Exposure to cold temperatures differentially modulates neural plasticity and stress responses in post-smolt Atlantic salmon (Salmo salar)

The transfer success of farmed post-smolt Atlantic salmon (Salmo salar) to sea-cages rely on neural adaptions to promote stress resilience. As low temperatures impact physiology, this suggests that off-season transfer to cold waters may be challenging. To address this, post-smolts reared at 13 °C seawater were abruptly transferred to 10 °C, 7 °C, and 4 °C, then acclimated to these respective temperatures for 58-days followed by an acute challenge test (ACT) using confinement stress. Plasma and brain samples were collected after i) the abrupt temperature transfer at 1-h and 1-day, ii) 58-days of acclimation, and iii) 1-h post ACT. In tandem to measuring plasma cortisol levels, the expression of key genes involved in telencephalic regulation (crf, crfbp, mr, gr1, gr2 and hsd11b2) and neural plasticity (neurod, bdnf, pcna, and cfos) were analyzed. Post-smolts exposed to the 7 °C and 4 °C displayed the largest alteration in telencephalic functions, differentially regulating mr and gr1, to elevate the mr/g1 ratio for downregulating Gr1, proposing an elevated stress loads. After acclimation, these coincided with blunted stress responses capacities to ACTs for both cortisol and telencephalic neural activity (cfos), suggesting a continuation of challenges and reduced the capacity to mount a stress response. Concomitantly, these telencephalic alterations in CRs coincided with a differential modulation in neural plasticity, measured as elevated bdnf and neurod during the abrupt transfer period (acute) and after acclimation (prolonged), respectively, revealing neural responses are still robustly maintained to retain a degree of stress resilience. However, exposure of post-smolts to 4 °C clearly induced the most adverse and suppressive effects in telencephalic functions, cued by a suppression in pcna and stress response capacities, downregulation in the CRF system, and largest elevation in the mr/g1 ratio. Conversely, acclimating post-smolts to 7 °C elevated 11hsdb2 proposing a greater inhibition of cortisol action that may point to still adequate maintenance of CR and neural processes. Taken together, these findings show that cold temperatures alter key neural processes required for maintaining proper stress management, providing an alternative explanation for reductions in fish stress reactivity commonly observed with declining temperature. Therefore, exposing post-smolts at 13 °C to temperature reductions of 6 °C or greater should be avoided in aquaculture.