Afferent and efferent connections of the nucleus prethalamicus in the yellowfin goby Acanthogobius flavimanus

Abstract

The nucleus prethalamicus (PTh) receives fibers from the optic tectum and then projects to the dorsal telencephalon in the yellowfin goby Acanthogobius flavimanus. However, it remained unclear whether the PTh is a visual relay nucleus, because the optic tectum receives not only visual but also other sensory modalities. Furthermore, precise telencephalic regions receiving prethalamic input remained unknown in the goby. We therefore investigated the full set of afferent and efferent connections of the PTh by direct tracer injections into the nucleus. Injections into the PTh labeled cells in the optic tectum, ventromedial thalamic nucleus, central and medial parts of the dorsal telencephalon, and caudal lobe of the cerebellum. We found that the somata of most tecto-prethalamic neurons are present in the stratum periventriculare. Their dendrites ascend to reach the major retinorecipient layers of the tectum. The PTh is composed of two subnuclei (medial and lateral) and topographic organization was appreciated only for tectal projections to the lateral subnucleus (PTh-l), which also receives sparse retinal projections. In contrast, the medial subnucleus receives fibers only from the medial tectum. We found that the PTh projects to nine subregions in the dorsal telencephalon and four in the ventral telencephalon. Furthermore, cerebellar injections revealed that cerebello-prethalamic fibers cross the midline twice to innervate the PTh-l on both sides. The present study is the first detailed report on the full set of the connections of PTh, which suggests that the PTh relays visual information from the optic tectum to the telencephalon.

The organization of the zebrafish pallium from a hodological perspective

“…A cytoarchitectonically distinct Dc central zone well separated from Dl and rostral pallium was recognized in the telencephalon of various teleosts (Murakami et al, 1983;Harvey-Girard et al, 2012;Elliott et al, 2017). Hodologically, Dc neurons project to the optic tectum in goldfish (Grober & Sharma, 1981) and the goby Acanthogobius flavimanus (Hagio et al, 2018;Hagio et al, 2021), which is similar to that shown in zebrafish. However, in the goby, tectal afferent neurons are located in a central part (Dcm) adjacent to Dm within a large Dc.…”

“…As a result, the connectivity of the pallium in murine species is known in great detail (Oh et al., 2014; Paxinos, 2014; Zingg et al., 2014). In teleosts, tract tracing studies have reported the connections of pallial areas in several species, mostly in goldfish (Northcutt, 2006; Yamamoto & Ito, 2005a, 2005b, 2008), electric fish (Correa & Hoffmann, 1999; Giassi et al., 2012; Giassi et al., 2012; Sas et al., 1993; von der Emde & Prechtl, 1999), rainbow trout (Folgueira et al., 2004a, 2004b), and some acanthopterygians (Hagio, Sato, et al., 2018; Hagio, Kawaguchi, et al., 2021; Murakami et al., 1983). The results of these studies reveal some conserved pallial connections, among them the projections to Dp from the olfactory bulb and to Dl and/or Dm from preglomerular nuclei (Folgueira, Huesa, et al., 2002; Folgueira, Anadón, et al., 2004a, 2004b, 2005; Kato et al., 2012; Northcutt, 2006; Striedter, 1991; Yamamoto & Ito, 2005a, 2008; Yang et al., 2007; Zupanc, 1997).…”

Obituary: Hironobu Ito, M.D., Ph.D. (1939–2020)

“…The pathway is reminiscent of the extrageniculate visual pathway in mammals. The presence of the same pathway was recently confirmed in a goby fish (Hagio, Kawaguchi, Abe, & Yamamoto, 2020;Hagio, Sato, & Yamamoto, 2018). A presumed homologous pathway was also identified in cyprinids (Northcutt, 2006;Yamamoto & Ito, 2008), in which the diencephalic relay nucleus is called the lateral preglomerular nucleus (part of which is visual).…”

The Cytoarchitecture of the Tectal-Related Pallium of Squirrelfish, Holocentrus sp.

“…Two examples of “special” types of Dl need attention as they likely show features that relate to phylogenic and/or ecological diversity. Studies in the yellowfin goby Acanthogobius flavimanus ( Hagio et al, 2018 , 2021 ) demonstrate an exceptional configuration of a Dl with 17 components. Many of the areas receive afferents from the nPTh but two regions Dl16 and Dl17 have an especially strong input from the structure ( Hagio et al, 2021 ).…”

“…Studies in the yellowfin goby Acanthogobius flavimanus ( Hagio et al, 2018 , 2021 ) demonstrate an exceptional configuration of a Dl with 17 components. Many of the areas receive afferents from the nPTh but two regions Dl16 and Dl17 have an especially strong input from the structure ( Hagio et al, 2021 ). Conspicuous vertical columns are not reported in any Dl areas.…”