Optogenetic induction of appetitive and aversive taste memories in Drosophila

Abstract

SUMMARYTastes are typically thought to evoke innate appetitive or aversive behaviours, prompting food acceptance or rejection. However, research in Drosophila melanogaster indicates that taste responses can be modified through experience-dependent changes in mushroom body circuits. In this study, we develop a novel taste learning paradigm using closed-loop optogenetics. We find that appetitive and aversive taste memories can be formed by pairing gustatory stimuli with optogenetic activation of sensory or dopaminergic neurons associated with reward or punishment. As with olfactory memories, distinct dopaminergic subpopulations drive the parallel formation of short- and long-term appetitive memories. Long-term memories are protein synthesis-dependent and have energetic requirements that are satisfied by a variety of caloric food sources or by direct stimulation of MB-MP1 dopaminergic neurons. Our paradigm affords new opportunities to probe plasticity mechanisms within the taste system and understand the extent to which taste responses are experience dependent.

Taste cues elicit prolonged modulation of feeding behavior in Drosophila

“…Because behavioral modulation in our paradigm does not require simultaneous exposure to both tastes, the underlying circuit mechanisms are likely to be distinct from those previously described. Indeed, we found that prolonged PER modulation in our paradigm does not require the mushroom body, which mediates associative taste learning ( Kirkhart and Scott, 2015 ; Masek et al., 2015 ; Jelen et al., 2021 ).…”

“…Most studies have investigated cross-modulation between different taste modalities when they are presented at overlapping times. Different tastes presented together are acutely integrated to determine behavior ( Wang et al., 2004 ; Inagaki et al., 2014 ) and can modulate future responses through associative learning ( Kirkhart and Scott, 2015 ; Masek et al., 2015 ; Jelen et al., 2021 ). Because behavioral modulation in our paradigm does not require simultaneous exposure to both tastes, the underlying circuit mechanisms are likely to be distinct from those previously described.…”

“…In addition to regulating immediate feeding behavior, taste cues can also modulate future responses through learning. For example, studies in Drosophila have shown that pairing sugar with either natural or optogenetically triggered bitter taste diminishes subsequent feeding responses to sugar ( Kirkhart and Scott, 2015 ; Masek et al., 2015 ; Jelen et al., 2021 ). Pairing taste cues with odors can also modify future odor responses ( Schwaerzel et al., 2003 ; Krashes et al., 2009 ; Huetteroth et al., 2015 ; Das et al., 2014 ).…”

“…Pairing taste cues with odors can also modify future odor responses ( Schwaerzel et al., 2003 ; Krashes et al., 2009 ; Huetteroth et al., 2015 ; Das et al., 2014 ). Learned taste-taste and odor-taste associations in Drosophila are mediated by the mushroom body, the primary learning and memory center of the fly brain ( Kirkhart and Scott, 2015 ; Masek et al., 2015 ; Jelen et al., 2021 ; Schwaerzel et al., 2003 ; Krashes et al., 2009 ; Huetteroth et al., 2015 ; Das et al., 2014 ).…”

“…These taste learning paradigms, in which one taste modulates the future response to another taste, have used simultaneous or near-simultaneous exposure to both taste cues ( Kirkhart and Scott, 2015 ; Masek et al., 2015 ; Jelen et al., 2021 ). In a natural environment, animals may encounter different taste cues sequentially rather than simultaneously.…”