An ascending visual pathway to the dorsal telencephalon through the optic tectum and nucleus prethalamicus in the yellowfin goby <i>Acanthogobius flavimanus</i> (Temminck &amp; Schlegel, 1845)

Thomas

et al. 2020

eLife

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Ascending visual projections similar to the mammalian thalamocortical pathway are found in a wide range of vertebrate species, but their homology is debated. To get better insights into their evolutionary origin, we examined the developmental origin of a thalamic-like sensory structure of teleosts, the preglomerular complex (PG), focusing on the visual projection neurons. Similarly to the tectofugal thalamic nuclei in amniotes, the lateral nucleus of PG receives tectal information and projects to the pallium. However, our cell lineage study in zebrafish reveals that the majority of PG cells are derived from the midbrain, unlike the amniote thalamus. We also demonstrate that the PG projection neurons develop gradually until late juvenile stages. Our data suggest that teleost PG, as a whole, is not homologous to the amniote thalamus. Thus, the thalamocortical-like projections evolved from a non-forebrain cell population, which indicates a surprising degree of variation in the vertebrate sensory systems.

Section: Discussionmentioning

confidence: 99%

Non-thalamic origin of zebrafish sensory nuclei implies convergent evolution of visual pathways in amniotes and teleosts

Bloch

Thomas

et al. 2020

eLife

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“…The other is called the "tectofugal" or "extra-geniculate" pathway, in which retinal inputs reach the extrastriate visual cortex via two structures, the tectum (superior colliculus in mammals) and another thalamic nucleus (pulvinar in primates and lateral posterior nucleus in other mammals like rodents). Since then, most studies in non-mammals have been interpreted based on this notion of "two visual systems" (Hall and Ebner, 1970;Karten and Hodos, 1970;Riss and Jakway, 1970;Ingle, 1973;Karten et al, 1973;Hagio et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Non-thalamic origin of zebrafish sensory relay nucleus: convergent evolution of visual pathways in amniotes and teleosts

Thomas

Heuzé

et al. 2020

Preprint

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Ascending visual projections similar to the mammalian thalamocortical pathway are found in a wide range of vertebrate species, but their homologous relationship is debated. To get better insights into their evolutionary origin, we examined the developmental origin of a visual relay nucleus in zebrafish (a teleost fish). Similarly to the tectofugal visual thalamic nuclei in amniotes, the lateral part of the preglomerular complex (PG) in teleosts receives tectal information and projects to the pallium.However, our cell lineage study reveals that the majority of PG cells are derived from the midbrain, not from the forebrain. We also demonstrate that the PG projection neurons develop gradually until juvenile stage, unlike the thalamic projection neurons.Our data suggest that teleost PG is not homologous to the amniote thalamus and that thalamocortical-like projections can evolve from a non-forebrain cell population. Thus, sensory pathways in vertebrate brains exhibit a surprising degree of variation.ventral telencephalon containing the striatum; Figure 1; amphibians; Th  SPa), with little projections to the pallium (Kicliter, 1979; Neary and Northcutt, 1983; Wilczynski and Northcutt, 1983; Butler, 1994a).Outside of tetrapods, brain structures are highly divergent compared to amniotes, and thus it is even more complicated to draw an evolutionary scenario. Although teleosts also have sensory afferents to the pallium, the morphology of the teleost pallium is very different from that of tetrapods, as the developmental processes are different (evagination in tetrapods versus eversion in teleosts). Different authors have proposed several hypotheses concerning which part of the teleost pallium would correspond to the mammalian neocortex (Braford, 1995; Wullimann and Mueller, 2004;Northcutt, 2006;Yamamoto et al., 2007; Mueller et al., 2011). Recently, cell lineage studies of the zebrafish pallium have modified the classical view of the eversion model (Dirian et al., 2014;Furlan et al., 2017), and we have proposed a new interpretation on the pallial homology .In teleosts, the controversy is not only on the pallial homology. It has also been debated whether or not the structure giving rise to the major pallial projections is homologous to the tetrapod thalamus (Wullimann and Rink, 2002;Northcutt, 2006;Yamamoto and Ito, 2008; Mueller, 2012). This structure is named the preglomerular complex (PG; Figure 1; teleosts; PG  Pal). In order to determine the evolutionary scenario of sensory pathways in bony vertebrates (Osteichthyes), it is important to investigate whether or not the teleost PG is homologous to the amniote thalamus.As for the controversy on the pallial homology, different authors claim different hypotheses. On the one hand, based on descriptive embryology, the teleost PG has been considered to originate from the basal portion of the diencephalon, the posterior tuberculum (Bergquist, 1932; Braford and Northcutt, 1983; Butler and Hodos, 2005; 6

“…Tectal injections labeled terminals not only in the neuropil of PTh of the ipsilateral side as described above but also in the contralateral nucleus with the ipsilateral component being a bit denser. As described previously (Hagio et al, 2018), fibers terminating in the contralateral PTh crossed the midline through the postoptic commissure.…”

Section: Injection Into the Optic Tectum And Optic Nervementioning

confidence: 92%

“…Tectal injections of the present study indicate that both subnuclei receive tectal projections in the yellowfin goby, unlike the situation in holocentrids. Also, we have reanalyzed our previous telencephalic injection materials (Hagio et al, 2018)…”

Section: Connections Between the Optic Tectum And Pthmentioning

confidence: 99%

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

J of Comparative Neurology

Kawaguchi

Abe

et al. 2020

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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.