Early establishment of adult-like nigrotectal architecture in the neonatal cat: A double-labeling study using carbocyanine dyes

• Published in: Neuroscience Vol. 137; no. 4; pp. 1309 - 1319
• Main Authors: Gabriele, M.L., Smoot, J.E., Jiang, H., Stein, B.E., McHaffie, J.G.
• Format: Journal Article
• Language: English
• Published: Oxford Elsevier Ltd 2006; Elsevier
• Subjects: Animals; Animals, Newborn; Axonal Transport; basal ganglia; Biological and medical sciences; Carbocyanines; Cats; Coloring Agents; development; DiI; Eye and associated structures. Visual pathways and centers. Vision; Fundamental and applied biological sciences. Psychology; Models, Animal; Neurons - cytology; Neurons - physiology; oculomotor; substantia nigra; Substantia Nigra - anatomy & histology; Substantia Nigra - growth & development; Substantia Nigra - physiology; Superior Colliculi - anatomy & histology; Superior Colliculi - growth & development; Superior Colliculi - physiology; superior colliculus; Vertebrates: nervous system and sense organs; AChE; substantia nigra; development; basal ganglia; DiI; superior colliculus; oculomotor; SC; SNl; RF; sgi; SNr; so; sgp; DiD; sgs; Human; Fissipedia; Carnivora; Dil; Central nervous system; Basal ganglion; Colliculus superior; Encephalon; Vertebrata; Mammalia; Locus niger; Newborn; Visual pathway; Animal; Cat; Development; Early
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/j.neuroscience.2005.10.035

Virtually nothing is known about the ontogeny of substantia nigra, pars reticulata projections to the midbrain superior colliculus, even though this pathway is critical for the basal ganglia modulation of midbrain-mediated visuomotor behaviors. The present studies used the lipophilic carbocyanine dyes 1,1′-dioctodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate and 1,1′-dioctodecyl-3,3,3′,3′-tetramethylindodi, 4-chlorobenzenesulfonate salt to examine the crossed and uncrossed nigrotectal projections in neonatal cats, from parturition to 14 days postnatal (the technical limits of the tracing technique). In retrograde experiments, paired placement of the dyes in each superior colliculus produced numerous retrogradely-labeled nigrotectal neurons, with the uncrossed neurons far out numbering their crossed counterparts. No double-labeled neurons were observed, indicating that crossed and uncrossed nigrotectal neurons are segregated at birth. In anterograde experiments, dye placements into each substantia nigra, pars reticulata resulted in an iterative series of labeled patches, aligned medial-to-lateral across the intermediate and deep superior colliculus, a pattern reminiscent of the adult. Uncrossed neonatal axons had simple linear morphologies with few branch points; by contrast, crossed axons displayed more extensive terminal arbors that were distributed diffusely throughout the rostrocaudal extent of the contralateral superior colliculus In the final series of experiments, one dye was placed unilaterally in the substantia nigra, pars reticulata, while the second dye was positioned in the predorsal bundle, in order to bilaterally label superior colliculus output neurons. Although both crossed and uncrossed axons appeared to have contacted superior colliculus output neurons, crossed axons preferentially targeted the soma and proximal dendrites, whereas uncrossed terminals were distributed more distally. Throughout this early postnatal period, no significant changes in cellular morphologies or gross modification of terminal projection patterns were observed; however, the presence of growth cones in even the oldest animals studied suggests that the refinement of the nigrotectal projections extends well into postnatal life. Nevertheless, the segregation of crossed and uncrossed nigrotectal neurons into a highly organized afferent mosaic that has established synaptic contacts with superior colliculus output neurons indicates that many of the salient features characterizing nigrotectal projections are established prior to the onset of visual experience.