Linking a smell with an electric shock does not always have an aversive effect in flies.
Can relief from pain be a pleasure? If so, noxious events should — despite their typically aversive effects — also have a ‘rewarding’ after-effect1,2,3. Through training fruitflies by using an electric shock paired with an odour, we show here that the shock can condition either avoidance of this odour or approach to it. These opposing behaviours depend on the relative timing of the shock and odour presentations during training, and indicate that a shock can act as either an aversive reinforcer or an appetitive one.
To measure both aspects of these bidirectional behavioural responses within the same set-up, we used fruitflies (Drosophila melanogaster) that had undergone odour-discrimination learning reinforced by electric shock4 (Fig. 1a). All experimental groups received the same amount of odour–shock training. The only variable was the interstimulus interval (ISI), which was the interval between the onset times of exposure to the odour for association (the ‘trained’ odour) and to the shock (Fig. 1a). Training sessions were repeated four times and were separated by a 20-minute rest in a food vial.
The conditioned behaviour was tested 15 min after training in a forced-choice situation, by counting how many animals chose either a control or the trained odour (odour A or B, respectively; Fig. 1a). Positive learning indices indicate conditioned avoidance of the trained odour, whereas negative scores indicate conditioned approach to it.
During testing, flies showed opposite responses to the trained odour (either conditioned avoidance or approach), depending on the temporal sequence of odour and shock that they had experienced during training (Fig. 1b). If the odour preceded the shock, flies showed conditioned avoidance (for ISIs of −23 s and −3 s; P<0.005; Fig. 1b). However, when the shock preceded the odour, flies showed conditioned approach (for ISIs of +32 s and +42s; P<0.005; Fig. 1b). We conclude that flies were able to associate the same odour with either danger or safety. Control groups trained using very long ISIs gave no evidence of learning (for example, for ISIs of −83 s or +187 s, P>0.005 for forward or backward control, respectively; Fig. 1b).
We found that the effect of shock turns from punishing to rewarding in a time window around shock application (pink shading in Fig. 1b). This indicates that odours can act as predictors of danger when they precede shock during training but, owing to a long-lasting after-effect of shock, they can also be used to predict safety when they follow shock during training. Conditioned avoidance was stronger than conditioned approach (P<0.05, t-test: ISI, −23 s compared with +32 s). This quantitative comparison is possible because the two aspects of timing-dependent behavioural plasticity were directly measured within the same set-up, rather than indirectly2,5.
Bidirectional synaptic plasticity has a comparable dependence on timing: the sequence of two inputs determines whether synapses are potentiated or depressed6,7,8. This characteristic would lead to bidirectional associative learning if it occurred during association formation at the neuronal convergence site of odour and shock. Alternatively, the dual and opposing behavioural effects of shock could reflect a bidirectional modulation of internal reinforcement signalling, as found in mammalian dopaminergic neurons9,10. It will be interesting to investigate whether the appetitive effect of shock in flies shares a common neuronal circuitry with reward processing4. The detailed characterization of the rewarding after-effect of negative reinforcement should advance our understanding of the behavioural consequences of traumatic experience.
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The authors declare no competing financial interests.
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Tanimoto, H., Heisenberg, M. & Gerber, B. Event timing turns punishment to reward. Nature 430, 983 (2004). https://doi.org/10.1038/430983a
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