A Plastic Visual Pathway Regulates Cooperative Behavior in Drosophila Larvae

Dombrovski, Mark; Kim, Anna; Poussard, Leanne M.; Vaccari, Andrea; Acton, Scott T.; Spillman, Emma; Condron, Barry; Yuan, Quan

doi:10.1016/j.cub.2019.04.060

Cited by 22 publications

(38 citation statements)

References 47 publications

(97 reference statements)

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“…1a). This proposal is further supported by recent studies on the role of the Rh6-PR/lOLP pathway in larval movement detection and social clustering behaviors 27 . However, it remains unclear how the lOLPs support differential coding for ON and OFF signals without anatomical separation at either the input or output level.…”

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confidence: 70%

Muscarinic acetylcholine receptor signaling generates OFF selectivity in a simple visual circuit

et al. 2019

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ON and OFF selectivity in visual processing is encoded by parallel pathways that respond to either light increments or decrements. Despite lacking the anatomical features to support split channels, Drosophila larvae effectively perform visually-guided behaviors. To understand principles guiding visual computation in this simple circuit, we focus on investigating the physiological properties and behavioral relevance of larval visual interneurons. We find that the ON vs. OFF discrimination in the larval visual circuit emerges through light-elicited cholinergic signaling that depolarizes a cholinergic interneuron (cha-lOLP) and hyperpolarizes a glutamatergic interneuron (glu-lOLP). Genetic studies further indicate that muscarinic acetylcholine receptor (mAchR)/Gαo signaling produces the sign-inversion required for OFF detection in glu-lOLP, the disruption of which strongly impacts both physiological responses of downstream projection neurons and dark-induced pausing behavior. Together, our studies identify the molecular and circuit mechanisms underlying ON vs. OFF discrimination in the Drosophila larval visual system.

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confidence: 70%

Muscarinic acetylcholine receptor signaling generates OFF selectivity in a simple visual circuit

et al. 2019

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“…Techniques of “pre-processed” vial production and transplantation of 200 L2 (60 hAEL) larvae were adapted from our previous studies (Dombrovski et al 2017 , 2019 and Fig. 1 a).…”

Section: Methodsmentioning

confidence: 99%

“…Earlier studies also indicate that to cluster, larvae must pass through a visual critical period early in the third instar (Dombrovski et al 2017(Dombrovski et al , 2019, and animals transplanted into vials of processed food after this critical period show greatly reduced clustering. Therefore, we tested the effects of reducing clustering by post-visual critical period transplantation.…”

Section: Cooperative Foraging Further Delays Larval Development In Prmentioning

confidence: 95%

“…To address these questions, we make use of a novel experimental model system featuring cooperative foraging behavior in larval Drosophila melanogaster . Interestingly, although behavioral and developmental aspects of larval solitary foraging behavior were addressed a long time ago (Sokolowski 1982 ; Godoy-Herrera 1977 , 1986 ; Wu et al 2003 ; Kim et al 2017 ), mechanistic and neuroethological features of cooperative foraging in larval Drosophila have only recently been characterized (Durisko et al 2014 ; Dombrovski et al 2017 , 2019 ; Khodaei and Long 2019 ). Feeding clusters form in semi-liquid food, comprised of 10–200 animals and share a unique set of characteristics that make it an attractive model for studying collective social behavior.…”

Section: Introductionmentioning

confidence: 99%

“…Intriguingly, cluster membership and ability to efficiently engage in visually guided cooperation require prior visual and social experience during a critical period in development (Slepian et al 2015 ; Dombrovski et al 2017 ). In addition, emergence of clustering is associated with functional changes of larval visual circuit (Dombrovski et al 2019 ). This raises the question as to the function of this behavior and its emergence in evolution.…”

Section: Introductionmentioning

confidence: 99%

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Cooperative foraging during larval stage affects fitness in Drosophila

et al. 2020

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Cooperative behavior can confer advantages to animals. This is especially true for cooperative foraging which provides fitness benefits through more efficient acquisition and consumption of food. While examples of group foraging have been widely described, the principles governing formation of such aggregations and rules that determine group membership remain poorly understood. Here, we take advantage of an experimental model system featuring cooperative foraging behavior in Drosophila. Under crowded conditions, fly larvae form coordinated digging groups (clusters), where individuals are linked together by sensory cues and group membership requires prior experience. However, fitness benefits of Drosophila larval clustering remain unknown. We demonstrate that animals raised in crowded conditions on food partially processed by other larvae experience a developmental delay presumably due to the decreased nutritional value of the substrate. Intriguingly, same conditions promote the formation of cooperative foraging clusters which further extends larval stage compared to nonclustering animals. Remarkably, this developmental retardation also results in a relative increase in wing size, serving an indicator of adult fitness. Thus, we find that the clustering-induced developmental delay is accompanied by fitness benefits. Therefore, cooperative foraging, while delaying development, may have evolved to give Drosophila larvae benefits when presented with competition for limited food resources.

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Critical periods shaping the social brain: A perspective from Drosophila

Dombrovski

Condron

2020

BioEssays

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Many sensory processing regions of the central brain undergo critical periods of experience-dependent plasticity. During this time ethologically relevant information shapes circuit structure and function. The mechanisms that control critical period timing and duration are poorly understood, and this is of special importance for those later periods of development, which often give rise to complex cognitive functions such as social behavior. Here, we review recent findings in Drosophila, an organism that has some unique experimental advantages, and introduce novel views for manipulating plasticity in the post-embryonic brain. Critical periods in larval and young adult flies resemble classic vertebrate models with distinct onset and termination, display clear connections with complex behaviors, and provide opportunities to control the time course of plasticity. These findings may extend our knowledge about mechanisms underlying extension and reopening of critical periods, a concept that has great relevance to many human neurodevelopmental disorders.

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A Plastic Visual Pathway Regulates Cooperative Behavior in Drosophila Larvae

Cited by 22 publications

References 47 publications

Muscarinic acetylcholine receptor signaling generates OFF selectivity in a simple visual circuit

Muscarinic acetylcholine receptor signaling generates OFF selectivity in a simple visual circuit

Cooperative foraging during larval stage affects fitness in Drosophila

Critical periods shaping the social brain: A perspective from Drosophila

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