Chun-Ying Yang

A New Interpretation on the Homology of the Teleostean Telencephalon Based on Hodology and a New Eversion Model

Various hypotheses regarding the homology of the teleostean telencephalon with that of other vertebrates have been proposed to date. However, a firm conclusion on this issue has yet to be drawn. We propose here a new hypothesis with a new eversion model. Our hodological data and the analysis of dorsal telencephalic organization in adult cyprinids suggest that: (1) the area dorsalis pars posterior corresponds to the lateral pallium; (2) ventral region of area dorsalis pars lateralis to the medial pallium; (3) pars medialis, dorsal region of pars lateralis, pars dorsalis, and pars centralis of the area dorsalis to the dorsal pallium, and (4) nucleus taenia to the ventral pallium. We propose in a three dimensional model that the eversion process occurs not only dorsolaterally but also caudolaterally. We consider that the caudally directed component dominates for ventral zones of the pallium, or the lateral and ventral pallia; and the periventricular surface of these zones shift caudally, laterally, and then rostrally in teleosts with pronounced telencephalic eversion. This new model fits well with the putative homology based on hodology and the organization of telencephalic divisions in the adult brain.

Fiber connections of the lateral valvular nucleus in a percomorph teleost, tilapia (Oreochromis niloticus)

Fiber connections of the lateral valvular nucleus were investigated in a percomorph teleost, the tilapia (Oreochromis niloticus), by tract‐tracing methods. Following tracer injections into the lateral valvular nucleus, neurons were labeled in the ipsilateral dorsal part of dorsal telencephalic area, corpus glomerulosum pars anterior, dorsomedial thalamic nucleus, central nucleus of the inferior lobe, mammillary body, semicircular torus, valvular and cerebellar corpus, in the bilateral rostral regions of the central part of dorsal telencephalic area, dorsal region of the medial part of dorsal telencephalic area, habenula, anterior tuberal nucleus, posterior tuberal nucleus, and spinal cord, and in the contralateral lateral funicular nucleus. Labeled fibers and terminals were found in the ipsilateral cerebellar corpus and bilateral valvula of the cerebellum. Tracers were injected into portions of the telencephalon, pretectum, inferior lobe, and cerebellum to confirm reciprocally connections with the lateral valvular nucleus and to determine afferent terminal morphology in the lateral valvular nucleus. Telencephalic fibers terminated mainly in a dorsolateral portion of the lateral valvular nucleus. Terminals from the corpus glomerulosum pars anterior, central nucleus of the inferior lobe, and mammillary body showed more diffuse distributions and were not confined to particular portions of the lateral valvular nucleus. Labeled terminals in the lateral valvular nucleus were cup‐shaped or of beaded morphology. These results indicate that the lateral valvular nucleus receives projections from various sources including the telencephalon, pretectum, and inferior lobe to relay information to the valvular and cerebellar corpus. In addition, the corpus glomerulosum pars anterior in tilapia is considered to be homologous to the magnocellular part of superficial pretectal nucleus in cyprinids. J. Comp. Neurol. 474:209–226, 2004.

Fiber Connections of the Nucleus isthmi in the Carp (Cyprinus carpio) and Tilapia (Oreochromis niloticus)

The nucleus pretectalis (NP) is a prominent nucleus in the percomorph pretectum and has been shown to project to the nucleus isthmi in the filefish by an HRP tract-tracing method [Ito et al., 1981], but a homologous nucleus to the NP is apparently lacking in ostariophysans. The present study examined fiber connections of the nucleus isthmi in an ostariophysan teleost, the carp (Cyprinidae, Cyprinus carpio), to identify a nucleus homologous to the percomorph nucleus pretectalis. Identical studies in a percomorph tilapia (Cichlidae, Oreochromis niloticus) were also performed. Injections of biotinylated dextran amine (BDA) or biocytin to the carp nucleus isthmi labeled cells in the ipsilateral optic tectum and nucleus ruber of Goldstein [1905]. Labeled tectal neurons were located in the stratum periventriculare (SPV) and the stratum fibrosum et griseum superficiale (SFGS). The somata in the SPV were pyriform and those in the SFGS were fusiform. No labeled cells were found in the pretectum. Labeled terminals were seen in the ipsilateral nucleus pretectalis superficialis pars parvocellularis (PSp), optic tectum, and bilateral nucleus ruber. Terminals in the nucleus ruber appear to come from tectal neurons in the SFGS labeled by isthmic injections. Thus the nucleus isthmi has reciprocal fiber connections with the ipsilateral optic tectum, receives projections from the ipsilateral nucleus ruber, and projects to the ipsilateral PSp. The nucleus pretectalis homologue is apparently absent in the carp. Studies in tilapia showed that the nucleus isthmi receives bilateral projections from the NP and optic tectum. In addition, the present study revealed a previously unknown afferent from the nucleus ruber to the percomorph nucleus isthmi. The tilapia nucleus isthmi projects to the same targets as in the carp. Isthmic projection neurons in the tilapia optic tectum were located in the SPV and pyriform with a similar shape to the carp SPV neurons that project to the nucleus isthmi. No labeled cells were found in the SFGS of tilapia optic tectum. The fusiform neurons in the SFGS of the carp optic tectum possess various hodological similarities with the NP and may correspond to the NP neurons of percomorphs.

Topographical organization of an indirect telencephalo-cerebellar pathway through the nucleus paracommissuralis in a teleost, Oreochromis niloticus.

The nucleus paracommissuralis (NPC) of teleosts is a relay nucleus of an indirect telencephalo-cerebellar pathway. However, cells of origin in telencephalic subdivisions and terminal patterns of the NPC fibers in the cerebellum remain unclear. We studied these issues by means of tract-tracing methods in a cichlid, tilapia (Oreochromis niloticus). After tracer injections into the NPC, retrogradely labeled cells were found bilaterally in dorsal and ventral regions of the area dorsalis telencephali pars centralis (dDc and vDc) and area dorsalis telencephali pars dorsalis (Dd). Anterogradely labeled terminals were found in a caudal part of the bilateral corpus cerebelli (CC). The labeled terminals were restricted in the granular layer, which can be divided into dorsal and ventral regions based on cytoarchitecture. We injected tracers separately into the three telencephalic portions (dDc, vDc, and Dd) and into the dorsal or ventral regions of granular layer in the caudal CC. The results revealed a topographical organization of the indirect telencephalo-cerebellar pathway. A medial portion of the NPC received fibers from the vDc and projected to the ventral region of the caudal CC. An intermediate portion of the NPC received fibers from the dDc and Dd, and in turn projected to the dorsal region of the caudal CC. A lateral portion of the NPC received fibers from the Dd and in turn projected to the dorsal region of the caudal CC. The Dc is known to receive visual input via the area dorsalis telencephali pars lateralis, and the Dd is presumably a multimodal telencephalic portion. The present study suggests that the indirect telencephalo-cerebellar pathway through the NPC might convey descending visual and multimodal information to the CC in a topographical manner. We also demonstrated other indirect telencephalo-cerebellar pathways through the nucleus lateralis valvulae and the area pretectalis.

Fiber connections of the torus longitudinalis and optic tectum in holocentrid teleosts

Fiber connections of the torus longitudinalis (TL) and target(s) of toral recipient tectal neurons (pyramidal cells) in the optic tectum were examined by tract‐tracing methods in holocentrids. Injections into the stratum marginale (SM) labeled neurons in the stratum opticum and stratum fibrosum et griseum superficiale (SFGS). They had superficial spiny dendrites, with a fan‐shaped branching pattern in SM and a thick basal dendrite that gave rise to bushy horizontal branches at the boundary between the SFGS and the stratum griseum centrale (SGC), where an axon and a thin dendrite arose. The axon terminated in a middle cellular layer of the SGC, and the thin dendrite ramified slightly deeper to this cellular layer. The SM injections also labeled cells in the ipsilateral TL. Injections into either the lateral or the medial part of TL labeled terminals in the ipsilateral SM and neurons in the bilateral nucleus paracommissuralis (NPC) and nucleus subvalvularis and ipsilateral nucleus subeminentialis. Only medial TL injections labeled cells in the ipsilateral SGC. These neurons had a basal dendrite that branched in the middle cellular layer of SGC, suggesting that they receive inputs from the pyramidal cells and project back to the TL to form a closed circuit. Only lateral TL injections labeled terminals in the corpus cerebelli. A visual telencephalic portion projects to the NPC and sublayers of SGC, where dendrites of the pyramidal cells and SGC neurons ramify. The present results therefore suggest that the TL and SM are components of an intricate circuitry that exerts telencephalic descending visual influence on the optic tectum and corpus cerebelli. J. Comp. Neurol. 462:194–212, 2003.

Somatotopic Organization of the Trigeminal Ganglion Cells in a Cichlid Fish, Oreochromis (Tilapia) niloticus

Somatotopic organization of the trigeminal ganglion is known in some vertebrates. The precise pattern of somatotopy, however, seems to vary in different vertebrate groups. Furthermore, the somatotopic organization remains to be studied in teleosts. From an evolutionary point of view, the morphology and somatotopic organization of the trigeminal ganglion of a percomorph teleost, Tilapia, were investigated by means of the tract-tracing method using biocytin and three-dimensional reconstruction models with a computer. The trigeminal ganglion was one cell aggregate elongated in the dorsoventral direction, which was separate from the facial and anterior lateral line ganglia. Biocytin applications to the trigeminal nerve root labeled ordinary ganglion cells in the trigeminal ganglion and a few displaced trigeminal ganglion cells in the facial ganglion. Biocytin applications to three primary branches (the ophthalmic, maxillary, and mandibular nerves) revealed that trigeminal ganglion cells were somatotopically distributed in the ganglion reflecting the dorsoventral order of the three branches. Ganglion cells of the ophthalmic nerve were distributed in the dorsal part of the trigeminal ganglion, those of the mandibular nerve in the ventral part, and those of the maxillary nerve in the intermediate part. Some of maxillary and mandibular ganglion cells appear to overlap in their boundary region, whereas ophthalmic ganglion cells did not intermingle with ganglion cells of other branches. Labeled-primary fibers terminated in the sensory trigeminal nucleus, descending trigeminal nucleus, medial funicular nucleus, a ventral part of the facial lobe, reticular formation, and trigeminal motor nucleus. Labeled cells were observed in the mesencephalic trigeminal nucleus and the trigeminal motor nucleus. The results suggest that the morphology and somatotopic organization of the trigeminal ganglion of tilapia are similar to those of mammals, except that the axis of the somatotopic organization of the ganglion in mammals is a mediolateral direction reflecting the mediolateral order of the ophthalmic, maxillary, and mandibular nerves.

Projections of the sensory trigeminal nucleus in a percomorph teleost, tilapia (Oreochromis niloticus)

The sensory trigeminal nucleus of teleosts is the rostralmost nucleus among the trigeminal sensory nuclear group in the rhombencephalon. The sensory trigeminal nucleus is known to receive the somatosensory afferents of the ophthalmic, maxillar, and mandibular nerves. However, the central connections of the sensory trigeminal nucleus remain unclear. Efferents of the sensory trigeminal nucleus were examined by means of tract‐tracing methods, in a percomorph teleost, tilapia. After tracer injections to the sensory trigeminal nucleus, labeled terminals were seen bilaterally in the ventromedial thalamic nucleus, periventricular pretectal nucleus, medial part of preglomerular nucleus, stratum album centrale of the optic tectum, ventrolateral nucleus of the semicircular torus, lateral valvular nucleus, prethalamic nucleus, tegmentoterminal nucleus, and superior and inferior reticular formation, with preference for the contralateral side. Labeled terminals were also found bilaterally in the oculomotor nucleus, trochlear nucleus, trigeminal motor nucleus, facial motor nucleus, facial lobe, descending trigeminal nucleus, medial funicular nucleus, and contralateral sensory trigeminal nucleus and inferior olive. Labeled terminals in the oculomotor nucleus and trochlear nucleus showed similar densities on both sides of the brain. However, labelings in the trigeminal motor nucleus, facial motor nucleus, facial lobe, descending trigeminal nucleus, and medial funicular nucleus showed a clear ipsilateral dominance. Reciprocal tracer injection experiments to the ventromedial thalamic nucleus, optic tectum, and semicircular torus resulted in labeled cell bodies in the sensory trigeminal nucleus, with a few also in the descending trigeminal nucleus. J. Comp. Neurol. 495:279–298, 2006.

Afferent sources to the inferior olive and distribution of the olivocerebellar climbing fibers in cyprinids

The inferior olive in teleosts is a major afferent origin to the cerebellum. However, inputs to the inferior olive remain largely unknown. The present study examined fiber connections of the inferior olive by tract‐tracing methods in cyprinids. After tracer injections into the inferior olive, labeled somata were observed bilaterally in the pretectum, nucleus ruber, principal sensory trigeminal nucleus, descending trigeminal nucleus, inferior reticular formation, and cerebellar valvula. Principal sensory trigeminal and valvular afferents exhibited a clear contralateral preponderance, while afferents from the nucleus ruber were predominantly ipsilateral. Labeled somata were also seen ipsilaterally in the descending octaval nucleus, and contralaterally in the optic tectum, lateral funicular nucleus, cerebellar corpus, and inferior olive. A few somata were labeled in the inferior raphe. Climbing fibers terminated contralaterally in the ganglionic and molecular layers of the cerebellum, showing peculiar glomerular appearances. Labeled climbing fiber terminals were mainly distributed in the ventral region of cerebellar corpus, the medioventral region of lateral lobe of rostral cerebellar valvula, and the lateroventral region of medial lobe of cerebellar valvula in the present injection materials. Fiber connections of the inferior olive in teleosts thus appear quite similar to those in mammals. J. Comp. Neurol. 507:1409–1427, 2008.

Afferent Connections of the Corpus cerebelli in Holocentrid Teleosts

The holocentrid corpus cerebelli (CC) is composed of the dorsal (CCd) and ventral (CCv) lobes. In the present study, afferent connections of the CCd and CCv in holocentrid teleosts (Sargocentron rubrum and S. diadema) were examined by means of tract-tracing methods. Tracer injections into either lobe of the CC labeled neurons in the ipsilateral area pretectalis pars anterior et posterior, nucleus paracommissuralis (NPC), nucleus accessorius opticus and nucleus tegmentocerebellaris. Labeled neurons were also present in the bilateral nucleus lateralis valvulae (NLV), nucleus raphes, nucleus reticularis lateralis and inferior reticular formation, and in the contralateral inferior olive. Injections into the CCd labeled only a few neurons in the area pretectalis pars anterior et posterior, nucleus accessorius opticus and nucleus tegmentocerebellaris, whereas many labeled cells were seen in these nuclei after CCv injections. Injections into the CCv also revealed afferent connections that were not observed after CCd injections. The CCv injections labeled additional neurons in the ipsilateral torus longitudinalis and nucleus subeminentialis and in the bilateral nucleus subvalvularis and nucleus of the commissure of Wallenberg. These differences in afferent connections suggest functional differences between the CCd and CCv. After injections into the CCd, labeled neurons in the NPC were restricted to a medial portion of the nucleus. On the other hand, after injections into the CCv, labeled neurons were found throughout the NPC. Labeled neurons in the NLV were mainly located in its rostral portion following CCd injections, whereas labeled neurons were mainly distributed in the medial portion following CCv injections. These observations suggest topographical organizations of the NPC-CC and NLV-CC projections.

Fiber connections of the torus longitudinalis in a teleost: Cyprinus carpio re‐examined

Fiber connections of the carp torus longitudinalis were re‐examined by means of tract‐tracing methods. The torus longitudinalis projected mainly to the stratum marginale of the optic tectum, area pretectalis, and corpus cerebelli. The stratum marginale was anterogradely labeled only by biocytin, but not by horseradish peroxidase. Because the stratum is composed of extremely fine axons of the small toral neurons, this may be ascribed to different molecular weights of the tracers. The main afferent sources to the torus longitudinalis were the nucleus subvalvularis, which was located beneath the nucleus lateralis valvulae, the nucleus subeminentialis pars magnocellularis, and neurons along the posterior mesencephalo‐cerebellar tract. Some labeled cells also appeared in the area pretectalis, nucleus paracommissuralis, optic tectum, and torus semicircularis. In a previous paper, it was incorrectly reported that the valvula cerebelli was the main source of afferents to the torus longitudinalis. Here we report the reason for the previous mistake in relation to the techniques employed. J. Comp. Neurol. 457:202–211, 2003.