Integration of Parallel Opposing Memories Underlies Memory Extinction.
Jacob, Pedro F
Edmondson-Stait, Amelia J
Smith, Carlas S
Lauritzen, J Scott
Bock, Davi D
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Felsenberg, J., Jacob, P. F., Walker, T., Barnstedt, O., Edmondson-Stait, A. J., Pleijzier, M., Otto, N., et al. (2018). Integration of Parallel Opposing Memories Underlies Memory Extinction.. Cell, 175 (3), 709-722.e15. https://doi.org/10.1016/j.cell.2018.08.021
Accurately predicting an outcome requires that animals learn supporting and conflicting evidence from sequential experience. In mammals and invertebrates, learned fear responses can be suppressed by experiencing predictive cues without punishment, a process called memory extinction. Here, we show that extinction of aversive memories in Drosophila requires specific dopaminergic neurons, which indicate that omission of punishment is remembered as a positive experience. Functional imaging revealed co-existence of intracellular calcium traces in different places in the mushroom body output neuron network for both the original aversive memory and a new appetitive extinction memory. Light and ultrastructural anatomy are consistent with parallel competing memories being combined within mushroom body output neurons that direct avoidance. Indeed, extinction-evoked plasticity in a pair of these neurons neutralizes the potentiated odor response imposed in the network by aversive learning. Therefore, flies track the accuracy of learned expectations by accumulating and integrating memories of conflicting events.
Drosophila, competition, connectomics, dopamine, extinction, memory, neural circuit, neural plasticity, parallel memory
S.W. was funded by a Wellcome Principal Research Fellowship (200846/Z/16/Z), by the Gatsby Charitable Foundation (GAT3237), and by the Bettencourt-Schueller Foundation. J.F. was supported by the DFG (FE 1563/1-1). G.S.X.E.J. was funded by Medical Research Council. D.D.B. funded by HHMI. G.S.X.E.J., D.D.B., and S.W. were funded by a Wellcome Collaborative Award (203261/Z/16/Z).
WELLCOME TRUST (203261/Z/16/Z)
ECH2020 EUROPEAN RESEARCH COUNCIL (ERC) (649111)
External DOI: https://doi.org/10.1016/j.cell.2018.08.021
This record's URL: https://www.repository.cam.ac.uk/handle/1810/289391
Attribution 4.0 International
Licence URL: http://creativecommons.org/licenses/by/4.0/
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