Overlap and divergence of neural circuits mediating distinct behavioral responses to sugar

Abstract

SUMMARYA single sensory cue can elicit diverse behavioral responses. For example, the taste of sugar robustly promotes feeding1, 2but also influences other behaviors, such as altering locomotor patterns to maximize food-finding3, 4or conferring a rewarding value onto associated contexts or cues.5–7Here, we investigate how sweet taste elicits multiple appetitive behaviors inDrosophila. Are different sugar-evoked behaviors coordinately regulated? At what point does the sugar circuit diverge into different pathways that drive distinct behaviors? We first established an optogenetic paradigm to study the effects of sugar taste on locomotion, spatial preference, and associative learning. We then tested how different sugar-evoked behaviors were modulated by internal and external factors, including hunger, diet, or the presence of an aversive taste. Different behaviors were generally modulated in similar ways, but we also observed some differences that reveal selective modulation of specific behavioral pathways. Finally, we investigated where the sugar taste circuit diverges into different behavioral pathways. A recent study identified a sensory-motor circuit comprising five layers of neurons that drives the initiation of feeding in response to sugar.8By individually manipulating each of these neurons, we show that circuits mediating different innate responses to sugar are partially overlapping and begin to diverge at the level of second- and third-order neurons, whereas circuits for innate versus learned behaviors may diverge at the first synapse. Connectomic analyses reveal distinct subcircuits that mediate different behaviors. Together, these studies provide insight into how neural circuits are organized to elicit diverse behavioral responses to a single stimulus.

Taste cells expressingIonotropic Receptor 94ereciprocally impact feeding and egg laying inDrosophila

“…To determine if IR94e GRNs may be involved in other behaviors that rely on chemosensation, we turned to the Drosophila melanogaster whole-brain connectome in which every neuron and synapse from one female brain has been fully reconstructed with predicted neurotransmitters [4][5][6]39 . IR94e and other GRNs were previously identified in the connectome where they were found to synapse with local interneurons and putative taste projection neurons (TPNs) 31,33,[40][41][42] . Using FlyWire 5 , we identified a link to oviposition by establishing that IR94e GRNs synapse onto five projection neurons that connect to oviposition descending neurons (OviDNs), either directly or through one interneuron (Fig.…”

“…The Drosophila whole-brain connectome has already facilitated the description of a complete PER circuit 31 , the majority of SEZ neurons 40 , and specific GRN circuits related to taste processing 41,42 . Recently, a leaky integrate-and-fire model based on the connectome predicted that IR94e GRNs would be inhibitory through the PER circuitry, which was supported by the observation that IR94e activation mildly inhibited sucrose PER 33 .…”