Possible Multiple Evolution of Indirect Telencephalo-Cerebellar Pathways in Teleosts: Studies in Carassius Auratus and Pantodon Buchholzi
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Cell Tissue Res (1993) 274:447-455 Cell Tissue Research Springer-Verlag 1993 Possible multiple evolution of indirect telencephalo-cerebellar pathways in teleosts: studies in Carassius auratus and Pantodon buchholzi Mario F. Wullimann 1, Dietrich L. Meyer 2 i Institut fiir Hirnforschung,Universit/it Bremen, FB 2-NW II, Postfach 33 04 40, D-28334 Bremen, Germany 2 Abteilung Neuroanatomie, Zentrum Anatomie, Universit/it G6ttingen, D-37075 GSttingen, Germany Received: 1 March 1993 / Accepted: 30 April 1993 Abstract. Among vertebrates, telencephalo-pontine sys- pendently (Roth and Wullimann, in press). In contrast to tems exist only in birds and mammals. However, three birds and mammals, teleost fishes lack a pons. However, nuclei in the diencephalon and mesencephalon of teleost three nuclei in the diencephalon and mesencephalon of fishes have been indicated analogous to the pons to various teleost species (see Discussion) have been indicat- represent relay stations between telencephalon and cere- ed as relay stations for telencephalo-cerebellar pathways. bellum. Since two of these nuclei (dorsal preglomerular (1) Some euteleosts, the evolutionarily most derived nucleus, dorsal tegmental nucleus) have only been de- teleost clade (Fig. 5), possess a telencephalo-cerebellar scribed in the highly derived, electrosensory mormyrids, pathway via the nucleus paracommissuralis, which is lo- we investigated telencephalic connections in two non- cated most dorsally in the diencephalon (Karten and Fin- electrosensory teleosts, the goldfish Carassius auratus ger 1976; Ito et al. 1982; Striedter 1990). The nucleus and and the freshwater butterflyfish Pantodon buchholzi, and the related pathway have only been described in eu- cerebellar connections only in the latter species, since for teleosts (Wullimann and Northcutt 1988). Among eu- C. auratus these connections are already established. teleosts, however, the cyprinids have been argued to lack Horseradish peroxidase tracing reveals that C. auratus a nucleus paracommissuralis (Ito et al. 1982). In contrast, has a dorsal tegmental nucleus and a paracommissural Wullimann and Northcutt (1988) described a minute nu- nucleus both of which are telencephalo-recipient and cleus paracommissuralis in the cyprinid Carassius aura- project to the cerebellum, and that P. buchholzi has a tus, based on its projection to the corpus cerebelli. dorsal preglomerular nucleus with such connections. (2) A second telencephalo-cerebellar pathway via a These results extend our knowlegde of the distribution dorsal tegmental nucleus in the African electric fish and, therefore, the phylogeny of telencephalo-cerebellar Gnathonemus petersi has been discovered more recently systems in teleosts. Similar to tetrapods, teleosts appear (Meek et al. 1986; Wullimann and Northcutt 1990). There to have developed telencephalo-cerebellar systems sever- is evidence (see Discussion) that this nucleus receives al times independently. telencephalic input and projects to the cerebellum in var- ious other teleost species belonging to the osteoglosso- Key words: Cerebellum - Evolution - Brain, vertebrate - morph as well as the euteleost clades. However, it has not Pons Telencephalon - Carassius auratus, Pantodon been demonstrated that the two connections exist togeth- buchholzi ( Teleostei) er in a single teleost species except for the highly special- ized G. petersi. (3) In addition, G. petersi displays a third telen- cephalo-cerebellar pathway. A dorsal subdivision of the diencephalic preglomerular area, the dorsal preglomeru- Introduction lar nucleus, has a massive terminal field from the telen- cephalon (Wullimann and Northcutt 1987, 1990). It has The telencephalon of mammals and birds exerts influence previously been shown that this nucleus (dorsal anterior on the cerebellum via metencephalic pontine nuclei. pretectal nucleus of Meek et al. 1986) projects heavily to Comparable systems have not been described in other the corpus cerebelli. This diencephalic telencephalo-cere- tetrapods. The distant phylogenetic relationship of these bellar relay center can reasonably be assumed to be in- two major vertebrate groups suggests that avian and volved in the processing of electrosensory information mammalian telencephalo-pontine systems evolved inde- (i.e., electrolocation), since it receives ascending input from the lateral nucleus of the torus semicircularis, the Correspondence to: M.F. Wullimann mesencephalic target of the electrolocative component of 448 this sensory modality (Finger et al. 1981). As electrore- area dorsalis telencephali (telencephalic nomenclature ception evolved newly in mormyrids (Bullock et al. 1983), and subdivisions of Nieuwenhuys and Meek 1990), addi- Wullimann and Northcutt (1990) have interpreted this tional portions of the area dorsalis (e.g., the medial and telencephalo-preglomerulo-cerebellar pathway as a dorsal zones) were also partially affected. After such uniquely derived (autapomorphic) feature of mormyrids. rather large injections into the dorsal area of the telen- However, non-electrosensory osteoglossomorphs have cephalon, the heavily labeled medial and lateral forebrain not been investigated for the presence of this pathway. bundles can be traced into the diencephalon (Fig. la). At The goal of the present study is to test further the this level, the lateral forebrain bundle gives off a large evolutionary polarity of the three telencephalo-cerebellar dorsal tract. The latter contains efferent fibers which systems observed in various teleost species. Since the eventually reach the nucleus paracommissuralis (Fig. lc), cerebellar connections have been extensively document- the dorsal tegmental nucleus (Figs. ld,e;4c) and the cen- ed in C. auratus (Wullimann and Northcutt 1988), we tral zone of the optic tectum (Fig. lb-0. Additional effer- chose this ostariophysine species to investigate whether ents, which deviate from the lateral forebrain bundle even the nucleus paracommissuralis and the dorsal tegmental more rostrally, reach the ventrolateral thalamic and dor- nucleus are telencephalo-recipient. Further, we investi- sal posterior thalamic nuclei (Fig. la,b). The medial fore- gated the non-electrosensory osteoglossomorph R buch- brain bundle courses ventrocaudally and reaches the pos- holzi for the presence of a telencephalo-cerebeilar path- terior tuberal nucleus, where labeled cells and terminals way via the dorsal preglomerular nucleus. are observed (Fig. ld). The neuroanatomical terminology is that of Braford The lateral forebrain bundle gives off terminals to the and Northcutt (1983), as modified by Wullimann and anterior, lateral, and medial preglomerular nuclei. In Northcutt (1990) and Wullimann and Meyer (1990). contrast to P. buchholzi, there is no separate telen- cephalo-recipient preglomerular nucleus dorsal to the lateral pregtomerular nucleus. Many retrogradely labeled cells are present in these three preglomerular nuclei in C. Materials and methods auratus, and in the posterior thalamic and the sub- glomerular nuclei (Fig. la-e). However, the tertiary gus- Horseradish peroxidase (HRP) tracing experiments tatory nucleus, the commissural preglomerular nucleus and the corpus mammillare are devoid of label. Two teleostean species, the goldfish (Carassius auratus) and the Additional efferent projections which run in the later- freshwater butterflyfish (Pantodon buchhoIzi) were used in the al forebrain bundle, reach the anterior tuberal nucleus, present study. HRP injections were made into the telencephalon (C. auratus: 9 cases; P. buchholzi: 4 cases) or into the cerebellum (P. the nucleus of the lateral torus, the diffuse and, strongly, buchholzi: 2 cases). The animals were deeply anesthetized in a dilute the central nuclei of the inferior lobe (Fig. 1a-e). Further solution of tricaine methanesulfonate (MS 222, Sigma, Deisenhofen, caudally, the superior raphe and the locus coeruleus are Germany). A small cranial hole was made at the appropriate loca- retrogradely labeled (Fig. 10. All connections are strictly tion and solid HRP (Boehringer, Mannheim, Germany) was pin-in- ipsilateral, with the exception of the ones to and from the jected into the telencephalon or the corpus cerebelli. A piece of posterior tuberal nucleus, from the superior raphe and Gelfoam (Upjohn) was placed onto the injection site and the wound closed with Histoacryl (Braun, Melsungen, Germany). from the locus coeruleus. After survival times ranging from 1 to 6 days, the animals were re-anesthetized with MS 222 and perfused transcardially with cold teleost Ringer's solution, followed by 4% glutaraldehyde in 0.1 M Pantodon buchholzi phosphate buffer (pH 7.4). The brains were removed from the cra- nia, postfixed for 1 h in the same fixative containing 30% sucrose Telencephalic connections. The specific connections of and cryprotected overnight in 30% sucrose-phosphate buffer before they were cut transversely on a cryostat at a thickness of 25 gm. The most telencephalic subdivisions (e.g., with the pre- sections were reacted according to either the Hanker-Yates proto- glomerular area) in P. buchholzi were recently investigat- col (Hanker et al. 1977) or the protocol of Ebbesson et al. (1981). ed in detail with the carbocyanine dye DiI (Wullimann Some sections were counterstained with cresyl violet. and Roth 1992; and unpublished observations) and will be published separately. Here, only HRP-data on telen- cephalic injections in P. buchholzi are reported which se- Histological procedures lectively relate to nuclei also projecting