Diverse physiology and function of dopaminergic neurons in behaving Drosophila

Abstract

In many animals, including both mammals and insects like Drosophila, dopamine is associated with learning, motivation, and regulation of voluntary movement. In mammals, the activity of individual dopaminergic neurons (DANs) (Fisher et al., 2019; Kim et al., 2019) can correlate with movement initiation and rewarding stimuli, and the same is also true in Drosophila. There are ~50 distinct morphological types of DAN in the Drosophila brain, many of which have largely unknown functional roles. We set out to study the connectivity and in vivo physiology of three previously uncharacterized types of DANs that arborize in the lateral horn, a higher olfactory processing region. We found that these DANs are functionally diverse. The activity of two of these DANs was correlated with odor stimuli and locomotion, and repeated presentations of odor resulted in adaptation of both their odor-related and locomotor-related activity. By contrast, the third DAN was mainly correlated with locomotion, was unresponsive to odor, and was non-adapting. Thus, the lateral horn is innervated by diverse DANs encoding distinct combinations of olfactory signals, locomotor signals, and recent experience. In a separate study, we investigated the physiology and functional role of another DAN, this one located in the fly’s compass network. Recent work suggests that associative plasticity in this network enables visual landmarks to be mapped onto specific heading directions to aid in navigation. Given the well-established role of dopamine in associative plasticity elsewhere in the fly brain, we hypothesized that this DAN might be mediating that phenomenon. We recorded the activity of the DAN in walking flies and found that it is active mainly during locomotion, and is strongly correlated with the fly’s current rotational (turning) speed. Activating the DAN in the presence of a visual landmark results in an acute increase in the compass signal and persistent remapping of the landmark’s location relative to the fly’s heading (or formation of such a map if one does not already exist). Importantly, we did not observe this persistent effect when we activated the DAN in the absence of visual landmarks. These results support a model in which dopamine controls the association of visual landmarks with the brain’s internal compass.