Abstract
SummarySensory cues in the natural environment predict reward or punishment, important for survival. For example, the ability to detect attractive tastes indicating palatable food is essential for foraging while the recognition of inedible substrates prevents harm. While some of these sensory responses are innate, they can undergo fundamental changes due to prior experience associated with the stimulus. However, the mechanisms underlying such behavioral switching of an innate sensory response at the neuron and network levels require further investigation. We used the model learning system of Lymnaea stagnalis1, 2, 3 to address the question of how an anticipated aversive outcome reverses the behavioral response to a previously effective feeding stimulus, sucrose. Key to the switching mechanism is an extrinsic inhibitory interneuron of the feeding network, PlB (pleural buccal4,5), which is inhibited by sucrose to allow a feeding response. After multi-trial aversive associative conditioning, pairing sucrose with strong tactile stimuli to the head, PlB’s firing rate increases in response to sucrose application to the lips and the feeding response is suppressed; this learned response is reversed by the photoinactivation of a single PlB. A learning-induced persistent change in the cellular properties of PlB that results in an increase rather than a decrease in its firing rate in response to sucrose provides a neurophysiological mechanism for this behavioral switch. A key interneuron, PeD12 (Pedal-Dorsal 12), of the defensive withdrawal network5,6 does not mediate the conditioned suppression of feeding, but its facilitated output contributes to the sensitization of the withdrawal response.
Highlights
At 24 h post-training, the US. Application of sucrose (the CS)+US paired group of animals showed a significantly reduced feeding response compared to the unpaired and naive group, and compared to its own pre-training feeding response to sucrose (Figure 1B, statistics in legend)
There was no significant difference between the pre- and post-training feeding responses to sucrose in the unpaired and naive group (Figure 1B) or in any of the other control groups used in the experiments (Figure S1B, statistics in legend), confirming that the change in the CS+US paired group was the result of associative learning
It was important to confirm that the reduction of the behavioral response after aversive conditioning is specific to the sucrose stimulus
Summary
At 24 h post-training, the CS+US paired group of animals showed a significantly reduced feeding response compared to the unpaired and naive group, and compared to its own pre-training feeding response to sucrose (Figure 1B, statistics in legend). There was no significant difference between the pre- and post-training feeding responses to sucrose in the unpaired and naive group (Figure 1B) or in any of the other control groups used in the experiments (Figure S1B, statistics in legend), confirming that the change in the CS+US paired group was the result of associative learning. It was important to confirm that the reduction of the behavioral response after aversive conditioning is specific to the sucrose stimulus Another salient feeding stimulus, fresh cucumber juice, was applied 24 h after aversive training with sucrose as the CS but there were no reductions in the feeding response
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