Int. J. Dev. Biol. 61: 749 - 761 (2017)

https://doi.org/10.1387/ijdb.170153sc

Vol 61, Issue 10-11-12

Special Issue: The Amphioxus Model System

The origin of dopaminergic systems in chordate brains: insights from amphioxus

Published: 20 December 2017

Elisabeth Zieger¹, Thurston C. Lacalli*^,2, Mario Pestarino³, Michael Schubert¹ and Simona Candiani*^,3

¹Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Observatoire Océanologique de Villefranche-sur-Mer, Villefranche-sur-Mer, France, ²Biology Department, University of Victoria, Victoria, BC, Canada and ³Laboratory of Developmental Neurobiology, DISTAV, University of Genova, Genova, Italy

Abstract

The basic anatomy of the central nervous system (CNS) is well conserved within the vertebrates and differs in significant ways from that of non-vertebrate chordates. Of the latter, amphioxus is of special interest, being the best available stand-in for the basal chordate condition. Immunohistochemical and gene expression studies on the developing CNS of amphioxus embryos and larvae are now sufficiently advanced that we can begin to assign specific neurotransmitter phenotypes to neurons identified by transmission electron microscopy (TEM), and then compare the distribution of cell types to that in vertebrate brains. Here, by monitoring tyrosine hydroxylase (TH) transcripts and protein, along with serial TEM, we identify a population of catecholamine-containing neurons in the anterior nerve cord of amphioxus larvae and describe their pattern of synaptic inputs and outputs. Inputs parallel those to the large paired neurons that control the larval escape response, suggesting that the TH+ system functions as an accessory excitatory and perhaps modulatory pathway in larval locomotion, with the added feature of recruiting an assortment of additional interneurons to the circuitry. The TH+ cells probably contain either L-DOPA or dopamine, and correspond closely with a cell population known from previous work on adult amphioxus to be dopaminergic. This population lies in a CNS domain now thought to comprise a combined vertebrate diencephalon plus mesencephalon, the implication being that dopaminergic nuclei in both of these brain regions could derive from a single dien-mesencephalic population in the last common ancestor of amphioxus and vertebrates.

Keywords

dien-mesencephalon, evolution, serial transmission electron microscopy, tyrosine hydroxylase