Peri-pubertal exposure to testicular hormones organizes response to novel environments and social behaviour in adult male rats

Abstract

Previous research has shown that exposure to testicular hormones during the peri-pubertal period of life has long-term, organizational effects on adult sexual behaviour and underlying neural mechanisms in laboratory rodents. However, the organizational effects of peri-pubertal testicular hormones on other aspects of behaviour and brain function are less well understood. Here, we investigated the effects of manipulating peri-pubertal testicular hormone exposure on later behavioural responses to novel environments and on hormone receptors in various brain regions that are involved in response to novelty. Male rodents generally spend less time in the exposed areas of novel environments than females, and this sex difference emerges during the peri-pubertal period. Male Lister-hooded rats (Rattus norvegicus) were castrated either before puberty or after puberty, then tested in three novel environments (elevated plus-maze, light–dark box, open field) and in an object/social novelty task in adulthood. Androgen receptor (AR), oestrogen receptor (ER1) and corticotropin-releasing factor receptor (CRF-R2) mRNA expression were quantified in the hypothalamus, hippocampus and medial amygdala. The results showed that pre-pubertally castrated males spent more time in the exposed areas of the elevated-plus maze and light–dark box than post-pubertally castrated males, and also confirmed that peri-pubertal hormone exposure influences later response to an opposite-sex conspecific. Hormone receptor gene expression levels did not differ between pre-pubertally and post-pubertally castrated males in any of the brain regions examined. This study therefore demonstrates that testicular hormone exposure during the peri-pubertal period masculinizes later response to novel environments, although the neural mechanisms remain to be fully elucidated.

Social experience during adolescence in female rats increases 50 kHz ultrasonic vocalizations in adulthood, without affecting anxiety‐like behavior

“…Although SE subjects spent the highest average amount of time in contact with this barrier, the difference between groups of females was not significant. For all groups, the absolute amount of time spent next to the barrier with the male was very similar to a previous study using the same apparatus in which the position of the two sexes was reversed (Brown, Kulbarsh, Spencer, & Duval, ), suggesting that female rats are as motivated as males to investigate an opposite‐sex conspecific in this task. Previous studies have shown that adult female and male rats that have been group‐housed during adolescence engage in more social exploration with same‐ and opposite‐sex rats than do rats that have been pair housed or single housed during this stage of life (e.g., Brenes et al, ; Molenda‐Figueira, Bell, Lorme, & Sisk, ; Peña et al, ), while male rats exposed to adolescent social instability exhibit impaired social interactions with same‐sex and opposite‐sex peers in adulthood (Green et al, ; McCormick et al, ; Ward & Reed, ).…”

On the Role of Testosterone in Anxiety-Like Behavior Across Life in Experimental Rodents

“…In rats, male gonadectomy, either at puberty onset or shortly thereafter, results in lower anxiety in the open area, the behavioral response typical for females ( 29 ). Similar effects of pre-pubertal castration were found in the elevated plus maze and light-dark box, where adult male rats that had been gonadectomized prior to puberty exhibit a higher frequency of head-dipping and more time spent in the open arms or in the light part of the light-dark box ( 33 ). Environment-related social anxiety in males is organized also by pubertal sex hormones, where the aromatization of testosterone seems to be critical ( 49 ).…”

“…In time spent in the bright chamber of the light-dark box, contradictory results have been found. In some experiments, females show higher anxiety than males ( 32 ), in other experiments, the opposite sex difference was proved ( 33 ), while the lack of sex differences is published rarely ( 27 ). It should be noted that sex differences in experimental animals in anxiety-like behavior might depend on many factors, such as strain ( 34 ) or breeding condition ( 32 ), and other sources of inter-individual variability are likely not identified yet ( 35 ).…”

The organizing actions of adolescent gonadal steroid hormones on brain and behavioral development

“…More recent work has examined how the presence or absence of testosterone during puberty influences the behavior of male rats in other tests of anxiety. These studies show that compared with male rats GDX in adulthood, prepubertally GDX male rats spend more time in the open arms of an elevated plus maze and more time in the light section of a light-dark box, indicating in both cases that prepubertal GDX results in a less anxious phenotype in adulthood (Brown, Kulbarsh, Spencer, & Duval, 2015). Together, these studies support the idea that the presence of testicular hormones during adolescence organizes anxiety-like behaviors in male rats, specifically making them more anxious after adolescence than before.…”