The dorsoanterior brain of adult amphioxus shares similarities in expression profile and neuronal composition with the vertebrate telencephalon

Èlia Benito-Gutiérrez,Gáspár Jékely,Jocelyn Tang,Detlev Arendt,Aleksandra Marconi,Manuel Stemmer,Giacomo Gattoni,Laura N Schuhmacher,Silvia D Rohr

doi:10.1186/s12915-021-01045-w

Abstract

BackgroundThe evolutionary origin of the telencephalon, the most anterior part of the vertebrate brain, remains obscure. Since no obvious counterpart to the telencephalon has yet been identified in invertebrate chordates, it is difficult to trace telencephalic origins. One way to identify homologous brain parts between distantly related animal groups is to focus on the combinatorial expression of conserved regionalisation genes that specify brain regions.ResultsHere, we report the combined expression of conserved transcription factors known to specify the telencephalon in the vertebrates in the chordate amphioxus. Focusing on adult specimens, we detect specific co-expression of these factors in the dorsal part of the anterior brain vesicle, which we refer to as Pars anterodorsalis (PAD). As in vertebrates, expression of the transcription factors FoxG1, Emx and Lhx2/9 overlaps that of Pax4/6 dorsally and of Nkx2.1 ventrally, where we also detect expression of the Hedgehog ligand. This specific pattern of co-expression is not observed prior to metamorphosis. Similar to the vertebrate telencephalon, the amphioxus PAD is characterised by the presence of GABAergic neurons and dorsal accumulations of glutamatergic as well as dopaminergic neurons. We also observe sustained proliferation of neuronal progenitors at the ventricular zone of the amphioxus brain vesicle, as observed in the vertebrate brain.ConclusionsOur findings suggest that the PAD in the adult amphioxus brain vesicle and the vertebrate telencephalon evolved from the same brain precursor region in ancestral chordates, which would imply homology of these structures. Our comparative data also indicate that this ancestral brain already contained GABA-, glutamatergic and dopaminergic neurons, as is characteristic for the olfactory bulb of the vertebrate telencephalon. We further speculate that the telencephalon might have evolved in vertebrates via a heterochronic shift in developmental timing.

Highlights

The evolutionary origin of the telencephalon, the most anterior part of the vertebrate brain, remains obscure
Transcription factors involved in telencephalon development are expressed in the adult amphioxus brain Taking advantage of our pipeline, we investigated the expression of FoxG1, Emx, Lhx2, Fezf, Nkx2.1 and Pax4/6 transcription factors in the amphioxus postmetamorphic cerebral vesicle
We focused on the occurrence of key transmitters in terminally differentiated neurons, such as GABA, glutamate and acetylcholine, which we spatially related to a restricted population of dorsal dopaminergic neurons [58]

Summary

Introduction

The evolutionary origin of the telencephalon, the most anterior part of the vertebrate brain, remains obscure. The combined regional co-expression of foxg and emx conveys the initial specification of the telencephalic brain region [4, 5]; Lhx is required for the formation of cortical progenitors [6]; and Pax and Nkx2.1 subdivide the telencephalon into the dorsal pallial and ventral subpallial domain in mouse, zebrafish and lamprey [4, 7]. While the pallial domain gives rise to glutamatergic neurons, the subpallial domain gives rise to GABAergic neurons, of which some migrate dorsally into the pallium. The mature pallium comprises the cerebral cortex with glutamatergic and GABAergic neurons and the olfactory bulb with glutamatergic, GABA- and dopaminergic neurons. The ventral subpallium in turn comprises GABAergic neuron types constituting most of the basal ganglia [8]

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