; however, neonatal IO lesions were associated with substantial Jacobson, 199 1). There is considerable debate regarding the role increases in mandibular terminal fields in the trigeminal brain- of competition in the development and maintenance of the so- stem nuclear complex. Jacquin and Rhoades suggested that the matic sensory system, however. Investigators have typically ex- relative immaturity of the hamster trigeminal brainstem com- amined competitive interactions by removing one or more in- plex at birth might be linked to a greater growth potential of puts to a given target, allowing the remaining input(s) to have the undamaged primary afferents. Waite and Permentier (199 1) a competitive advantage. Liu and Chambers pioneered this work and Jacquin et al. (1993) have recently employed the IO tran- by partially denervating the cat spinal cord (Liu and Chambers, section model to reexamine the interaction between the central 1958). They found that the distribution of the intraspinal dorsal terminal arbors ofrat trigeminal primary afferents. These studies root processes of an intervening (undamaged) dorsal root was focused on the central projections of primary afferent neurons markedly increased following this partial denervation paradigm. that innervate the postero-orbital and supraorbital sinus hairs. The authors concluded that this increase was the result of the The postero-orbital follicle is supplied by the zygomaticofacial outgrowth of new processes from the spared dorsal root axons nerve, a branch of the maxillary division. The supraorbital vi- (axonal sprouting). This work established axonal sprouting as a brissa is supplied by a branch of the ophthalmic division. Waite phenomenon relevant to plasticity in the CNS and suggested and Permentier (199 1) found that the terminal area correspond- that the central processes of primary afferent neurons compete ing to the central terminations of the postero-orbital afferents with each other for target territory. These observations have was approximately doubled in three ofthe four trigeminal brain- since been expanded by a number of groups, and there is now stem subnuclei following the IO lesion in neonates (a smaller substantial evidence indicating that partial denervation of the but significant increase was also noted when the lesion was spinal cord via the spared root preparation results in an increase performed on postnatal day 7). Jacquin et al. (1993) were able in the density of the projection of the spared root in the segment to show that the neonatal IO injury also results in an increase of entry and adjacent segments (Goldberger and Murray, 1982; in the size of the cytochrome oxidase (CO) patches correspond- Strominger and Woolsey, 1987; McNeil1 et al., 1991; Besse et ing to the postero-orbital and supraorbital vibrissae. These data al., 1992; but see Devor and Claman, 1980; Rodin et al., 1983; suggest that undamaged trigeminal primary afferents may in- Rodin and Kruger, 1984), an increase in the number of un- deed be capable of sprouting into denervated territory under myelinated axons