Gene expression in the amygdala and hippocampus of cyclic and acyclic gilts

Authors: WIJESENA, HIRUNI - Orise Fellow; Nonneman, Danny - Dan; Keel, Brittney; Lents, Clay

Submitted to: Journal of Animal Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/4/2021
Publication Date: 1/4/2022
Citation: Wijesena, H.R., Nonneman, D.J., Keel, B.N., Lents, C.A. 2022. Gene expression in the amygdala and hippocampus of cyclic and acyclic gilts. Journal of Animal Science. Article skab372. https://doi.org/10.1093/jas/skab372.
DOI: https://doi.org/10.1093/jas/skab372

Interpretive Summary: Approximately 12% of gilts selected for entry into the swine breeding herd fail to produce a litter because they do not to display sexual behavior necessary for breeding when exposed to boars; a condition called prebreeding anestrus. To better understand how to solve this problem, ARS scientists at Clay Center, Nebraska, studied how genes in the hippocampus and the amygdala, two regions of the brain involved in sexual behavior, differed in gilts with prebreeding anestrus compared to control gilts with estrus. Both tissues showed high plasticity to gonadal hormones and dynamic changes in gene expression at different stages of the estrous cycle. Several of the genes expressed differently between anestrus gilts and control gilts regulate gamma-aminobutyric acid, a major inhibitory neurotransmitter. This is the study to identify genes in the hippocampus and amygdala of the pig brain of gilts with prebreeding anestrus and results will be important for identifying new methods to solve this problem.

Technical Abstract: Age at first estrus is the earliest phenotypic indicator of future reproductive success of gilts. Prebreeding anestrus is a major reason for reproductive failure leading to culling of replacement gilts. The two types of prebreeding anestrus are delay in attaining puberty (prepubertal anestrus, PPA) and silent ovulation (behavioral anestrus, BA). Neural tissues such as amygdala and hippocampus play a major role in regulating sexual behavior, social interactions, and receptivity to males. Differences in gene expression in the amygdala and hippocampus of gilts were analyzed in three comparisons; 1) PPA cases and cyclic controls at follicular phase of estrous cycle, 2) BA cases and cyclic controls at luteal phase of estrous cycle, and 3) gilts at different stages of the ovarian cycle (cyclic gilts at follicular phase and luteal phase of estrous cycle) to gain functional understanding of how these rarely studied tissues may differ between pubertal phenotypes and different stages of the estrous cycle of gilts. Differentially expressed genes (DEG) between PPA and BA cases and their respective cyclic controls were involved in neurological and behavioral disorders as well as nervous system functions that could directly or indirectly involved in development of behaviors related to estrus. The comparison between cyclic follicular and luteal phase control gilts identified the greatest number of DEG in the hippocampus and amygdala. These DEG were involved in adult neurogenesis and neural synapse (e.g., GABAergic, dopamine, cholinergic) suggesting that these tissues undergo structural changes and synaptic plasticity in gilts. This is the first report to demonstrate that the stage of estrous cycle is associated with dynamic changes in gene expression within porcine hippocampus and amygdala and indicates a role of gonadal steroids in regulating their biology.