Olfactory and Neuromodulatory Signals Reverse Visual Object Avoidance to Approach in Drosophila

Cheng, Karen Y.; Colbath, Rachel A; Frye, Mark A.

doi:10.1016/j.cub.2019.05.010

Cited by 47 publications

(22 citation statements)

References 80 publications

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“…Additional studies have shown that aminergic neurotransmitters can modulate visual information processing in flies and other insects [26,[41][42][43][44][45][46]. Octopamine, the invertebrate equivalent of noradrenaline, is present in processes innervating the medulla, lobula and lobula plate in Drosophila, where it regulates state-dependent modulation of visual interneurons [42,46] including the saliency of objects during flight [43]. Serotonergic neurons also innervate the optic ganglia [47][48][49][50][51][52] and previous studies indicate that serotonin impacts cellular activity and visual behaviors in insects [44,45,[53][54][55][56].…”

Section: Introductionmentioning

confidence: 99%

Serotonergic modulation of visual neurons in Drosophila melanogaster

et al. 2020

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Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It remains unclear whether serotonin modulates the physiology of interneurons in the optic ganglia. To address this question, we first mapped the expression patterns of serotonin receptors in the visual system, focusing on a subset of cells with processes in the first optic ganglion, the lamina. Serotonin receptor expression was found in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for spatiotemporal luminance contrast, and both 5-HT1A and 5-HT1B in T1 cells, whose function is unknown. Subcellular mapping with GFP-tagged 5-HT2B and 5-HT1A constructs indicated that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla neuropil is the primary site of serotonergic regulation for these neurons. Exogenous serotonin increased basal intracellular calcium in L2 terminals in layer M2 and modestly decreased the duration of visually induced calcium transients in L2 neurons following repeated dark flashes, but otherwise did not alter the calcium transients. Flies without functional 5-HT2B failed to show an increase in basal calcium in response to serotonin. 5-HT2B mutants also failed to show a change in amplitude in their response to repeated light flashes but other calcium transient parameters were relatively unaffected. While we did not detect serotonin receptor expression in L1 neurons, they, like L2, underwent serotonin-induced changes in basal calcium, presumably via interactions with other cells. These data demonstrate that serotonin modulates the physiology of interneurons involved in early visual processing in Drosophila.

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Section: Introductionmentioning

confidence: 99%

Serotonergic modulation of visual neurons in Drosophila melanogaster

et al. 2020

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“…In contrast to elongated vertical bars, which flies steer toward, flies steer away from smaller objects, which are presumably interpreted as a threat (Maimon et al, 2008 ). This avoidance of small objects switches to attraction in the presence of an attractive odor, such as vinegar (Cheng et al, 2019 ). The presence of a food odor may signify that the small object is not a threat but in fact a potential food source.…”

Section: Modulation By Environmental Contextmentioning

confidence: 99%

“…The presence of a food odor may signify that the small object is not a threat but in fact a potential food source. This odor-dependent switch from visual aversion to attraction can be mimicked by optogenetically activating modulatory octopaminergic neurons or motion-sensitive visual pathways in the optic lobe (Cheng et al, 2019 ). Previous work showed that vinegar activates octopaminergic neurons innervating the visual system (Wasserman et al, 2015 ).…”

Section: Modulation By Environmental Contextmentioning

confidence: 99%

Neural Circuits Underlying Behavioral Flexibility: Insights From Drosophila

Devineni

Scaplen

2022

Front. Behav. Neurosci.

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Behavioral flexibility is critical to survival. Animals must adapt their behavioral responses based on changes in the environmental context, internal state, or experience. Studies in Drosophila melanogaster have provided insight into the neural circuit mechanisms underlying behavioral flexibility. Here we discuss how Drosophila behavior is modulated by internal and behavioral state, environmental context, and learning. We describe general principles of neural circuit organization and modulation that underlie behavioral flexibility, principles that are likely to extend to other species.

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“…This modulation is consistent with, yet more subtle than, their free flight behaviour. It is worth noting that the difference between free flight [3] and tethered behaviour is also less pronounced in Drosophila [36]. Although the behavioural modulation we observed was subtle, quantifying the modulation allowed us to design a tethered preparation in which we could use calcium imaging to observe the neural basis for the behavioural modulation.…”

mentioning

confidence: 94%

Visual-olfactory integration in the human disease vector mosquito,Aedes aegypti

Vinauger

Breugel

Locke

et al. 2019

Preprint

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Mosquitoes rely on the integration of multiple sensory cues, including olfactory, visual, and thermal stimuli, to detect, identify and locate their hosts [1][2][3][4]. Although we increasingly know more about the role of chemosensory behaviours in mediating mosquito-host interactions [1], the role of visual cues remains comparatively less studied [3], and how the combination of olfactory and visual information is integrated in the mosquito brain remains unknown. In the present study, we used a tethered-flight LED arena, which allowed for quantitative control over the stimuli, to show that CO2 exposure affects target-tracking responses, but not responses to large-field visual stimuli. In addition, we show that CO2 modulates behavioural responses to visual objects in a time-dependent manner. To gain insight into the neural basis of this olfactory and visual coupling, we conducted two-photon microscopy experiments in a new GCaMP6s-expressing mosquito line. Imaging revealed that the majority of ROIs in the lobula region of the optic lobe exhibited strong responses to small-field stimuli, but showed little response to a large-field stimulus. Approximately 20% of the neurons we imaged were modulated when an attractive odour preceded the visual stimulus; these same neurons also elicited a small response when the odour was presented alone. By contrast, imaging in the antennal lobe revealed no modulation when visual stimuli were presented before or after the olfactory stimulus. Together, our results are the first to reveal the dynamics of olfactory modulation in visually evoked behaviours of mosquitoes, and suggest that coupling between these sensory systems is asymmetrical and timedependent.3 Results and DiscussionTo detect and locate suitable hosts, mosquitoes rely on multiple sensory cues, including olfactory, visual, and thermosensory information [1][2][3][4][5] while flying through a dynamic environment [6]. Whereas responses to olfactory (for review [7][8][9]) and, to a lesser extent, thermal stimuli [10,11] have been well studied, comparatively less is known about how visual cues evoke behavioural responses in mosquitoes (but see [12,13]) and how olfaction and vision are integrated. A recent study showed that CO2 detection activates a strong attraction to visual features that is critical for mediating interaction with close-range cues like heat and other host volatiles [3]. However, because this study relied on free-flight assays, it was difficult to control the sensory experience of the mosquitoes, which is a function of both their trajectories through space and the spatiotemporal distribution of the stimuli within the wind tunnel. In other animals, ranging from bees to humans, prior exposure to a visual stimulus can modify olfactory responses [14][15][16], and vice versa [17]. It thus remains an open question how the temporal order and interval between detection of olfactory and visual stimuli influences mosquito behaviour and processing in the brain.In contrast to free-flight assays, tethered flight experiments ...

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Olfactory and Neuromodulatory Signals Reverse Visual Object Avoidance to Approach in Drosophila

Cited by 47 publications

References 80 publications

Serotonergic modulation of visual neurons in Drosophila melanogaster

Serotonergic modulation of visual neurons in Drosophila melanogaster

Neural Circuits Underlying Behavioral Flexibility: Insights From Drosophila

Visual-olfactory integration in the human disease vector mosquito,Aedes aegypti

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