Predictive olfactory learning in Drosophila

Abstract

Olfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

Collective action or individual choice: Spontaneity and individuality contribute to decision-making in Drosophila

“…But an individual fly will make its own decision” (cited by [ 39 ]). Similar observations as in the quote were described for flies conditioned to prefer a particular odor [ 40 ] and recently mentioned again in [ 41 ]. In both cases, the setup used was similar to the classic countercurrent phototaxis paradigm (CPP) developed by Benzer, where flies have several opportunities in one session to approach a light source and the population ends up being split according to how many times each fly chose approaching the light [ 42 ].…”

A Mechanistic Model for Reward Prediction and Extinction Learning in the Fruit Fly

“…In vertebrates, it has been shown that prediction error coding dopaminergic neurons (DANs) are involved in learning ( Schultz et al, 1997 ; Schultz, 2016 ). Recent studies give rise to the assumption that DANs could play a similar role in Drosophila melanogaster ( Hammer, 1997 ; Riemensperger et al, 2005 ; Ichinose et al, 2015 ; Eichler et al, 2017 ; Felsenberg et al, 2017 , 2018 ; Zhao et al, 2021 ; Eschbach et al, 2020 ) and other insects ( Terao and Mizunami, 2017 ), rejuvenating an earlier hypothesis based on experimental observations in the honeybee ( Hammer, 1997 ).…”

A Drosophila Circuit for Habituation Override

“…In the mushroom body, dopaminergic neurons potentially compute novelty by combining excitatory inputs from olfactory sensory channels with inhibitory inputs driven by familiarity encoding interneurons (Zhao et al, 2021) (and see Discussion). If TH-positive cells were to play a similar role in the SEZ, then they would be predicted to receive direct or indirect inputs from taste sensory neurons as well as input from familiarity-representing inhibitory neurons.…”