The caloric value of food intake structurally adjusts a neuronal mushroom body circuit mediating olfactory learning in Drosophila

Büsr Çoban, Haiko Poppinga, El Yazid Rachad, Bart Geurten, David Vasmer, Francisco Jesus Rodriguez Jimenez, Yogesh Gadgil, Stephan Hubertus Deimel, Idan Alyagor, Oren Schuldiner, Ilona C. Grunwald Kadow, Thomas Dieter Riemensperger, Annekathrin Widmann, André Fiala

Research output: Contribution to journalArticlepeer-review


Associative learning enables the adaptive adjustment of behavioral decisions based on acquired, predicted outcomes. The valence of what is learned is influenced not only by the learned stimuli and their temporal relations, but also by prior experiences and internal states. In this study, we used the fruit fly Drosophila melanogaster to demonstrate that neuronal circuits involved in associative olfactory learning undergo restructuring during extended periods of low-caloric food intake. Specifically, we observed a decrease in the connections between specific dopaminergic neurons (DANs) and Kenyon cells at distinct compartments of the mushroom body. This structural synaptic plasticity was contingent upon the presence of allatostatin A receptors in specific DANs and could be mimicked optogenetically by expressing a light-activated adenylate cyclase in exactly these DANs. Importantly, we found that this rearrangement in synaptic connections influenced aversive, punishment-induced olfactory learning but did not impact appetitive, reward-based learning. Whether induced by prolonged low-caloric conditions or optogenetic manipulation of cAMP levels, this synaptic rearrangement resulted in a reduction of aversive associative learning. Consequently, the balance between positive and negative reinforcing signals shifted, diminishing the ability to learn to avoid odor cues signaling negative outcomes. These results exemplify how a neuronal circuit required for learning and memory undergoes structural plasticity dependent on prior experiences of the nutritional value of food.

Original languageEnglish
Pages (from-to)1-15
Number of pages15
JournalLearning and Memory
Issue number5
StatePublished - May 2024

All Science Journal Classification (ASJC) codes

  • Neuropsychology and Physiological Psychology
  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience


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