Peripheral Influences on Connectivity in the Developing Rat Trigeminal System

The trigeminal system of the rat shows a high degree of discrete anatomical organization. I would like to take this opportunity to review the evidence for peripheral influences on the development of this discrete anatomical organization in both the normal animal and in ones which have suffered neonatal receptor damage. In fact, among other things, I would like to demonstrate that the loss of several whiskers can have as severe an effect on the structural organization of the brain as the loss of an eye. In this brief review I will not attempt to be all-inclusive. Rather, I will focus on the contribution that I and my several collaborators have made. The impetus for our studies of the trigeminal system was the report of Woolsey and Van Der Loos (1970) that in the portion of mouse somatosensory neocortex devoted to the vibrissae representation the cells of layer IV are arranged into discrete aggregates which they termed “barrels.” Further, the number and spatial distribution of the “barrels,” as well as physiological evidence (Woolsey, 1967; Welker, 1971), suggested that in both the rat and mouse there was a unique one-to-one relationship between a particular cytoarchitectonic unit, or “barrel,” and a mystacial vibrissae. Given this high degree of functional and structural organization in the neocortical layer where thalamocortical projections terminate, a natural question to ask was whether or not this discrete organization was also reflected in the afferent projections to this cortical layer. Utilizing anterograde degeneration techniques, I was able to determine that in the rat the terminations of the thalamocortical projections to the vibrissae representation portion of somatosensory cortex are indeed arranged into discrete clusters (Killackey, 1973). Further, the spatial distribution of these clusters replicated the distribution of sinus hair and vibrissae follicles on the muzzle of the rat (Killackey and Leshin, 1975). The discrete nature of these thalamocortical projections is relatively unique and contrasts with the continuous distribution of thalamocortical projections to the face region of cortex in such generalized mammalian species as the opossum and hedgehog (Killackey, 1973). Furthermore, thalamocortical projections are continuous in a rodent species which has developed visual specializations and inhabits an arboreal niche, the Eastern grey squirrel (Killackey, 1973). However, other terrestrial rodents in which the vibrissae are well developed, such as the gerbil, also exhibit discontinuous thalamocortical projections. The available evidence would suggest that this is a specialization of the somatosensory system which has chiefly evolved in small rodents (Woolsey, Welker and Schwartz, 1975). Perhaps the somatosensory system is able to provide the most reliable information about the external world to small rodents which are normally very close to the earth’s surface, spend time burrowing beneath the ground, and generally inhabit a niche where both visual and auditory information is limited. In this regard it should be noted that rats and other rodents have evolved Stereotypic patterns of whisker movements, termed “whisking,” which seem to play an extremely important role in their environmental exploration (Vincent, 1912; Welker, 1964).