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AC and PKC differentiate operant and classical learning in Drosophila
AuthorBjörn Brembs
Author email bjoern©
Author website
DescriptionFlies without adenylyl cyclase (rutabaga mutants) and transgenic flies expressing an inhibitory pseudosubstrate of protein kinase C (PKCi) under the control of a heat-shock promoter were subjected to three experimental procedures: one with only a classical predictor, one with only an operant predictor and one with both predictors. There was a double dissociation of PKC and AC on operant and classical learning in Drosophila. AC is required for classical, but not for operant learning and PKC is required for operant, but not for classical learning. We also found a hierarchical interaction between operant and classical components in learning situations where both operant and classical predictors are present. In such situations, the classical component dominates the learning task as evidenced by impaired learning in rut mutants but not in the PKCi flies. Experiments with transgenic flies impairing mushroom-body function revealed that the mushroom-bodies mediate this hierarchical interaction by inhibiting operant learning when a classical predictor is present. This inhibition enables generalization of the classical memory and prevents premature habit formation. Extended training in wildtype flies produced a phenocopy of mushroom-body impaired flies, such that generalization was abolished and goal-directed actions were transformed into habitual responses.
In conclusion, operant learning situations consisting of both operant and classical predictors lead to a hierarchical and reciprocal interaction between two memory systems in the fly's brain. The AC-dependent classical system inhibits memory storage by the PKC-dependent operant system via the mushroom-bodies. The operant system, in turn, facilitates memory storage by the classical system via unknown, non-mushroom-body pathways. This interaction leads to efficient learning, enables generalization and prevents premature habit-formation. Habit formation after extended training reveals the gate-keeping role of the mushroom-bodies, allowing only well-rehearsed behaviors to crystallize into habits.
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