Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila

By Raphael Cohn, Ianessa Morantte, V. Ruta. 2015

409 citations recorded by the source corpus.

SUMMARY Learned and adaptive behaviors rely on neural circuits that flexibly couple the same sensory input to alternative output pathways. Here, we show that the Drosophila mushroom body functions like a switchboard in which neuromodulation reroutes the same odor signal to different behavioral circuits, depending on the state and experience of the fly. Using functional synaptic imaging and electrophysiology, we reveal that dopaminergic inputs to the mushroom body modulate synaptic transmission with exquisite spatial specificity, allowing individual neurons to differentially convey olfactory signals to each of their postsynaptic targets. Moreover, we show that the dopaminergic neurons function as an interconnected network, encoding information about both an animal's external context and internal state to coordinate synaptic plasticity throughout the mushroom body. Our data suggest a general circuit mechanism for behavioral flexibility in which neuromodulatory networks act with synaptic precision to transform a single sensory input into different patterns of output activity.

Subfields: Cellular and Molecular Neuroscience, Endocrine and Autonomic Systems, Neuroscience

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Cellular and Molecular Neuroscience

In Endocrine and Autonomic Systems

In Neuroscience

Citations in the corpus

A Comprehensive Survey of Continual Learning: Theory, Method and Application (2023, background): “, a memory center in fruit fly) coordinating multiple parallel compartments to process the sequentially-arrived experiences [23], [24], [78], [310], [421], corresponding to the use of modular networks in continual learning [15], [353], [430].”
Incorporating neuro-inspired adaptability for continual learning in artificial intelligence (2023, neutral): “We further explore the organizing principles of the γMB system that support its function, which employs five compartments (γ1–γ5) with dynamic modulations to perform continual learning in parallel 20–24 .”
CoSCL: Cooperation of Small Continual Learners is Stronger than a Big One (2022, neutral): “In contrast, the robust biological learning system applies multiple compartments (i.e, sub-networks) to process sequential experiences in parallel, and integrates their outputs in a weighted-sum fashion to guide adaptive behaviors [3,9,32].”
Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “Taken together, these observations suggest that DAN activation paired with an odor produces an aversive behavioral response to that odor by decreasing the MBON’s attractive output.”
Toward an Integration of Deep Learning and Neuroscience (2016, background): “Extensions of such approaches could perhaps be used to ask which cost functions the brain is optimizing. odor representations (Caron et al., 2013; Aso et al., 2014a,b; Cohn et al., 2015).”
Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, background): “At the level of these compartments, information is stored on appetitive and aversive (odor) associations, in addition to non- associative information, such as the relative familiarity of an odor (Owald and Waddell, 2015; Owald et al., 2015; Aso et al., 2019; Aso et al., 2014b; Aso et al., 2014a; Bou”
A connectome of a learning and memory center in the adult Drosophila brain (2017, methodology): “Although changes in KC>MBON strength contribute to this process (Cohn et al., 2015), our results here suggest that such state changes could also potentially be conveyed to the MBONs directly from the DANs.”
A genetically-encoded fluorescent sensor enables rapid and specific detection of dopamine in flies, fish, and mice (2018, result): “Thus, GRABDA sensors create new opportunities for exploring how specific compartments in the MB of the fly may exhibit distinct DA dynamics, which has been suggested by previous reports (Aso et al., 2014; Cognigni et al., 2018; Cohn et al., 2015; Mao and Davis, 2009).”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, positive): “Recent work has now demonstrated compartment-specific changes in synaptic strength at KC-to-MBON synapses following paired optogenetic activation of dopaminergic neurons with KC activation (Cohn et al., 2015; Hige et al., 2015a).”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “Dopamine receptor expression is heterogeneous across both KCs and MBONs (Crocker et al. 2016, Croset et al. 2018), so the differences could lie in the signaling cascades that drive plasticity or in the mechanics of adjusting synaptic vesicle release.”
Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “Many DANs respond 206 specifically to punishment (electric shock) or reward (sugar) [63], and blocking DANs 207 prevents memory formation [64-66], while artificial activation of DANs alone during odor 208 stimulus is sufficient to induce memory formation [67-73] (see Table 1).”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “We imaged optical reporters of secondmessengers downstream of Gas and Gaq during conditioning, focusing on KC axons given that they likely serve as a relevant locus for associative plasticity in the mushroom body (Boto et al., 2014; Cohn et al., 2015; Qin et al., 2012; Zars et al., 2000).”