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Devineni, A. V.

Publications and source records attributed to Devineni, A. V..

7 recordsLinked to original sources

Dual roles of Drosophila reward-encoding dopamine neurons in regulating innate and learned behaviors

Dopaminergic neurons (DANs) play a key role in learning the value of cues that predict reward. The fruit fly Drosophila has provided a powerful model to dissect the mechanisms by which reward-encoding DANs mediate reward learning. However, the role of these DANs in regulating innate behaviors is less clear. Here, we show that activating the entire population of reward-encoding DANs in Drosophila drives innate aversion in multiple behavioral assays, including feeding, locomotion, and spatial preference, even as these neurons confer a positive value onto associated cues to drive future learned attraction. Activating subsets of DANs reveals that the effects on innate and learned behaviors are dissociable. Based on known circuitry, it is likely that innate aversion and learned attraction elicited by DANs arise from distinct effects - direct activation versus synaptic plasticity - on the same target neurons. These results reveal distinct roles for reward-encoding DANs in guiding immediate and future behavior.

neuroscience↗

Connectomic analysis of taste circuits in Drosophila

Our sense of taste is critical for regulating food consumption. The fruit fly Drosophila represents a highly tractable model to investigate mechanisms of taste processing, but taste circuits beyond sensory neurons are largely unidentified. Here, we use a whole-brain connectome to investigate the organization of Drosophila taste circuits. We trace pathways from four populations of sensory neurons that detect different taste modalities and project to the subesophageal zone (SEZ). We find that second-order taste neurons are primarily located within the SEZ and largely segregated by taste modality, whereas third-order neurons have more projections outside the SEZ and more overlap between modalities. Taste projections out of the SEZ innervate regions implicated in feeding, olfactory processing, and learning. We characterize interconnections between taste pathways, identify modality-dependent differences in taste neuron properties, and use computational simulations to relate connectivity to predicted activity. These studies provide insight into the architecture of Drosophila taste circuits.

neuroscience↗

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

A single sensory cue can elicit diverse behavioral responses. For example, the taste of sugar robustly promotes feeding1, 2 but also influences other behaviors, such as altering locomotor patterns to maximize food-finding3, 4 or conferring a rewarding value onto associated contexts or cues.5-7 Here, we investigate how sweet taste elicits multiple appetitive behaviors in Drosophila. 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.8 By 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.

neuroscience↗

Taste cues elicit prolonged modulation of feeding behavior in Drosophila

Taste cues regulate immediate feeding behavior, but their ability to modulate future behavior has been less well-studied. Pairing one taste with another can modulate subsequent feeding responses through associative learning, but this requires simultaneous exposure to both stimuli. We investigated whether exposure to one taste modulates future responses to other tastes even when they do not overlap in time. Using Drosophila, we found that brief exposure to sugar enhanced future feeding responses, whereas bitter exposure suppressed them. This modulation relies on neural pathways distinct from those that acutely regulate feeding or mediate learning-dependent changes. Sensory neuron activity was required not only during initial taste exposure but also afterward, suggesting that ongoing sensory activity may maintain experience-dependent changes in downstream circuits. Thus, the brain stores a memory of each taste stimulus after it disappears, enabling animals to integrate information as they sequentially sample different taste cues that signal local food quality.

neuroscience↗

Selective integration of diverse taste inputs within a single taste modality

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 second-order 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.

neuroscience↗

Individual bitter-sensing neurons in Drosophila exhibit both ON and OFF responses that influence synaptic plasticity

The brain creates internal representations that translate sensory stimuli into appropriate behavior. Most studies of sensory processing focus on which subsets of neurons are activated by a stimulus, but the temporal features of the neural response are also important for behavior. In the taste system, the timing of peripheral sensory responses has rarely been examined. We investigated the temporal properties of taste responses in Drosophila melanogaster and discovered that different types of taste sensory neurons show striking differences in their response dynamics. Strong responses to stimulus onset (ON responses) and offset (OFF responses) were observed in bitter-sensing neurons in the labellum, whereas bitter neurons in the leg and other classes of labellar taste neurons showed only an ON response. Individual bitter labellar neurons generate both the ON and OFF responses through a cell-intrinsic mechanism that requires canonical bitter receptors. The bitter ON and OFF responses at the periphery are propagated to dopaminergic neurons that innervate the mushroom body and mediate aversive learning. When bitter is used as a reinforcement cue, the bitter ON and OFF responses can drive opposing types of synaptic plasticity and the effect of the OFF response dominates, likely due to the rapid and preferential habituation of the ON response. Together, these studies characterize novel features of neural responses in the taste system and reveal their importance for neural circuit function.

neuroscience↗

Acetic acid activates distinct taste pathways in Drosophila to elicit opposing, state-dependent feeding responses

Taste circuits are genetically determined to elicit an innate appetitive or aversive response, ensuring that animals consume nutritious foods and avoid the ingestion of toxins. We have examined the response of the fruit fly Drosophila melanogaster to acetic acid, a tastant that can be a metabolic resource but can also be toxic to the fly. Our data reveal that flies accommodate these conflicting attributes of acetic acid by virtue of a hunger-dependent switch in their behavioral response to this stimulus. Fed flies show taste aversion to acetic acid, likely a response to its potential toxicity, whereas starved flies show a robust appetitive response that may reflect their overriding need for calories. These opposing responses are mediated by two different classes of taste neurons. Acetic acid activates both the sugar and bitter pathways, which have opposing effects on feeding behavior. Hunger shifts the response from aversion to attraction by enhancing the appetitive sugar pathway as well as suppressing the aversive bitter pathway. Thus a single tastant can drive opposing behaviors by activating distinct taste pathways modulated by internal state.

neuroscience↗