Neurobiology of Wild and Hatchery-Reared Atlantic Salmon: How Nurture Drives Neuroplasticity

Abstract

Life experiences in the rearing environment shape the neural and behavioral plasticity of animals. In fish stocking practices, the hatchery environment is relatively stimulus-deprived and does not optimally prepare fish for release into the wild. While the behavioral differences between wild and hatchery-reared fish have been examined to some extent, few studies have compared neurobiological characteristics between wild and hatchery-reared individuals. Here, we compare the expression of immediate early gene cfos and neuroplasticity marker brain-derived neurotrophic factor (bdnf) in telencephalic subregions associated with processing of stimuli in wild and hatchery-reared Atlantic salmon at basal and 30 min post (acute) stress conditions. Using in situ hybridization, we found that the expression level of these markers is highly specific per neuronal region and affected by both the origin of the fish, and exposure to acute stress. Expression of cfos was increased by stress in all brain regions and cfos was more highly expressed in the Dlv (functional equivalent to the mammalian hippocampus) of hatchery-reared compared to wild fish. Expression of bdnf was higher overall in hatchery fish, while acute stress upregulated bdnf in the Dm (functional equivalent to the mammalian amygdala) of wild, but not hatchery individuals. Our findings demonstrate that the hatchery environment affects neuroplasticity and neural activation in brain regions that are important for learning processes and stress reactivity, providing a neuronal foundation for the behavioral differences observed between wild and hatchery-reared fish.

Keywords: Atlantic salmon; bdnf; cfos; fish stocking; immediate early gene; in situ hybridization; neuroplasticity.

FIGURE 1

Selected subregions of the telencephalon. A transverse view of the Atlantic salmon telencephalon with a Toluidine Blue-stained left lobe and a schematic representation of the right lobe depicting the location of the dorsal (Dld) and ventral (Dlv) dorsolateral pallium, the dorsal (Dmd), and ventral (Dmv) dorsomedial pallium and the ventral part of the ventral telencephalon (Vv).

FIGURE 2

Acute stress elevates plasma cortisol levels. Effect of origin (hatchery vs. wild) and treatment (basal vs. stress) on mean ± SEM plasma cortisol levels of Atlantic salmon parr. Two-way analysis of variance (ANOVA) statistics are displayed in the figure, n = 7 per treatment.

FIGURE 3

In situ hybridization labeled cfos and bdnf cells in the Dl, Dld, and Dlv. Effect of origin (hatchery vs. wild) and treatment (basal vs. stress) on mean ± SEM expression of cfos (A–C) and brain-derived neurotrophic factor (bdnf; D–F) in the entire (dorsal + ventral) dorsolateral pallium (Dl; A,D), as well as the dorsal only (Dld; B,E) and the ventral only (Dlv; C,F) subregions. Two-way analysis of variance (ANOVA) statistics are displayed in each panel, n = 7 per treatment. Groups that do not share a similar lowercase letter are significantly different from one another (Tukey–Kramer HSD post-hoc test).

FIGURE 4

In situ hybridization labeled cfos and bdnf cells in the Dm, Dmd, and Dmv. Effect of origin (hatchery vs. wild) and treatment (basal vs. stress) on mean ± SEM expression of cfos (A–C) and brain-derived neurotrophic factor (bdnf; D–F) in the entire (dorsal + ventral) dorsomedial pallium (Dm; A,D), as well as the dorsal only (Dmd; B,E) and the ventral only (Dmv; C,F) subregions. Two-way analysis of variance (ANOVA) statistics are displayed in each panel, n = 7 per treatment. Groups that do not share a similar lowercase letter are significantly different from one another (Tukey–Kramer HSD post-hoc test).

FIGURE 5

In situ hybridization labeled cfos and bdnf cells in the Vv. Effect of origin (hatchery vs. wild) and treatment (basal vs. stress) on mean ± SEM expression of cfos (A) and brain-derived neurotrophic factor (bdnf; B) in the ventral part of the ventral telencephalon (Vv). Two-way analysis of variance (ANOVA) statistics are displayed in each panel, n = 7 per treatment.

FIGURE 6

Representative example of in situ hybridization of cfos and bdnf; images used for the quantification analysis. Representative pictures of the expression of cfos (A,B,E,F,I,J) and brain-derived neurotrophic factor (bdnf; C,D,G,H,K,L) transcripts (purple cells) in the dorsomedial pallium (Dm; A–D), dorsolateral pallium (Dl; E–H), and ventral part of the ventral telencephalon (Vv; I–L) of wild and hatchery-reared Atlantic salmon parr under basal or after acute stress conditions. WB, wild basal; WS, wild stress; HB, hatchery-reared basal; HS, hatchery-reared stress. Arrows indicate transcript-labeled cells and all scale bars measure 100 μm.