Abstract
SummaryIn 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.
Highlights
Learning and internal states guide appropriate behavior by altering the properties of neural circuits
GAL4 Control of GABA-ergic MVP2 Neurons We used the R83A12-GAL4 (Jenett et al, 2012) and the MB112C split-GAL4 combination (Aso et al, 2014b; Aso et al, 2014a) drivers to investigate the role of MVP2 (MBON-g1pedc>ab) neurons
Expressing the dendritic UASDenMark (Nicolaıet al., 2010) and presynaptic UAS-GFP-Syd1 (Owald et al, 2010) markers in MVP2 neurons with R83A12 control suggests that dendrites of MVP2 occupy the g1 and base of the peduncle regions of the mushroom body (MB) (Figure 1C), where they are interspersed with the processes of the MP1 dopaminergic neurons (DANs) (Figure 1D), whereas the presynaptic regions are mostly within, or in close proximity to, the MB lobes (Figure 1C)
Summary
Learning and internal states guide appropriate behavior by altering the properties of neural circuits. A great number of studies across phyla have elucidated brain structures and cellular mechanisms that underlie these changes, but we still know relatively little about how experience and states are implemented in the functional connectivity of a neural network. Inhibition across a range of timescales from milliseconds to days, mediated by neurotransmitters, neuromodulators, and a variety of neuropeptides, is emerging as a critical and general operating principle of neural circuit function and behavioral control (Klausberger and Somogyi, 2008; Fishell and Rudy, 2011; Letzkus et al, 2015). Fast and persistent inhibition can alter neural excitability and the efficacy of synaptic transmission and thereby re-route the flow of information through circuits (Vogels and Abbott, 2005; Schwab and Houk, 2015). It is important to understand the mechanisms that control, and the circumstances in which, the level of inhibition is altered in the nervous system
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