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

Department of Cell Biology, Universidad Complutense de Madrid, Spain.
The Journal of Comparative Neurology (Impact Factor: 3.66). 01/1996; 363(2):197-220. DOI: 10.1002/cne.903630204
Source: PubMed

ABSTRACT 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.

  • [Show abstract] [Hide abstract]
    ABSTRACT: The adult Xenopus optic tectum receives and integrates visual and nonvisual sensory information. Nonvisual inputs include mechanosensory inputs from the lateral line, auditory, somatosensory, and vestibular systems. While much is known about the development of visual inputs in this species, almost nothing is known about the development of mechanosensory inputs to the tectum. In this study, we investigated mechanosensory inputs to the tectum during critical developmental stages (stages 42-49) in which the retinotectal map is being established. Tract-tracing studies using lipophilic dyes revealed a large projection between the hindbrain and the tectum as early as stage 42; this projection carries information from the Vth, VIIth, and VIIIth nerves. By directly stimulating hindbrain and visual inputs using an isolated whole-brain preparation, we found that all tectal cells studied received both visual and hindbrain input during these early developmental stages. Pharmacological data indicated that the hindbrain-tectal projection is glutamatergic and that there are no direct inhibitory hindbrain-tectal ascending projections. We found that unlike visual inputs, hindbrain inputs do not show a decrease in paired-pulse facilitation over this developmental period. Interestingly, over this developmental period, hindbrain inputs show a transient increase followed by a significant decrease in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionate (AMPA)/N-methyl-D-aspartate (NMDA) ratio and show no change in quantal size, both in contrast to visual inputs. Our data support a model by which fibers are added to the hindbrain-tectal projection across development. Nascent fibers form new synapses with tectal neurons and primarily activate NMDA receptors. At a time when retinal ganglion cells and their tectal synapses mature, hindbrain-tectal synapses are still undergoing a period of rapid synaptogenesis. This study supports the idea that immature tectal cells receive converging visual and mechanosensory information and indicates that the Xenopus tectum might be an ideal preparation to study the early development of potential multisensory interactions at the cellular level.
    Journal of Neurophysiology 09/2009; 102(6):3392-404. · 3.30 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Lungfishes (dipnoans) are currently considered the closest living relatives of tetrapods. The organization of the cholinergic systems in the brain has been carefully analyzed in most vertebrate groups, and major shared characteristics have been described, although traits particular to each vertebrate class have also been found. In the present study, we provide the first detailed information on the distribution of cholinergic cell bodies and fibers in the central nervous system in two representative species of lungfishes, the African lungfish (Protopterus dolloi) and the Australian lungfish (Neoceratodus forsteri), as revealed by immunohistochemistry against the enzyme choline acetyltransferase (ChAT). Distinct groups of ChAT immunoreactive (ChAT-ir) cells were observed in the basal telencephalon, habenula, isthmic nucleus, laterodorsal tegmental nucleus, cranial nerve motor nuclei, and the motor column of the spinal cord, and these groups seem to be highly conserved among vertebrates. In lungfishes, the presence of a cholinergic cell group in the thalamus and the absence of ChAT-ir cells in the tectum are variable traits, unique to this group and appearing several times during evolution. Other characters were observed exclusively in Neoceratodus, such as the presence of cholinergic cells in the suprachiasmatic nucleus, the pretectal region and the superior raphe nucleus. Cholinergic fibers were found in the medial pallium, basal telencephalon, thalamus and prethalamus, optic tectum and interpeduncular nucleus. Comparison of these results with those from other classes of vertebrates, including a segmental analysis to correlate cell populations, reveals that the cholinergic systems in lungfishes largely resemble those of amphibians and other tetrapods.
    Brain Structure and Function 08/2011; 217(2):549-76. · 7.84 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: There is a clear core-shell organization in the auditory nuclei of amniotes. However, such organization only exists in the mesencephalic, but not in the diencephalic auditory regions of amphibians. To gain insights into how this core-shell organization developed and evolved, we injected a small dose of [(3)H]-thymidine into tadpoles of Xenopus laevis at peak stages of neurogenesis in the mesencephalic and diencephalic auditory areas. Following different survival times, the germinal sites and migrating routes of cells were examined in the shell (laminar nucleus, Tl; magnocellular nucleus, Tmc) and core (principal nucleus, Tp) regions of the mesencephalic auditory nucleus, torus semicircularis (Ts), as well as in the diencephalic auditory areas (posterior thalamic nucleus, P; central thalamic nucleus, C). Double labeling for [(3)H]-thymidine autoradiography and immunohistochemistry for vimentin was also performed to help determine the routes of cell migration. We found three major results. First, the germinal sites of Tp were intercalated between Tl and Tmc, arising from those of the shell regions. Second, although the germinal sites of Tl, Tmc, and Tp were located in the same brain levels (at rostromedial or caudomedial levels of Ts), neurogenesis in Tl or Tmc started earlier than that in Tp. Finally, the P and C were also generated in different ventricle sites. However, unlike Ts their neurogenesis showed no obvious temporal differences. These data demonstrate that a highly differentiated auditory region, such as Tp in Ts, is lacking in the diencephalon of amphibian. Our data are discussed from the view of the constitution and evolutionary origins of auditory nuclei in vertebrates.
    Brain research 02/2011; 1373:67-78. · 2.46 Impact Factor