Insensitivity to reward shifts in zebrafish (Danio rerio) and implications for assessing affective states

Theory and empirical findings predict that individuals in a negative affective state are more sensitive to unexpected reward loss and less sensitive to unexpected reward gain compared to individuals in a neutral or positive affective state. We explore the use of sensitivity to reward shifts measured during successive contrast tasks as an indicator of affect in zebrafish (Danio rerio). In line with the assumption that exposure to rewarding stimuli induces a relatively positive affective state compared to exposure to stimuli that they do not prefer, we confirmed that zebrafish prefer enriched over barren environments, suggesting that the enriched environment is associated with positive affective states. We trained individuals to swim down a channel for food rewards of differing value and then presented them with unexpected increases or decreases in reward value. Contrary to our hypothesis, individuals conditioned to a high-value reward continued swimming at the same speed when reward value was downshifted, thus showing no successive negative contrast effect and appearing insensitive to reward loss. Individuals whose rewards were upshifted gradually increased their speed, but did not display successive positive contrast effects typical of sensitivity to reward gains. In both cases, housing type did not result in differences in swim time. One potential explanation is that goal-directed control of behaviour is necessary for an animal to show a successive contrast response to unexpected reward gain or loss, and the behaviour of zebrafish in this task was under habitual control, perhaps due to over-training. If so, refinements to task design and training procedures will allow further progress with this assay.