Effects of acute and chronic stress on telencephalic neurochemistry and gene expression in rainbow trout (Oncorhynchus mykiss)

Abstract

By filtering relevant sensory inputs and initiating stress responses, the brain is an essential organ in stress coping and adaptation. However, exposure to chronic or repeated stress can lead to allostatic overload, where neuroendocrinal and behavioral reactions to stress become maladaptive. This work examines forebrain mechanisms involved in allostatic processes in teleost fishes. Plasma cortisol, forebrain serotonergic (5-HTergic) neurochemistry, and mRNA levels of corticotropin-releasing factor (CRF), CRF-binding protein (CRF-BP), CRF receptors (CRFR1 and CRFR2), mineralocorticoid receptor (MR), glucocorticoid receptors (GR1 and GR2) and serotonin type 1A (5-HT 1A ) receptors (5-HT 1Aα and 5-HT 1Aβ ) were investigated at 1 h before and 0, 1 and 4 h after acute stress, in two groups of rainbow trout held in densities of 25 and 140 kg m −3 for 28 days. Generally, being held at 140 kg m −3 resulted in a less pronounced cortisol response. This effect was also reflected in lower forebrain 5-HTergic turnover, but not in mRNA levels in any of the investigated genes. This lends further support to reports that allostatic load causes fish to be incapable of mounting a proper cortisol response to an acute stressor, and suggests that changes in forebrain 5-HT metabolism are involved in allostatic processes in fish. Independent of rearing densities, mRNA levels of 5-HT 1Aα and MR were downregulated 4 h post-stress compared with values 1 h post-stress, suggesting that these receptors are under feedback control and take part in the downregulation of the hypothalamic-pituitary-interrenal (HPI) axis after exposure to an acute stressor.

Regulation of the corticosteroid signalling system in rainbow trout HPI axis during confinement stress

“…However, in our study, we did not observe any significant change in the three receptors mRNA levels during short term (hours) and long term (up to 7 days) exposure to confinement. For acute stress exposure, these data obtained in the hypothalamus are in accordance with previous studies showing that acute stressors did not change GR1 expression levels in rainbow trout preoptic area (POA) (Alderman et al, 2012) or GR1 and GR2 expression in trout telencephalon (Moltesen et al, 2016). In carp, a 24h restraint stress did not modify significantly MR, GR1 and GR2 mRNA levels in the hypothalamus (Stolte et al, 2008a).…”

“…In carp, a 24h restraint stress did not modify significantly MR, GR1 and GR2 mRNA levels in the hypothalamus (Stolte et al, 2008a). However, in rainbow trout, a down regulation of MR after acute stress in the telencephalon but not in the hypothalamus was reported by Johansen et al (2011) and a significant effect of acute stress on MR expression was observed in the trout telencephalon (Moltesen et al, 2016). Effects of chronic stress exposure has also been studied and, generally, these studies suggest also significant effects on receptors expression in the brain in association with changes in HPI axis reactivity: Thus, exposure of Atlantic salmon to unpredictable chronic stress resulted in a decreased expression of GR1, GR2 in the POA (Madaro et al, 2015) but repeated chasing stress had different effects on GR1 and GR2 expression in the POA whether experiments are done on parr or postsmolts (Madaro et al, 2016).…”

“…An important feature of cortisol as a stress hormone is its negative feedback control on HPI axis activity at the levels of hypothalamus, pituitary and interrenal gland. Generally, a down-regulation of the HPI axis reactivity is observed during chronic stress in fish (Barton, 2002, Barton et al, 2005, Madaro et al, 2015, Moltesen et al, 2016. However, the role of corticosteroid receptors in this feedback regulation of HPI axis still needs to be clarified.…”

Confirmation that pulse and continuous peracetic acid administration does not disrupt the acute stress response in rainbow trout

“…The serotonergic system is believed to participate at a high hierarchical level in the organization of the neuroendocrine response to stress in vertebrates (Winberg and Nilsson, 1993;Gesto et al, 2013;Lanfumey et al, 2008). The chasing stress challenge induced a transient increase in telencephalic serotonergic activity (Table 2), similar to previous studies in rainbow trout exposed to acute stress (Gesto et al, 2013;Moltesen et al, 2016). Although this transient increase was only significant in the Control treatment group, the dynamics and the magnitude of the response were similar among treatment groups (Table 1) which supports an equal stress response for all fish in the experiment.…”

“…A reduction in the cortisol response to stress stimuli could, however, be due to different reasons and does not necessarily reflect a process of habituation. For example, the physiological stress responses can become desensitized or exhausted after repeated or chronic exposure to stress (Cyr and Romero, 2009;McKenzie et al, 2012;Barton et al, 2005;Madaro et al, 2015;Moltesen et al, 2016), even when the animals have not habituated to the stressor. Furthermore, different aquatic pollutants are capable of disrupting the normal function of the neuroendocrine pathways involved in the vertebrate stress response, altering the normal synthesis and release of stress hormones such as catecholamines and corticosteroids (Gesto et al, 2008;Ings et al, 2012;Hontela et al, 1997).…”