Reward signaling in a recurrent circuit of dopaminergic neurons and peptidergic Kenyon cells

• Published in: Nature communications Vol. 10; no. 1; pp. 3097 - 14
• Main Authors: Lyutova, Radostina, Selcho, Mareike, Pfeuffer, Maximilian, Segebarth, Dennis, Habenstein, Jens, Rohwedder, Astrid, Frantzmann, Felix, Wegener, Christian, Thum, Andreas S., Pauls, Dennis
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 15-07-2019; Nature Publishing Group; Nature Portfolio
• Subjects: 13/51; 14/19; 14/28; 14/35; 631/378/1595; 631/378/3920; 64/24; Acetylcholine; Acetylcholine - metabolism; Animals; Appetite - physiology; Behavior; Brain; Brain - cytology; Brain - physiology; Cell activation; Circuits; Conditioning, Classical; Dopamine receptors; Dopaminergic Neurons - physiology; Drosophila melanogaster - physiology; Feedback; Feedback, Physiological; Fruit flies; Humanities and Social Sciences; Insects; Larva; Larvae; Memory - physiology; Models, Psychological; multidisciplinary; Mushroom bodies; Mushroom Bodies - cytology; Mushroom Bodies - physiology; Neural Pathways - physiology; Neurobiology; Neurons; Neuropeptide F; Neuropeptides - metabolism; Neurosciences; Odor; Odorants; Odors; Olfactory discrimination learning; Olfactory Perception - physiology; Optogenetics; Reinforcement; Reward; Science; Science (multidisciplinary); Sensory stimulation; Signaling
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-019-11092-1

Dopaminergic neurons in the brain of the
Drosophila
larva play a key role in mediating reward information to the mushroom bodies during appetitive olfactory learning and memory. Using optogenetic activation of Kenyon cells we provide evidence that recurrent signaling exists between Kenyon cells and dopaminergic neurons of the primary protocerebral anterior (pPAM) cluster. Optogenetic activation of Kenyon cells paired with odor stimulation is sufficient to induce appetitive memory. Simultaneous impairment of the dopaminergic pPAM neurons abolishes appetitive memory expression. Thus, we argue that dopaminergic pPAM neurons mediate reward information to the Kenyon cells, and in turn receive feedback from Kenyon cells. We further show that this feedback signaling is dependent on short neuropeptide F, but not on acetylcholine known to be important for odor-shock memories in adult flies. Our data suggest that recurrent signaling routes within the larval mushroom body circuitry may represent a mechanism subserving memory stabilization.
Olfactory information from Kenyon cells in the mushroom body and reward information from pPAM dopaminergic neurons is required for appetitive olfactory learning and memory. Here, the authors report evidence for a feedback circuit mechanism between Kenyon cells and pPAM neurons for reward memory that involves short neuropeptide F.