Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons

Nicolas L. Chiaia, Carol A. Bennett-Clarke, Marcia Eck, Fletcher White, Robert S. Crissman, Robert W. Rhoades

Research output: Contribution to journalArticle

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Abstract

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 to 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 lesions 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 μm 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.

Original languageEnglish (US)
Pages (from-to)62-76
Number of pages15
JournalJournal of Neuroscience
Volume12
Issue number1
StatePublished - 1992
Externally publishedYes

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Vibrissae
Afferent Neurons
Electron Transport Complex IV
Brain Stem
Staining and Labeling
Axons
Parturition
Trigeminal Nuclei
Trigeminal Ganglion
Succinate Dehydrogenase
Horseradish Peroxidase
Ganglia
Plastics
Rodentia

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Chiaia, N. L., Bennett-Clarke, C. A., Eck, M., White, F., Crissman, R. S., & Rhoades, R. W. (1992). Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons. Journal of Neuroscience, 12(1), 62-76.

Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons. / Chiaia, Nicolas L.; Bennett-Clarke, Carol A.; Eck, Marcia; White, Fletcher; Crissman, Robert S.; Rhoades, Robert W.

In: Journal of Neuroscience, Vol. 12, No. 1, 1992, p. 62-76.

Research output: Contribution to journalArticle

Chiaia, NL, Bennett-Clarke, CA, Eck, M, White, F, Crissman, RS & Rhoades, RW 1992, 'Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons', Journal of Neuroscience, vol. 12, no. 1, pp. 62-76.
Chiaia, Nicolas L. ; Bennett-Clarke, Carol A. ; Eck, Marcia ; White, Fletcher ; Crissman, Robert S. ; Rhoades, Robert W. / Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons. In: Journal of Neuroscience. 1992 ; Vol. 12, No. 1. pp. 62-76.
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abstract = "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 to 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 lesions 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 μm 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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