Unexpected rewards induce dopamine-dependent positive emotion–like state changes in bumblebees

Abstract

Whether invertebrates exhibit positive emotion-like states and what mechanisms underlie such states remain poorly understood. We demonstrate that bumblebees exhibit dopamine-dependent positive emotion-like states across behavioral contexts. After training with one rewarding and one unrewarding cue, bees that received pretest sucrose responded in a positive manner toward ambiguous cues. In a second experiment, pretest consumption of sucrose solution resulted in a shorter time to reinitiate foraging after a simulated predator attack. These behavioral changes were abolished with topical application of the dopamine antagonist fluphenazine. Further experiments established that pretest sucrose does not simply cause bees to become more exploratory. Our findings present a new opportunity for understanding the fundamental neural elements of emotions and may alter the view of how emotion states affect decision-making in animals.

Relationship between the grades of a learned aversive-feeding response and the dopamine contents inLymnaea

“…Thus, if the Day 5 snails are fed after they received the training, the memory phenotype can be expressed (Ito et al, 2015b). Recently, dopamine was also shown to be involved in positive emotion states, even in invertebrates (Perry et al, 2016). Our present findings thus suggest that one of the factors contributing to the ‘decision’ or ‘emotion’ to eat or not to eat is the dopamine content in the brain.…”

The relationship between personality and cognitionin the fowl, Gallus gallus

“…Recently studies have explored the influence of monoamines on judgment bias also in animals. Similar to the findings in humans, dopamine increased optimistic bias in rodents (Rodentia, Rygula et al 2014;Kregiel et al 2016) and bumblebees (Bombus terrestris, Perry et al 2016). In rodents, there is some evidence that serotonin (Rygula et al 2014;Anderson et al 2013) and norepinephrine (Rygula et al 2014;Enkel et al 2010) also influence judgment bias.…”

“…In the same study I further show that dopamine levels in the brain is associated with judgment bias. This is not surprising because dopamine is involved in learning about rewards (Wise 2004;Flagel et al 2011) and dopamine has recently been linked to judgment bias in other species (Sharot et al 2009;Rygula et al 2014;Kriegel et al 2016;Perry et al 2016). Here, I find support that levels of dopamine in the brain can influence judgment also in the fowl.…”

Sampling and tracking a changing environment: persistence and reward in the foraging decisions of bumblebees

“…Theoretical work suggests that optimism could be selected for by environmental uncertainty [52,53], and this can happen where fitness is being maximized over long time scales, despite optimism appearing as a bias over a short time scale. Recent empirical work shows that pessimistic and optimistic cognitive biases can be induced in bees following a negative or an unexpectedly positive experience [54,55]. The tracking models we have applied assume foragers are following a simple rule for their decisions (win -stay, loseshift) [9,10].…”