Gamma Neurons Mediate Dopaminergic Input during Aversive Olfactory Memory Formation in Drosophila

Qin, Hui; Cressy, Michael; Li, Wanhe; Coravos, Jonathan S.; Izzi, Stephanie A.; Dubnau, Josh

doi:10.1016/j.cub.2012.02.014

Cited by 165 publications

(196 citation statements)

References 48 publications

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“…36). In addition, the reported role of dopamine and serotonin in ARM (8,10,11) is consistent with the proposed structural plasticity model, as both neurotransmitters have been implicated in spine dynamics in both insects (37) and vertebrates (38,39).…”

Section: Discussionsupporting

confidence: 69%

“…It appears then that at least two circuits and parallel molecular pathways contribute to ARM (16): an Oct2β2 receptor-mediated Rsh-independent in the α′ß′ lobes (9) and an Rsh-dependent, d5HT1A serotonin receptor-mediated in the αβ (8), which also receives Dop2R-mediated signals (11). Finally, Dop1R1 and Dop2R activities in the γ lobes have been suggested to contribute to ARM (10,11). Drk, an SH2-SH3 domain adaptor protein orthologous to the mammalian Grb2, is also expressed preferentially in α/β neurons.…”

mentioning

confidence: 99%

“…Proteins with demonstrated roles in ARM formation include Radish (Rsh) (5); the constitutively active atypical PKC, PKM (6); the calcium channel Bruchpilot (Brp) (7); the d5HT1A serotonin and Oct2β2 octopamine receptors (8,9); the Dop1R1, Dop2R dopamine receptors (10,11); and Protein Kinase A (12). However, whether these molecules operate in one or more ARMmediating signaling cascades is presently unclear.…”

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confidence: 99%

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Drk-mediated signaling to Rho kinase is required for anesthesia-resistant memory in Drosophila

Kotoula

Moressis

Semelidou

et al. 2017

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

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Significance Anesthesia-resistant memory (ARM) has been puzzling because unlike long-term memory (LTM), it is translation independent in Drosophila . Although the two forms of consolidated memory are housed within the mushroom body neurons, they seem to employ distinct molecular pathways, with those that underlie ARM largely unknown. Elucidation of these pathways is essential to understanding ARM, how it differs from LTM, and what underlies their apparent inverse relationship. We reveal a signaling pathway that underlies ARM. Collectively, our results and already published results lead us to propose that a molecular hallmark of ARM formation is activity-dependent localized structural and functional changes in the neuronal actin cytoskeleton that alter synaptic strength or properties stable enough to last at least 24 h.

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Section: Discussionsupporting

confidence: 69%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Drk-mediated signaling to Rho kinase is required for anesthesia-resistant memory in Drosophila

Kotoula

Moressis

Semelidou

et al. 2017

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

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“…A wealth of evidence suggests that aversive olfactory memory exists as a persistent neural activity ("trace") in a sparse subset of MB neurons-initially in the γ lobes lasting for several minutes and then spreading to α/β lobes for several hours (34)(35)(36). This physiological trace drives a protein-synthesis-dependent process in postsynaptic MB-V3 neurons, yielding structural change at MB::MB-V3 synapses (Fig.…”

Section: Discussionmentioning

confidence: 99%

Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation

Pai

Chen

Lin

et al. 2013

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

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Memory is initially labile and gradually consolidated over time through new protein synthesis into a long-lasting stable form. Studies of odor-shock associative learning in Drosophila have established the mushroom body (MB) as a key brain structure involved in olfactory long-term memory (LTM) formation. Exactly how early neural activity encoded in thousands of MB neurons is consolidated into protein-synthesis-dependent LTM remains unclear. Here, several independent lines of evidence indicate that changes in two MB vertical lobe V3 (MB-V3) extrinsic neurons are required and contribute to an extended neural network involved in olfactory LTM: (i) inhibiting protein synthesis in MB-V3 neurons impairs LTM; (ii) MB-V3 neurons show enhanced neural activity after spaced but not massed training; (iii) MB-V3 dendrites, synapsing with hundreds of MB α/β neurons, exhibit dramatic structural plasticity after removal of olfactory inputs; (iv) neurotransmission from MB-V3 neurons is necessary for LTM retrieval; and (v) RNAi-mediated downregulation of oo18 RNA-binding protein (involved in local regulation of protein translation) in MB-V3 neurons impairs LTM. Our results suggest a model of long-term memory formation that includes a systems-level consolidation process, wherein an early, labile olfactory memory represented by neural activity in a sparse subset of MB neurons is converted into a stable LTM through protein synthesis in dendrites of MB-V3 neurons synapsed onto MB α lobes.L ong-term memory (LTM) and long-term synaptic plasticity require de novo protein synthesis, which is regulated at transcriptional and/or translational levels in a synapse-specific manner (1-3). Synapse-specific plasticity during LTM formation in some contexts may involve local regulation of protein translation by a family of RNA-binding proteins, the cytoplasmic polyadenylation element-binding proteins (CPEBs) (2). Neuronal CPEBs have two conformational states. The inactive state predominates at low levels of CPEB expression and represses translation from nascent mRNAs. The active state is achieved either via a self-perpetuating prion-like state when expression levels surpass a threshold or via Ca 2+ /calmoduline-dependent protein kinase II (CaMKII)-mediated phosphorylation, and translation is initiated by elongation of an mRNA's poly-A tail (4-6). In other species, CPEB1 has been shown to contribute to long-term facilitation or potentiation (5, 7). In Drosophila, oo18 RNA-binding protein 2 (ORB2) appears required for long-term memory formation after courtship conditioning (8, 9). Any role for ORB in fruit fly memory formation, however, remains unclear.Drosophila can learn to associate an odor (conditioned stimulus, CS) with foot-shock punishment (unconditioned stimulus, US). This odor-shock association initially is labile, lasting for only about a day after one training session. With repetitive, spaced training (ST) sessions (rest intervals between each session), a protein synthesis-dependent, LTM is formed. With repetitive, massed training (MT) ses...

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“…formation, consolidation and retrieval), so dissecting the neural circuits underlying is crucial for mechanistically understanding the memory processing and the pathological basis of neurological diseases associated with memory defi cits (Silva et al, 2009;van Strien et al, 2009;Small et al, 2011;Tye and Deisseroth, 2012). In Drosophila, with the power of sophisticated genetic toolbox and behavioral paradigm, extensive studies suggest a dynamic requirement for the three major subtypes of mushroom body (MB) neurons in olfactory conditioning: γ neurons server as a gateway to support memory formation by dopaminergic signal-mediated CS-US association (Blum et al, 2009;Qin et al, 2012), α'/β' neurons were transiently required to stabilize memory after training (Krashes et al, 2007) and to retrieve the immediate memory (Wang et al, 2008), and the outputs of α/β neurons are necessary for retrieving both aversive and appetitive long-term memory (LTM) (Isabel et al, 2004;Krashes et al, 2008;Trannoy et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

The differential requirement of mushroom body α/β subdivisions in long-term memory retrieval in Drosophila

et al. 2013

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The mushroom body (MB), a bilateral brain structure possessing about 2000-2500 neurons per hemisphere, plays a central role in olfactory learning and memory in Drosophila melanogaster. Extensive studies have demonstrated that three major types of MB neurons (α/β, α'/β' and γ) exhibit distinct functions in memory processing, including the critical role of approximately 1000 MB α/β neurons in retrieving long-term memory. Inspired by recent fi ndings that MB α/β neurons can be further divided into three subdivisions (surface, posterior and core) and wherein the α/β core neurons play an permissive role in long-term memory consolidation, we examined the functional differences of all the three morphological subdivisions of MB α/β by temporally precise manipulation of their synaptic outputs during long-term memory retrieval. We found the normal neurotransmission from a combination of MB α/β surface and posterior neurons is necessary for retrieving both aversive and appetitive long-term memory, whereas output from MB α/β posterior or core subdivision alone is dispensable. These results imply a specifi c requirement of about 500 MB α/β neurons in supporting long-term memory retrieval and a further functional partitioning for memory processing within the MB α/β region.

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Gamma Neurons Mediate Dopaminergic Input during Aversive Olfactory Memory Formation in Drosophila

Cited by 165 publications

References 48 publications

Drk-mediated signaling to Rho kinase is required for anesthesia-resistant memory in Drosophila

Drk-mediated signaling to Rho kinase is required for anesthesia-resistant memory in Drosophila

Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation

The differential requirement of mushroom body α/β subdivisions in long-term memory retrieval in Drosophila

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