title: Aversive Learning and Appetitive Motivation Toggle Feed-Forward Inhibition in the Drosophila Mushroom Body.
abstract: In Drosophila, negatively reinforcing dopaminergic neurons also provide the inhibitory control of satiety over appetitive memory expression. Here we show that aversive learning causes a persistent depression of the conditioned odor drive to two downstream feed-forward inhibitory GABAergic interneurons of the mushroom body, called MVP2, or mushroom body output neuron (MBON)-γ1pedc>α/β. However, MVP2 neuron output is only essential for expression of short-term aversive memory. Stimulating MVP2 neurons preferentially inhibits the odor-evoked activity of avoidance-directing MBONs and odor-driven avoidance behavior, whereas their inhibition enhances odor avoidance. In contrast, odor-evoked activity of MVP2 neurons is elevated in hungry flies, and their feed-forward inhibition is required for expression of appetitive memory at all times. Moreover, imposing MVP2 activity promotes inappropriate appetitive memory expression in food-satiated flies. Aversive learning and appetitive motivation therefore toggle alternate modes of a common feed-forward inhibitory MVP2 pathway to promote conditioned odor avoidance or approach.
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, UK.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Perisse
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, UK.
authors.forename: David
authors.initials: D
authors.lastname: Owald
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, UK.
authors.forename: Oliver
authors.initials: O
authors.lastname: Barnstedt
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, UK.
authors.forename: Clifford B
authors.initials: CB
authors.lastname: Talbot
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, UK.
authors.forename: Wolf
authors.initials: W
authors.lastname: Huetteroth
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, UK. Electronic address: scott.waddell@cncb.ox.ac.uk.
authors.forename: Scott
authors.initials: S
authors.lastname: Waddell
mesh_terms: D000818:Animals; D001070:Appetitive Behavior / Q000502:physiology*; D001362:Avoidance Learning / Q000502:physiology*; D003214:Conditioning, Classical / Q000502:physiology; D004331:Drosophila melanogaster; D004435:Eating / Q000502:physiology; D059330:GABAergic Neurons / Q000502:physiology; D007395:Interneurons / Q000502:physiology; D008570:Memory, Short-Term; D009042:Motivation / Q000502:physiology*; D024521:Mushroom Bodies / Q000502:physiology*; D009433:Neural Inhibition / Q000502:physiology*; D009812:Odorants