Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

Baltruschat, Lothar; Prisco, Luigi; Ranft, Philipp; Lauritzen, J. Scott; Fiala, André; Bock, Davi D.; Tavosanis, Gaia

doi:10.1016/j.celrep.2021.108871

Cited by 38 publications

(56 citation statements)

References 78 publications

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“…Taking advantage of emerging electron microscopy (EM) datasets covering a full adult fly brain (FAFB, (Zheng et al 2018)) or a large fraction of it (Hemibrain, (Scheffer et al 2020)), we examined the distribution of synaptic contacts between APL, PNs and KCs, the major cell types constituting the MGs of the mushroom body calyx (Leiss et al 2009b; Yasuyama, Meinertzhagen, and Schürmann 2002a; Baltruschat et al 2021) (Fig 1A). We recently reconstructed an entire MG in the FAFB dataset, starting from a PN-bouton of the DA1 glomerulus and tracing all its pre- and post-synaptic partners (Baltruschat et al 2021). Here, we focused on the synaptic connections involving APL.…”

Section: Resultsmentioning

confidence: 99%

“…APL is suggested to regulate sparse coding by participating in a closed feedback loop with the MB, similarly to its homolog giant GABAergic neuron (GGN) in the locust (Papadopoulou et al 2011; A. C. Lin et al 2014; Litwin-Kumar et al 2017). However, APL is both pre- and post- synaptic to PNs and KCs in the adult calyx (Yasuyama, Meinertzhagen, and Schürmann 2002b; Wu et al 2013; Baltruschat et al 2021). Additionally, APL response to localized stimuli is spatially restricted (Amin et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

Prisco

Deimel²,

Yeliseyeva

et al. 2021

Preprint

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To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

Prisco

Deimel²,

Yeliseyeva

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

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“…CREB-dependent regulation of gene expression in DAL neurons appears sufficient to promote systems memory consolidation by modulating neural excitability. Further studies may elucidate whether neural circuits involved in motivation and attention also modulate DAL neurons during LTM formation ( 25 , 26 ) and whether such prolonged neural activity also produces synaptic plasticity in DAL neurons ( 19 , 27 ).…”

Section: Discussionmentioning

confidence: 99%

CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila

Lin

Chen

Belle

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Episodic events are frequently consolidated into labile memory but are not necessarily transferred to persistent long-term memory (LTM). Regulatory mechanisms leading to LTM formation are poorly understood, however, especially at the resolution of identified neurons. Here, we demonstrate enhanced LTM following aversive olfactory conditioning in Drosophila when the transcription factor cyclic AMP response element binding protein A (CREBA) is induced in just two dorsal-anterior-lateral (DAL) neurons. Our experiments show that this process is regulated by protein–gene interactions in DAL neurons: (1) crebA transcription is induced by training and repressed by crebB overexpression, (2) CREBA bidirectionally modulates LTM formation, (3) crebA overexpression enhances training-induced gene transcription, and (4) increasing membrane excitability enhances LTM formation and gene expression. These findings suggest that activity-dependent gene expression in DAL neurons during LTM formation is regulated by CREB proteins.

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“…The microglomeruli that form as projection neurons from the antennal lobe connecting to the Kenyon cell dendrites at the calyx are also modified by experience. After conditioning young flies with an odorant (11- cis -vaccenylacetate) to form long-term memory, the size of the microglomeruli responding to this odorant decreased, but the number of such microglomeruli increased ( Baltruschat et al, 2021 ). This demonstrated that new synaptic boutons are formed during learning and for long-term memory and that structural change is linked to brain function.…”

Section: Structural Plasticity and Homeostasis In The Adult Drosophila Brainmentioning

confidence: 99%

“…It was recently shown that rut, which encodes Ca 2+ /CaM-dependent adenyl cyclase, is also required for structural plasticity at the calyx. In fact, long-term memory modifies the size and number of microglomeruli in the calyx, but this effect was abolished in rut mutants or by blocking protein synthesis ( Baltruschat et al, 2021 ). Thus, cAMP regulates plasticity in calyx but not the visual system, which means that distinct molecular pathways may underlie structural plasticity in distinct brain regions ( Barth and Heisenberg, 1997 ).…”

Section: Molecular Mechanisms Of Structural Brain Plasticitymentioning

confidence: 99%

The Toll Route to Structural Brain Plasticity

Hidalgo

2021

Front. Physiol.

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The human brain can change throughout life as we learn, adapt and age. A balance between structural brain plasticity and homeostasis characterizes the healthy brain, and the breakdown of this balance accompanies brain tumors, psychiatric disorders, and neurodegenerative diseases. However, the link between circuit modifications, brain function, and behavior remains unclear. Importantly, the underlying molecular mechanisms are starting to be uncovered. The fruit-fly Drosophila is a very powerful model organism to discover molecular mechanisms and test them in vivo. There is abundant evidence that the Drosophila brain is plastic, and here we travel from the pioneering discoveries to recent findings and progress on molecular mechanisms. We pause on the recent discovery that, in the Drosophila central nervous system, Toll receptors—which bind neurotrophin ligands—regulate structural plasticity during development and in the adult brain. Through their topographic distribution across distinct brain modules and their ability to switch between alternative signaling outcomes, Tolls can enable the brain to translate experience into structural change. Intriguing similarities between Toll and mammalian Toll-like receptor function could reveal a further involvement in structural plasticity, degeneration, and disease in the human brain.

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Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

Cited by 38 publications

References 78 publications

The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila

The Toll Route to Structural Brain Plasticity

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