The development of the serotonergic and dopaminergic systems during chicken mid-late embryogenesis

Xiaohong Huang; Shihuan Kuang; Todd J Applegate; Tsang-Long Lin; Heng-Wei Cheng

doi:10.1016/j.mce.2019.110472

The development of the serotonergic and dopaminergic systems during chicken mid-late embryogenesis

Mol Cell Endocrinol. 2019 Aug 1:493:110472. doi: 10.1016/j.mce.2019.110472. Epub 2019 Jun 2.

Authors

Xiaohong Huang¹, Shihuan Kuang¹, Todd J Applegate², Tsang-Long Lin³, Heng-Wei Cheng⁴

Affiliations

¹ Department of Animal Sciences, Purdue University, West Lafayette, IN, 47907, USA.
² Department of Poultry Science, University of Georgia, Athens, 30602, Georgia.
³ Animal Disease Diagnostic Lab, Purdue University, West Lafayette, IN, 47907, USA.
⁴ Livestock Behavior Research Unit, USDA-ARS, West Lafayette, IN, 47907, USA. Electronic address: hwcheng@purdue.edu.

PMID: 31167113
DOI: 10.1016/j.mce.2019.110472

Abstract

Serotonin (5-HT) acts as a morphogen influencing embryonic brain development, and as a neurotransmitter regulating multiple biological functions with lifelong effects on animal physical, physiological and mental health, especially during the rapid growth phase prior to birth when embryos face many challenges to reach structural and functional completion. In this study, the development of the serotoninergic (5-HTergic) system and its modulatory effect on the dopaminergic (DAergic) system and related neural circuits were investigated during the mid-late embryogenesis, embryonic day (E)12-E20, in the chicken's brain. During 5-HTergic neuronal maturation, a growth-related anatomical and functional remodeling was highlighted: the 5-HT neurons continuously grew during E12-E20 except for a remarkable regression during E14-E16. Correspondingly, there was a time-dependent change in the 5-HT synthetic capacity. Specifically, 5-HT concentrations in the raphe nuclei increased from E12 to E14, reaching a first plateau during E14-E16, then continuously increased up to E19, and reaching a second plateau between E19-E20. The second plateau of the 5-HT concentration was in correspondence with the establishment of the 5-HTergic autoregulatory loop during E19-E20 and the development of the DAergic system. The DA concentrations remained unchanged from E12 to E16, then started to increase at E16, reaching a maximum at E19, and diminished before hatching. The unique developing time sequence between the 5-HTergic and DAergic systems suggests that the 5-HTergic system may play a critical role in forming the 5-HT - DA neural circuit during chicken embryogenesis. These results provide new insights for understanding the functional organization of the 5-HTergic system during embryonic development and raise the possibility that prenatally modulating the 5-HTergic system may lead to long-lasting brain structural and functional alterations.

Keywords: Chicken; Dopamine; Embryonic brain development; Neuronal maturation; Serotonin.

Published by Elsevier B.V.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Brain / embryology*
Brain / metabolism
Chickens
Chromatography, High Pressure Liquid
Dopamine / metabolism*
Embryonic Development
Gene Expression Regulation, Developmental
Receptor, Serotonin, 5-HT1A / genetics
Receptor, Serotonin, 5-HT1A / metabolism
Serotonin / metabolism*
Serotonin Plasma Membrane Transport Proteins / genetics
Serotonin Plasma Membrane Transport Proteins / metabolism
Tryptophan Hydroxylase / genetics
Tryptophan Hydroxylase / metabolism

Substances

HTR1A protein, human
Serotonin Plasma Membrane Transport Proteins
Receptor, Serotonin, 5-HT1A
Serotonin
Tryptophan Hydroxylase
Dopamine