Omission of expected reward agitates Atlantic salmon (Salmo salar)

Abstract

The evolutionary background for cognition and awareness is currently under ardent scrutiny. Poikilothermic vertebrates such as teleost fishes are capable of classical conditioning and have long-term memories, but it remains unknown to what degree such capabilities are associated with affective states. Here, we investigate whether the concept of frustration may apply to Atlantic salmon. In mammals, this paradigm comprises the omission of an expected reward (OER), which elicits behavioural and physiological coping responses (e.g. aggression and stress reactions). Six groups with 200 fish in each were conditioned to associate a flashing light (CS) with feeding. Conditioning over 22 days led to a change from aversion to attraction to the CS. Subsequently, 3 groups served as control, and 3 groups were subjected to an OER paradigm for 9 days, in which the expected food reward was delayed for 30 min during two out of three daily meals. Compared to controls, OER groups displayed higher levels of aggression and more heterogeneous growth rates, indicating a more pronounced social hierarchy. Cortisol levels did, however, not differ between treatments and both groups responded similarly to acute stress. These results indicate that teleost fishes, like mammals, respond aggressively to OER. The capacity to respond behaviourally to frustrating conditions thus likely reflects an adaptive response to environmental unpredictability, which has been conserved throughout vertebrate evolution.

Coping with Unpredictability: Dopaminergic and Neurotrophic Responses to Omission of Expected Reward in Atlantic Salmon (Salmo salar L.)

“…Behavioral data from the current study was published in Vindas et al [19]. For clarity, the methods will be briefly described here.…”

“…One-way ANOVA was used to confirm a significant response to the conditioning regime (a detailed analysis of the conditioned response is presented in [19]). For the neuroendocrine variables (brain stem DA and 5-HT activity, telencephalic D1, BDNF and PCNA mRNA abundance, and plasma cortisol levels) a one-way ANOVA comparing 4 groups (i.e.…”

“…Such a motivational state is likely to affect behavior, and indeed, OER-induced frustration induces aggression in both mammals and birds [15]–[18]. Recently we reported that OER also increases aggressive behavior in a teleost model, the Atlantic salmon ( Salmo salar ) [19].…”

“…Therefore, in both undisturbed and acutely stressed salmon from the previously established OER paradigm [19], we quantify the neural plasticity marker abundance of BDNF and PCNA in the telencephalon, an area important for control of social interaction and aggression [41]. Furthermore, we quantify the abundance of DA receptors D1 and D2, which are involved in reward association in mammals [21], [27].…”

Frustrative reward omission increases aggressive behaviour of inferior fighters

“…Even though there is evidence of cognitive abilities in fishes [20,21], it remains under debate whether these abilities renders them capable of complex emotions [22,23]. However, recent evidence suggests that fish species show both behavioural and neuroendocrine responses to potentially frustrative situations [24][25][26][27], suggesting that this affective state is well conserved and has evolutionary roots within the early vertebrate lineage [24].…”