Two Individually Identified Paired Dopamine Neurons Signal Taste Punishment in Larval Drosophila
Authors: Denise Weber 1; Katrin Vogt 2; Andreas Thum 1
Affiliations: 1) Institute of Biology; Department of Genetics, University of Leipzig, Germany; 2) Department of Neurobiology, University of Konstanz, Germany
Keywords: f. learning/memory; n. chemosensation
Dopaminergic neurons (DANs) perform multiple tasks in the brain. Among other things, DANs mediate teaching signals such as information about rewards and punishments throughout the animal kingdom. They serve to evaluate sensory input, store the resulting associations as memory, and continuously update them according to relevance and reliability. Therefore, to better understand the functioning of the dopaminergic system, it is crucial to know what specific roles are mediated by each DAN. To this end, we are studying Drosophila larvae, whose brains consist of only about 12,000 neurons, of which only about 1% are DANs.
Only eight larval DANs presynaptically project to the mushroom body, a brain region in insects that is of central importance to associative olfactory learning. These eight DANs in turn anatomically subdivide into four cells of the primary protocerebral anterior medial cluster (pPAM) and four cells of the dorsolateral 1 cluster (DL1). As we have shown in previous studies, the activity of the pPAM DANs encodes the internal gustatory sugar reward signal. In this study, we investigate the four DANs of the DL1 cluster in terms of their cellular function with respect to gustatory teaching signals. We discover that two DANs (DAN-f1 and DAN-g1) innervating two specific compartments of the vertical lobe of the mushroom body are in combination acutely necessary for learning of odor-high salt punishment, but dispensable for appetitive learning and innate behavior toward the applied odors and salt. Optogenetical activation of DAN-f1 and DAN-g1 neurons in the larval brain is sufficient to encode punishment. The functional specificity of DAN-f1 and DAN-g1 within the DL1 cluster and towards the PAM cluster is further confirmed by synaptic reconstruction of sensory and DAN input neurons. Thus, the DL1 neurons convey a punishment teaching signal.
In summary, this indicates that a cellular division of labor of larval DANs exists with respect to the transmission of dopaminergic reward (pPAM cluster) and punishment (DL1 cluster) signals. Since the organizing principle of larval DANs is the same as that of its adult counterpart and that of the mammalian basal ganglion, it is possible that there are only a limited number of efficient neural circuit solutions to solve complex cognitive and behavioral problems in nature.