Reversal learning in Drosophila larvae

Abstract

Adjusting behavior to changed environmental contingencies is critical for survival, and reversal learning provides an experimental handle on such cognitive flexibility. Here, we investigate reversal learning in larval Drosophila. Using odor-taste associations, we establish olfactory reversal learning in the appetitive and the aversive domain, using either fructose as a reward or high-concentration sodium chloride as a punishment, respectively. Reversal learning is demonstrated both in differential and in absolute conditioning, in either valence domain. In differential conditioning, the animals are first trained such that an odor A is paired, for example, with the reward whereas odor B is not (A+/B); this is followed by a second training phase with reversed contingencies (A/B+). In absolute conditioning, odor B is omitted, such that the animals are first trained with paired presentations of A and reward, followed by unpaired training in the second training phase. Our results reveal "true" reversal learning in that the opposite associative effects of both the first and the second training phase are detectable after reversed-contingency training. In what is a surprisingly quick, one-trial contingency adjustment in the Drosophila larva, the present study establishes a simple and genetically easy accessible study case of cognitive flexibility.

Recurrent architecture for adaptive regulation of learning in the insect brain

“…An important aspect of reinforcement learning theories is the idea that modulatory neurons compare predicted and actual US (to compute so-called prediction errors) and drive memory formation or extinction depending on the sign of the prediction error. While Drosophila modulatory neurons have not yet been directly shown to represent prediction errors, adult and larval Drosophila are capable of extinction 3 ; 30 ; 31 , and our study reveals candidate motifs that could support the comparison of expected and actual US. We found that modulatory neurons receive convergent input from feedback pathways from MBONs and from US pathways ( Fig.…”

“…We assessed the contributions of different feedback pathways by repeating the optimization procedure for networks lacking such feedback and comparing their performance. Tasks included first-order conditioning and extinction which have been demonstrated in both larval 15 ; 30 and adult Drosophila 3 ; 31 , and second-order and context-dependent conditioning which have so far been investigated only in adult 32 ; 33 . In second-order conditioning, a reinforcement predicting conditioned stimulus is used to reinforce a second stimulus, while in context-dependent conditioning, the US valence depends on a previous contextual input.…”

Useful road maps: studying Drosophila larva’s central nervous system with the help of connectomics

“…Future research will include richer behavioral situations ( e.g . [ 42 , 72 , 73 ]), in vivo recording of whole-brain activity [ 23 , 24 , 25 ], modelling approaches ( e.g. [ 8 , 11 , 16 , 18 , 52 ]).…”

Multilevel feedback architecture for adaptive regulation of learning in the insect brain

“…While Drosophila modulatory neurons have not yet been directly shown to represent prediction errors, adult and larval Drosophila are capable of extinction 5, 13,53,141,154 , and our study reveals candidate motifs that could support the comparison of expected and actual US. We found that modulatory neurons receive convergent input from feedback pathways from MBONs and from US pathways ( Fig.…”