Full-length reviewChemoarchitecture of the anuran auditory midbrain
Introduction
In the auditory pathway of anurans, the midbrain torus semicircularis and tegmentum are of considerable interest as targets of neurotransmitters and neuromodulators. The principal nucleus of the torus semicircularis is the main projection area for ascending auditory afferents, whereas the magnocellular nucleus and especially the laminar nucleus constitute ascending and descending projections with sensory, premotor and motor areas in all parts of the brain [24], [58], [95]. Neurons of the midbrain tegmentum also respond to auditory stimulation and, similar to laminar nucleus neurons, project to sensory, premotor, and motor regions [58]. All three subnuclei of the torus semicircularis as well as the tegmentum receive descending direct or indirect input from the striatum and the dorsal thalamus. Especially the response of laminar nucleus neurons to auditory nerve stimulation could be altered by activation of forebrain efferents [21]. Since behavioral studies have shown that torus semicircularis and tegmentum are involved in audiomotor integration [86], [87], [95], shaping of neuronal responses in these nuclei may contribute essentially to selection and modification of motor programs according to the internal state of the animal. In order to understand the anatomical basis of these interfacing mechanisms, it is essential to work out the functional subarchitecture of the auditory midbrain in greater detail.
The central nervous system of anuran amphibians has been the object of numerous immunohistochemical studies. However, most of these have concentrated on the visual midbrain or have given overall distribution patterns without taking the toral subdivisions into account. Therefore, the aim of this study was to reveal the termination sites of various neurotransmitter inputs to the torus semicircularis and the midbrain tegmentum in detail. The nuclei giving rise to these inputs should be identified by comparing the pattern of immunolabeled nuclei in the entire brain with the results of tracing studies on toral connectivity [24], [57]. To gain additional insight into the functional organization, we wanted to describe the localization of neurons immunopositive for the different transmitters within the auditory midbrain. Furthermore, data from an earlier study on the distribution of steroid-concentrating neurons in Xenopus laevis [44], [45] should be corroborated in other species. We therefore investigated the distribution of serotonin, leucine–enkephalin, substance P, tyrosine–hydroxylase, dopamine D2-receptor, parvalbumin, aspartate, GABA, and estrogen-binding protein (estrogen-bp) immunoreactivity.
Many investigations have been carried out on neobatrachian species (e.g., Rana, Hyla). In order to broaden our knowledge about the Archaeobatrachia, we chose the species Bombina orientalis, Discoglossus pictus (Discoglossidae), and Xenopus laevis (Pipidae).
Section snippets
Materials and methods
A total of 61 adult animals was used in this study comprising 30 Discoglossus pictus, 19 Xenopus laevis, and 12 Bombina orientalis. The animals were taken from the laboratory’s breeding stock. For the detection of estrogen-bp reproductively active specimen (females with well-developed ovaries, males with thumb pads) were chosen. All antibodies were applied on animals of both sexes. The antibodies were obtained from different sources: polyclonal serotonin-antibody (rabbit) from Dianova (Hamburg,
Specificity
The procedure described above labeled neuronal cell bodies, dendrites, and terminal structures with a strong contrast to the background. In the case of the dopamine D2-receptor, only somata and basal dendrites were stained; no labeling of terminal structures could be achieved. The antibody against estrogen-bp labeled only the nuclei of neurons. The control sections never showed any immunoreactivity. If not explicitly mentioned, the distribution of the immunoreactive structures did not differ
Immunohistochemical findings
Eight of the antisera (i.e., serotonin, leucine–enkephalin, substance P, GABA, parvalbumin, tyrosine–hydroxylase, dopamine D2-receptor, and aspartate) yielded a specific labeling of somata, dendrites, axonal and terminal structures. Our results did not reveal principal species-specific differences in the distribution of immunoreactive structures in the torus semicircularis. The monoclonal antibody against the estrogen-bp had not been applied in amphibian material before, but yielded a clearly
Acknowledgements
We thank Dr. K. Braun (Magdeburg), Dr. J.J. Milde (Cologne), and Dr. A. Schmidt (Bremen) for providing several antibodies, as well as Abbott Diagnostica (Wiesbaden, Germany) for the generous gift of the estrogen-bp detection kit. Dr. J.J. Milde, Dr. R. Wegerhoff (Kiel), and M. Wallstein gave many helpful comments. This work was supported in part by the Deutsche Forschungsgemeinschaft.
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