Reconstructing the ancestral vertebrate brain

Abstract

Highly complicated morphologies and sophisticated functions of vertebrate brains have been established through evolution. However, the origin and early evolutionary history of the brain remain elusive, owing to lack of information regarding the brain architecture of extant and fossil species of jawless vertebrates (agnathans). Comparative analyses of the brain of less studied cyclostomes (only extant agnathan group, consisting of lampreys and hagfish) with the well-known sister group of jawed vertebrates (gnathostomes) are the only tools we have available to illustrate the ancestral architecture of the vertebrate brain. Previous developmental studies had shown that the lamprey lacked well-established brain compartments that are present in gnathostomes, such as the medial ganglionic eminence and the rhombic lip. The most accepted scenario suggested that cyclostomes had fewer compartments than that of the gnathostome brain and that gnathostomes thus evolved by a stepwise addition of innovations on its developmental sequence. However, recent studies have revealed that these compartments are present in hagfish embryos, indicating that these brain regions have been acquired before the split of cyclostomes and gnathostomes. By comparing two cyclostome lineages and gnathostomes, it has become possible to speculate about a more complex ancestral state of the brain, excluding derived traits in either of the lineages. In this review, we summarize recent studies on the brain development of the lamprey and hagfish. Then, we attempt to reconstruct the possible brain architecture of the last common ancestor of vertebrates. Finally, we discuss how the developmental plan of the vertebrate brain has been modified independently in different vertebrate lineages.

Patterning of a telencephalon-like region in the adult brain of amphioxus

“…This telencephalic domain is subdivided into sub-regions of distinct molecular identity. Our results suggest a new evolutionary scenario where late activation of Hh in amphioxus induces the formation of a broad FoxG1 domain (telencephalon) that further sub-divides into a dorsal domain expressing Emx-Lhx2/9-Pax4/6 , a ventral domain expressing Hh and an intermediate Hh-Nkx2.1 -positive domain, with the latter possibly representing a primitive MGE, which evolutionary origins were also controversial (Sugahara et al, 2017).…”

Dual midbrain and forebrain origins of thalamic inhibitory interneurons

“…transcription factors), are common to the amniote lineages (Métin et al, 2007; Tasic et al, 2018; Tosches et al, 2018; Arendt et al, 2019). Moreover, a conserved subpallial origin was demonstrated for cortical interneurons in the cyclostome hagfish, and therefore appears to be an ancestral feature of the vertebrate brain (Sugahara et al, 2016, 2017).…”

Multipotent radial glia progenitors and fate-restricted intermediate progenitors sequentially generate diverse cortical interneuron types

“…The basic organization of the subpallium, including the LGE, MGE and POA, may have its evolutionary origins in early vertebrates (Medina et al, 2014;Sugahara et al, 2017;Sugahara et al, 2016). Single cell transcriptome analyses in reptiles reveal that the number and diversity of pallial GABAergic interneurons are limited in reptiles compare to mammals (Tosches et al, 2018).…”