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Journal of Neuroscience, Vol 12, 62-76, Copyright © 1992 by Society for Neuroscience
Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons
NL Chiaia, CA Bennett-Clarke, M Eck, FA White, RS Crissman and RW Rhoades
Department of Anatomy, Medical College of Ohio, Toledo 43699.
Previous studies have shown that damage to vibrissa follicles in newborn
rats and mice does not alter the brainstem representations of the remaining
vibrissa as demonstrated by staining for mitochondrial enzymes such as
cytochrome oxidase (CO) succinic dehydrogenase. This study asked whether
this lack of effect might be due to the fact that the trigeminal primary
afferents in rodents are already quite well developed at birth. We assessed
this possibility by using CO staining the evaluate patterns in the
brainstems of pre- and postnatal rats. A vibrissa-related pattern began to
emerge in trigeminal nucleus principalis and subnucleus interpolaris (Spl)
by embryonic day (E-) 19 and appeared fully developed by the day of birth
(P-0). We also made partial lesions of the vibrissa pad on E-15-20 and on
P-0, killed pups on P-5-7, and measured the size of the CO-stained patches
in Spl on both sides of the brainstem. The correspondence between CO
patches and clusters of primary afferent terminal arbors was verified in
some animals by combining transganglionic horseradish peroxidase tracing
and CO staining. Vibrissa pad damage on E-15-18 resulted in significant
(20.1-36.9%) increases in the average area of the remaining CO patches in
Spl ipsilateral to the lesion. Vibrissa pad damage on E-19, E-20, and P-0
produced small (6.2-8.9%), but insignificant, increases in patch size in
Spl ipsilateral to the lesion. We used anatomical and electrophysiological
methods to determine whether our lesions altered the trigeminal innervation
of surviving vibrissa follicles. We recorded single trigeminal ganglion
cells from 12 rats that sustained vibrissa pad lesion on E-17. As in normal
rats, all of the 49 vibrissa-sensitive ganglion cells isolated in the
lesioned animals were responsive to deflection of one and only one
vibrissa. We also dissected 11 deep vibrissal nerves from intact follicles
in adult rats that sustained fetal vibrissa pad damage on E-17, and counted
numbers of myelinated axons in 1 microns plastic sections. These data were
compared with counts from corresponding follicles on the intact side of the
face. The average number of myelinated axons innervating follicles in the
damaged vibrissa pads was 196.8 +/- 27.9, and that for the corresponding
contralateral nerves was 194.6 +/- 25.7. These data suggest that
competitive interactions among the central arbors of trigeminal primary
afferents in fetal life may influence the development of central vibrissa
representations and, further, that lesion-induced central changes need not
be correlated with alterations in the peripheral innervation of undamaged
follicles.
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