Cellular and circuit mechanisms of olfactory associative learning in<i>Drosophila</i>

Boto, Tamara; Stahl, Aaron; Tomchik, Seth M.

doi:10.1080/01677063.2020.1715971

Cited by 33 publications

(28 citation statements)

References 143 publications

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“…The Drosophila model, which is compelling in respect of size, behavioral complexity and tractability of cellular processes, represents an ideal candidate to analyze the population code underlying sensory processing or memory formation [9][10][11] (Fig. 1A).…”

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confidence: 99%

In vivo large-scale analysis of Drosophila neuronal calcium traces by automated tracking of single somata

Delestro

Scheunemann

Pedrazzani

et al. 2020

Sci Rep

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How does the concerted activity of neuronal populations shape behavior? impediments to address this question are primarily due to critical experimental barriers. An integrated perspective on large scale neural information processing requires an in vivo approach that can combine the advantages of exhaustively observing all neurons dedicated to a given type of stimulus, and simultaneously achieve a resolution that is precise enough to capture individual neuron activity. current experimental data from in vivo observations are either restricted to a small fraction of the total number of neurons, or are based on larger brain volumes but at a low spatial and temporal resolution. Consequently, fundamental questions as to how sensory information is represented on a population scale remain unanswered. in Drosophila melanogaster, the mushroom body (MB) represents an excellent model to analyze sensory coding and memory plasticity. In this work, we present an experimental setup coupled with a dedicated computational method that provides in vivo measurements of the activity of hundreds of densely packed somata uniformly spread in the MB. We exploit spinning-disk confocal 3D imaging over time of the whole MB cell body layer in vivo while it is exposed to olfactory stimulation. Importantly, to derive individual signal from densely packed somata, we have developed a fully automated image analysis procedure that takes advantage of the specificities of our data. After anisotropy correction, our approach operates a dedicated spot detection and registration over the entire time sequence to transform trajectories to identifiable clusters. This enabled us to discard spurious detections and reconstruct missing ones in a robust way. We demonstrate that this approach outperformed existing methods in this specific context and made possible high-throughput analysis of approximately 500 single somata uniformly spread over the MB in various conditions. Applying this approach, we find that learned experiences change the population code of odor representations in the MB. After long-term memory (LTM) formation, we quantified an increase in responsive somata count and a stable single neuron signal. We predict that this method, which should further enable studying the population pattern of neuronal activity, has the potential to uncover fine details of sensory processing and memory plasticity.All behavior relies on accurate information processing of sensory signals carried out by the concerted activity of populations of neurons 1,2 . While much is known about the pathways of neuronal transduction, how the integration of information derives from the cooperative action of neuronal activity remains largely elusive. However, for many functions of the brain such as sensory processing or memory plasticity, the important coding might be represented within the neuronal population rather than the individual cell. In animal models, recent developments in the field of in vivo imaging tools have allowed neuroscientists to characterize neuronal activity patte...

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mentioning

confidence: 99%

In vivo large-scale analysis of Drosophila neuronal calcium traces by automated tracking of single somata

Delestro

Scheunemann

Pedrazzani

et al. 2020

Sci Rep

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“…Serotonergic neurons project to various anatomical structures in the adult Drosophila brain including the mushroom body (MB), a structure critical for olfactory learning in the flies 21,22,42 . Although recent studies suggest that the output of serotonergic neurons is essential for certain forms of olfactory learning [20][21][22]41 , the evidence for serotonin's role in olfactory appetitive learning in Drosophila remains rather sparse when compared to the extensive evidence for dopamine's role in olfactory learning (reviewed in 7 ).…”

Section: Discussionmentioning

confidence: 99%

Serotonin receptor 5-HT7 in Drosophila mushroom body neurons mediates larval appetitive olfactory learning

Ganguly

Cheng

Bajaj

et al. 2020

Sci Rep

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Serotonin (5-HT) and dopamine are critical neuromodulators known to regulate a range of behaviors in invertebrates and mammals, such as learning and memory. Effects of both serotonin and dopamine are mediated largely through their downstream G-protein coupled receptors through cAMP-PKA signaling. While the role of dopamine in olfactory learning in Drosophila is well described, the function of serotonin and its downstream receptors on Drosophila olfactory learning remain largely unexplored. In this study we show that the output of serotonergic neurons, possibly through points of synaptic contacts on the mushroom body (MB), is essential for training during olfactory associative learning in Drosophila larvae. Additionally, we demonstrate that the regulation of olfactory associative learning by serotonin is mediated by its downstream receptor (d5-HT7) in a cAMP-dependent manner. We show that d5-HT7 expression specifically in the MB, an anatomical structure essential for olfactory learning in Drosophila, is critical for olfactory associative learning. Importantly our work shows that spatio-temporal restriction of d5-HT7 expression to the MB is sufficient to rescue olfactory learning deficits in a d5-HT7 null larvae. In summary, our results establish a critical, and previously unknown, role of d5-HT7 in olfactory learning.

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“…odour) and an unconditioned stimulus (US, e.g. sugar reward) can lead to a short-lived memory trace (STM) within distinct circuits [1][2][3][4][5]. Memories can be consolidated into long-term memories (LTM) through processes that are not fully understood, but depend on denovo protein synthesis [6,7], require structural modifications within the involved neuronal circuits and might lead to the recruitment of additional ones [8][9][10][11][12][13][14][15][16][17].…”

Section: Discussionmentioning

confidence: 99%

Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

Baltruschat

Ranft

Prisco

et al. 2020

Preprint

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The capacity of utilizing past experience to guide future action is a fundamental and conserved function of the nervous system. Associative memory formation initiated by the coincident detection of a conditioned stimulus (CS, e.g. odour) and an unconditioned stimulus (US, e.g. sugar reward) can lead to a short-lived memory trace (STM) within distinct circuits. Memories can be consolidated into long-term memories (LTM) through processes that are not fully understood, but depend on de-novo protein synthesis, require structural modifications within the involved neuronal circuits and might lead to the recruitment of additional ones. Compared to modulation of existing connections, the reorganization of circuits affords the unique possibility of sampling for potential new partners. Nonetheless, only few examples of rewiring associated with learning have been established thus far. Here, we report that memory consolidation is associated with the structural and functional reorganization of an identified circuit in the adult fly brain. The formation and retrieval of olfactory associative memories in Drosophila requires the mushroom body (MB). We identified the individual synapses of olfactory projection neurons (PNs) that deliver a conditioned odour to the MB and reconstructed the complexity of the microcircuit they form. Combining behavioural experiments with high-resolution microscopy and functional imaging, we demonstrated that the consolidation of appetitive olfactory memories closely correlates with an increase in the number of synaptic complexes formed by the PNs that deliver the conditioned stimulus and their postsynaptic partners. These structural changes result in additional functional synaptic connections.

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Cellular and circuit mechanisms of olfactory associative learning inDrosophila

Cited by 33 publications

References 143 publications

In vivo large-scale analysis of Drosophila neuronal calcium traces by automated tracking of single somata

In vivo large-scale analysis of Drosophila neuronal calcium traces by automated tracking of single somata

Serotonin receptor 5-HT7 in Drosophila mushroom body neurons mediates larval appetitive olfactory learning

Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

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