Preparing Adult &lt;em&gt;Drosophila melanogaster&lt;/em&gt; for Whole Brain Imaging during Behavior and Stimuli Responses

Woller, Alexandra; Bandow, Paul; Aimon, Sophie; Kadow, Ilona C. Grunwald

doi:10.3791/61876

Cited by 7 publications

(9 citation statements)

References 13 publications

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“…For instance, recent evidence suggests that changes in hormone levels trigger circuit maturation in Drosophila flies during the first week of life ( Leinwand and Scott, 2021 ). We used whole brain lightfield imaging to record the activity of all neurons in the brain in living female flies ( nsyb-Gal4;UAS-CaMP ) ( Aimon et al, 2022 ; Aimon et al, 2019 ; Woller et al, 2021 Figure 2—figure supplement 1A ). Mating did not appear to change brain activity globally in 1-week-old mated and virgin females stimulated with putrescine, and we did not find any significant brain-wide mating state-dependent changes ( Figure 2—figure supplement 1B, C ).…”

Section: Resultsmentioning

confidence: 99%

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A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Boehm

Friedrich

Hunt

et al. 2022

eLife

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Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Drosophila females, we find that mating does not induce a global change in brain activity. Instead, mating modulates the pheromone response of dopaminergic neurons innervating the fly's learning and memory center, the mushroom body (MB). Using the mating-induced increased attraction to the odor of important nutrients, polyamines, we show that disruption of the female fly's ability to smell, for instance the pheromone cVA, during mating leads to a reduction in polyamine preference for days later indicating that the odor environment at mating lastingly influences female perception and choice behavior. Moreover, dopaminergic neurons including innervation of the β'1 compartment are sufficient to induce the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the β'1 compartment are activated by pheromone odor and their activity during mating bidirectionally modulates preference behavior in mated and virgin females. Their activity is not required, however, for the expression of polyamine attraction. Instead, inhibition of another type of MBON innervating the β'2 compartment enables expression of high odor attraction. In addition, the response of a lateral horn (LH) neuron, AD1b2, which output is required for the expression of polyamine attraction, shows a modulated polyamine response after mating. Taken together, our data in the fly suggests that mating-related sensory experience regulates female odor perception and expression of choice behavior through a dopamine-gated learning circuit.

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Section: Resultsmentioning

confidence: 99%

“…Successful mating or virginity was confirmed later by keeping the vials at 25 °C and checking for larvae a few days after the experiment. Flies were prepared for whole brain imaging at Day 4 after eclosion, as previously described ( Woller et al, 2021 ). The light field microscope was set up according to Aimon et al, 2019 .…”

Section: Methodsmentioning

confidence: 99%

A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Boehm

Friedrich

Hunt

et al. 2022

eLife

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“…For instance, recent evidence suggests that changes in hormone levels trigger circuit maturation in Drosophila flies during the first week of life (Leinwand & Scott, 2021). We used whole brain lightfield imaging to record the activity of all neurons in the brain in living female flies ( nsyb-Gal4;UAS-CaMP ) (Aimon, Cheng, Gjorgjieva, & Grunwald Kadow, 2022; Aimon et al, 2019; Woller, Bandow, Aimon & Grunwald Kadow, 2021) (Fig. S2A).…”

Section: Resultsmentioning

confidence: 99%

“…We used whole brain lightfield imaging to record the activity of all neurons in the brain in living female flies ( nsyb-Gal4;UAS-CaMP ) (Sophie Aimon, Cheng, Gjorgjieva, & Grunwald Kadow, 2022; S. Aimon et al, 2019; Woller, Bandow, Aimon, & Grunwald Kadow, 2021) (Fig. S2A).…”

Section: Resultsmentioning

confidence: 99%

A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Boehm

Friedrich

Bandow

et al. 2021

Preprint

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Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in most female animals. Here, we show that a mating-induced increase in olfactory attraction of female Drosophila flies to nutrients relies on interconnected neural pathways in the two higher olfactory brain regions, the lateral horn (LH) and the mushroom body (MB). Using whole brain calcium imaging, we find that mating does not induce a global change in the activity of the whole brain nor of entire brain regions, suggesting specific neuronal or network changes in the olfactory system. Systematic behavioral screening and electron microscopy (EM) connectomics identify two types of LH output neurons required for the attraction of females to polyamines -one of them previously implicated in the processing of male pheromones. In addition, we characterize multiple MB pathways capable of inducing or suppressing polyamine attraction, with synaptic connections to the identified LH neurons and a prominent role for the β′1 compartment. Moreover, β′1 dopaminergic neurons are modulated by mating and are sufficient to replace mating experience in virgins inducing the lasting behavioral switch in female preference. Taken together, our data in the fly suggests that reproductive state-dependent expression of female choice behavior is regulated by a dopamine-gated distributed learning circuit comprising both higher olfactory brain centers.

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“…We identified candidate neurons for all regions such as DNb02 and DNb01 for IPS-Y and LAL-PS, respectively (Table 2). These DNs were previously described by Namiki et al, who generated specific Gal4 lines for neuronal manipulation 32 . For instance, optogenetic activation of DNb01 induced twitching of the fly's front legs consistent with a role in turning 33 .…”

Section: Turning Activates Specific Brain Regions and Neuronsmentioning

confidence: 99%

Combined patterns of activity of major neuronal classes underpin a global change in brain state during spontaneous and forced walk inDrosophila

Aimon

Cheng

Gjorgjieva

et al. 2022

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Movement and behavioral state influence perception, and a stimulus can elicit opposite behavioral actions depending on whether the animal is moving toward or away from it. Here, we use fast wholebrain lightfield imaging in adult Drosophila melanogaster to analyze the relationship between movement and neuronal activity. Using pan-neuronal calcium imaging, we observe brainwide neuronal activity that tightly correlated with spontaneous bouts of movement. Imaging of specific sets of neurons across the brain reveals that both excitatory and inhibitory as well as different types of neuromodulatory neurons are active during walk inconsistent with a reduction of inhibition on neuronal activity. While most neuron types are activated at walk-onset, serotonergic neurons show more complex patterns of activity with neurons in several brain regions being inhibited during walk. Using available anatomical data, we map forward running and turning-induced activity onto different brain subregions and sometimes individual neurons. Moreover, we find that spontaneous walk and forced walk elicit highly similar wholebrain activity suggesting that a large part of the observed activity corresponds to walk itself rather than its initiation by higher brain centers. Based on our data, we conclude that movement and movement-related sensory feedback signals originating in the ventral nerve cord induce wide-spread activity in the brain allowing the integration of behavioral state into most or all brain processes.

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Preparing Adult <em>Drosophila melanogaster</em> for Whole Brain Imaging during Behavior and Stimuli Responses

Cited by 7 publications

References 13 publications

A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Combined patterns of activity of major neuronal classes underpin a global change in brain state during spontaneous and forced walk inDrosophila

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