Organization of Major Telencephalic Pathways in an Elasmobranch, the Thornback Ray <i>Platyrhinoidis triseriata</i>

Abstract

The forebrain of elasmobranchs is well developed, and in some species the relative brain/body weight is comparable to that in mammals. However, little is known about the organization of major telencephalic pathways. We injected biotinylated dextran amines into the olfactory bulb, lateral pallium, dorsomedial pallium, and the forebrain bundles of the thornback ray, Platyrhinoidis triseriata. Secondary olfactory fibers from the bulb innervate the lateral pallium, the ventral division of the rostral telencephalon and area superficialis basalis. Retrogradely labeled cells were seen exclusively in the lateral periventricular area. The projections of the lateral pallium appeared basically similar to those of the olfactory bulb, but labeling was much denser in the superficial part of area basalis. Some fibers were also seen to innervate the posterior tuberal nucleus. Injections into the dorsomedial pallium revealed a major input from area basalis. Only a few cells were retrogradely labeled in the dorsal thalamus and posterior lateral thalamic nucleus. Major efferents of the dorsomedial pallium appear to reach the contralateral inferior lobe of the hypothalamus and the lateral mesencephalic nucleus. Tracer injections into the forebrain bundles retrogradely labeled many cells in the diencephalon and the mesencephalon and also revealed terminal fields in area superficialis basalis. In addition, a large number of cells were labeled in the dorsomedial pallium. Descending telencephalic fibers innervate heavily the inferior lobes and the lateral mesencephalic nucleus. Our results show that higher order olfactory pathway courses from the lateral pallium through area basalis to the dorsomedial pallium and that ascending non-olfactory input is integrated in area superficialis basalis and the dorsal pallium along with olfactory information, rather than being processed in separate, non-olfactory centers.

A Developmental Approach to Forebrain Organization in Elasmobranchs: New Perspectives on the Regionalization of the Telencephalon

“…One of Prof. Nieuwenhuys' greatest works, the extraordinary threevolume set on the central nervous system of vertebrates, also includes a chapter on the central nervous system in cartilaginous fishes [Smeets, 1998] that is essential to an understanding of central nervous system organization in chondrichthyans. Finally, R. Glenn Northcutt has also contributed significantly to studies of the forebrain in chondrichthyan fishes [Northcutt, 1978[Northcutt, , 1989Hofmann and Northcutt, 2008], particularly in showing the importance of sampling brain variation among different species and recognizing adaptive patterns.…”

“…Experimental anatomical studies demonstrating the existence of non-olfactory connections in the telencephalon of elasmobranchs [Ebbesson and Schroeder, 1971;Schroeder and Ebbesson, 1974;Graeber et al, 1978;Luiten, 1981a, b;Smeets and Northcutt, 1987], and those revealing that only a restricted area of the telencephalon receives secondary olfactory fibers [Hofmann and Northcutt, 2008; see also Smeets, 1990Smeets, , 1998 for reviews] have been especially important, as they refuted the classic conception that elasmobranchs have a simple, exclusively olfactory telencephalon. With the improvement of immunohistochemical techniques, and the development of antibodies against diverse neuroactive substances, the complexity of the telencephalon in elasmobranchs has been increasingly revealed.…”

Forebrain Organization in Elasmobranchs

“…There are also differences in the presence of contralateral olfactory projections. Whereas no contralateral olfactory projections were found in the nurse shark Ginglymostoma [Ebbesson and Heimer, 1970;Ebbesson, 1972] and Raja [Smeets, 1983], such fiber tracts were observed in the catshark Scyliorhinus [Smeets, 1983], the bonnethead shark Sphyrna [Dryer and Graziadei, 1994], and the thornback guitarfish Platyrhinoidis [Hofmann and Northcutt, 2008]. In the last species, ipsilateral projections to the entopeduncular nucleus were also found.…”

“…Heimer [1969] and Ebbesson and Heimer [1970] were the first to show that secondary and tertiary olfactory projections are restricted to the lateral pallium and area superficialis basalis in a nurse shark, Ginglymostoma . Later studies largely confirmed these reports, although the extent of the projections and the reported presence of crossed olfactory projections vary, depending on the species and the authors [Smeets, 1983;Dryer and Graziadei, 1994;Hofmann and Northcutt, 2008].…”

“…Secondary olfactory projections have been investigated in the nurse shark Ginglymostoma [Heimer, 1969;Ebbesson and Heimer, 1970;Ebbesson, 1972], the catshark Scyliorhinus , a skate, Raja [Smeets, 1983], the bonnethead shark Sphyrna [Dryer and Graziadei, 1994], and the thornback guitarfish, Platyrhinoidis [Hofmann and Northcutt, 2008]. The major target of the olfactory fibers is the lateral pallium, but some fibers also extend into the area superficialis basalis in all species, except in Raja [Smeets, 1983].…”