Selective integration of diverse taste inputs within a single taste modality

Abstract

A fundamental question in sensory processing is how different channels of sensory input are processed to regulate behavior. Different input channels may converge onto common downstream pathways to drive the same behaviors, or they may activate separate pathways to regulate distinct behaviors. We investigated this question in the Drosophila bitter taste system, which contains diverse bitter-sensing cells residing in different taste organs. First, we optogenetically activated subsets of bitter neurons within each organ. These subsets elicited broad and highly overlapping behavioral effects, suggesting that they converge onto common downstream pathways, but we also observed behavioral differences that argue for biased convergence. Consistent with these results, transsynaptic tracing revealed that bitter neurons in different organs connect to overlapping downstream pathways with biased connectivity. We investigated taste processing in one type of downstream bitter neuron that projects to the higher brain. These neurons integrate input from multiple organs and regulate specific taste-related behaviors. We then traced downstream circuits, providing the first glimpse into taste processing in the higher brain. Together, these results reveal that different bitter inputs are selectively integrated early in the circuit, enabling the pooling of information, while the circuit then diverges into multiple pathways that may have different roles.

Driver lines for studying associative learning in Drosophila

“…On the other hand, gustatory sensory neurons constitute the first layer of neurons that detect food-related sensory signals (taste), which are conveyed to the MB through largely uncharacterized pathways (Bohra et al, 2018; Burke et al, 2012; Deere et al, 2023; Kim et al, 2017; Miyazaki et al, 2015; Sterne et al, 2021). GAL4 driver lines that recapitulate expression patterns of gustatory receptors (GRs) have been generated and utilized for functional studies (Dahanukar et al, 2007; Harris et al, 2015; Miyamoto et al, 2012; Wang et al, 2004; Yavuz et al, 2014).…”

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 .…”

Driver lines for studying associative learning in Drosophila

“…On the other hand, gustatory sensory neurons constitute the first layer of neurons that detect foodrelated sensory signals (taste), which are conveyed to the MB through largely uncharacterized pathways (Bohra et al, 2018 ;Burke et al, 2012 ;Deere et al, 2023 ;Kim et al, 2017 ;Miyazaki et al, 2015 ;Sterne et al, 2021 ). GAL4 driver lines that recapitulate expression patterns of gustatory receptors (GRs) have been generated and utilized for functional studies (Dahanukar et al, 2007 ;Harris et al, 2015 ;Miyamoto et al, 2012 ;Wang et al, 2004 ;Yavuz et al, 2014 ).…”