Anuran dorsal column nucleus: organization, immunohistochemical characterization, and fiber connections in Rana perezi and Xenopus laevis. J Comp Neurol

Department of Cell Biology, Universidad Complutense de Madrid, Spain.
The Journal of Comparative Neurology (Impact Factor: 3.23). 01/1996; 363(2):197-220. DOI: 10.1002/cne.903630204
Source: PubMed


As part of a research program on the evolution of somatosensory systems in vertebrates, the dorsal column nucleus (DCN) was studied with (immuno)histochemical and tract-tracing techniques in anurans (the large green frog, Rana perezi, and the clawed toad, Xenopus laevis). The anuran DCN contains some nicotinamide adenine dinucleotide phosphate diaphorase-positive neurons, very little calbindin D-28k, and a distinct parvalbumin-positive cell population. The anuran DCN is innervated by primary and non-primary spinal afferents, by primary afferents from cranial nerves V, VII, IX, and X, by serotonin-immunoreactive fibers, and by peptidergic fibers. Non-primary DCN afferents from the spinal cord appear to arise throughout the spinal cord, but particularly from the ipsilateral dorsal gray. The present study focused on the efferent connections of the DCN, in particular the targets of the medial lemniscus. The medial lemniscus could be traced throughout the brainstem and into the diencephalon. Along its course, the medial lemniscus gives off collaterals to various parts of the reticular formation, to the octavolateral area, and to the granular layer of the cerebellum. At mesencephalic levels, the medial lemniscus innervates the lateral part of the torus semicircularis as well as various tegmental nuclei. A striking difference between the two species studied is that while in R. perezi medial lemniscal fibers do not reach the tectum mesencephali, in X. laevis, intermediate and deep tectal layers are innervated. Beyond the midbrain, both dorsal and ventral thalamic areas are innervated by the medial lemniscus. The present study shows that the anuran "lemniscal pathway" is basically similar to that of amniotes.

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    • "As in birds and mammals, a projection to the torus semicircularis mediated by the medial lemniscus and originating from the DCN or one of its funicular nuclear homologs has been described in a teleost (Finger, 2000) and in amphibians (Muñoz et al., 1995). In fish and amphibians, auditory (octaval), mechanosensory and electrosensory inputs to the torus have traditionally been described as terminating separately (Bell, 1981; McCormick, 1982; 1989; De Wolf et al., 1983; Haugede-Carre, 1983; Echteler, 1984; Finger and Tong, 1984; Boord and Northcutt, 1988), but in birds, reptiles and lamprey there seems to be some overlap of auditory and somatosensory inputs to the torus (Belekhova et al., 1985; Künzle, 1986 Wild, 1995; present study; Gonzáles et al., 1999). "
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    ABSTRACT: The Wulst of birds, which is generally considered homologous with the isocortex of mammals, is an elevation on the dorsum of the telencephalon that is particularly prominent in predatory species, especially those with large, frontally placed eyes, such as owls. The Wulst, therefore, is largely visual, but a relatively small rostral portion is somatosensory in nature. In barn owls, this rostral somatosensory part of the Wulst forms a unique physical protuberance dedicated to the representation of the contralateral claw. Here we investigate whether the input to this "claw area" arises from dorsal thalamic neurons that, in turn, receive their somatosensory input from the gracile nucleus. After injections of biotinylated dextran amine into the gracile nucleus and cholera toxin B chain into the claw area, terminations from the former and retrogradely labeled neurons from the latter overlapped substantially in the thalamic nucleus dorsalis intermedius ventralis anterior. These results indicate the existence in this species of a "classical" trisynaptic somatosensory pathway from the body periphery to the telencephalic Wulst, via the dorsal thalamus, one that is likely involved in the barn owl's predatory behavior. The results are discussed in the context of somatosensory projections, primarily in this and other avian species.
    The Journal of Comparative Neurology 07/2008; 509(2):156-66. DOI:10.1002/cne.21731 · 3.23 Impact Factor
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    • "In N.IX–X, cell perikarya and neurites were immunolabeled with the calbindin antibody (Fig. 1 A). Calbindin expression elsewhere in the rhombencephalon was limited to the Purkinje cells of the cerebellum, cells of the dorsal tegmental area of the medulla, and sparse cells in the reticular formation and central gray as well as the dorsal rhombencephalic calbindin-expressing nuclei previously described by Muñoz et al. (1995) "
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    ABSTRACT: Androgens can rescue axotomized motor neurons from cell death. Here we examine a possible mechanism for this trophic action in juvenile Xenopus laevis: regulation of a calcium-binding protein, calbindin, after axotomy. Western analysis revealed that a monoclonal antibody to calbindin D specifically recognizes a single approximately 28 kDa band in X. laevis CNS and rat cerebellum. Retrograde transport of peroxidase combined with immunohistochemistry demonstrated that somata, axons, and synaptic terminals of laryngeal motor neurons in nucleus (N.) IX-X of X. laevis are calbindin-positive. The number of calbindin-positive cells was compared in the intact and axotomized sides of N.IX-X of gonadectomized males that were either hormonally untreated or DHT-treated for 1 month. Although axotomy decreased the number of calbindin-positive cells by 86% in hormonally untreated males, the decrease was only 56% in DHT-treated animals. Compared with hormonally untreated animals, the number of calbindin-labeled cells in N.IX-X of DHT-treated males was increased in both the intact (14%) and axotomized sides (75%). We conclude that axotomy decreases and that DHT enhances calbindin immunoreactivity in N.IX-X. Axotomy-induced decrease in calbindin immunoreactivity precedes cell loss in N.IX-X and may impair the capacity of motor neurons to regulate cytoplasmic calcium. Androgen-mediated maintenance of calbindin expression is thus a candidate cellular mechanism for trophic maintenance of hormone target neurons.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 11/1997; 17(19):7396-403. · 6.34 Impact Factor
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    ABSTRACT: The distribution of NADPH-diaphorase (ND) activity was histochemically investigated in the brain of the frog Rana perezi. This technique provides a highly selective labeling of neurons and tracts. In the telencephalon, labeled cells are present in the olfactory bulb, pallial regions, septal area, nucleus of the diagonal band, striatum, and amygdala. Positive neurons surround the preoptic and infundibular recesses of the third ventricle. The magnocellular and suprachiasmatic hypothalamic nuclei contain stained cells. Numerous neurons are present in the anterior, lateral anterior, central, and lateral posteroventral thalamic nuclei. Positive terminal fields are organized in the same thalamic areas but most conspicuously in the visual recipient plexus of Bellonci, corpus geniculatum of the thalamus, and the superficial ventral thalamic nucleus. Labeled fibers and cell groups are observed in the pretectal area, the mesencephalic optic tectum, and the torus semicircularis. The nuclei of the mesencephalic tegmentum contain abundant labeled cells and a conspicuous cell population is localized medial and caudal to the isthmic nucleus. Numerous cells in the rhombencephalon are distributed in the octaval area, raphe nucleus, reticular nuclei, sensory trigeminal nuclei, nucleus of the solitary tract, and, at the obex levels, the dorsal column nucleus. Positive fibers are abundant in the superior olivary nucleus, the descending trigeminal, and the solitary tracts. In the spinal cord, a large population of intensely labeled neurons is present in all fields of the gray matter throughout its rostrocaudal extent. Several sensory pathways were heavily stained including part of the olfactory, visual, auditory, and somatosensory pathways. The distribution of ND-positive cells did not correspond to any single known neurotransmitter or neuroactive molecule system. In particular, abundant codistribution of ND and catecholamines is found in the anuran brain. Double labeling techniques have revealed restricted colocalization in the same neurons and only in the posterior tubercle and locus coeruleus. If ND is in amphibians a selective marker for neurons containing nitric oxide synthase, as generally proposed, with this method the neurons that may synthesize nitric oxide would be identified. This study provides evidence that nitric oxide may be involved in novel tasks, primarily related to forebrain functions, that are already present in amphibians.
    The Journal of Comparative Neurology 03/1996; 367(1):54-69. DOI:10.1002/(SICI)1096-9861(19960325)367:1<54::AID-CNE5>3.0.CO;2-I · 3.23 Impact Factor
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