Imaging of an Early Memory Trace in the<i>Drosophila</i>Mushroom Body

Wang, Yalin; Mamiya, Akira; Chiang, Ann‐Shyn; Zhong, Yi

doi:10.1523/jneurosci.2958-07.2008

Cited by 127 publications

(162 citation statements)

References 41 publications

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“…The early memory trace has been visualized only in the α′/β′ neurons in which neurotransmission outputs are required for memory acquisition and consolidation but not for retrieval (20,45). Consistent with this notion, developmental disruption of DPM neurons, so that their fibers project mostly but not entirely to the α′/β′ lobes, produces significantly higher memory than the amnesiac mutant (39), suggesting that the Amnesiac peptide acts primarily on α′/β′ neurons.…”

Section: Resultsmentioning

confidence: 85%

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Lee

Lin

Chang

et al. 2011

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

133

151

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Pavlovian olfactory learning in Drosophila produces two genetically distinct forms of intermediate-term memories: anesthesia-sensitive memory, which requires the amnesiac gene, and anesthesiaresistant memory (ARM), which requires the radish gene. Here, we report that ARM is specifically enhanced or inhibited in flies with elevated or reduced serotonin (5HT) levels, respectively. The requirement for 5HT was additive with the memory defect of the amnesiac mutation but was occluded by the radish mutation. This result suggests that 5HT and Radish protein act on the same pathway for ARM formation. Three supporting lines of evidence indicate that ARM formation requires 5HT released from only two dorsal paired medial (DPM) neurons onto the mushroom bodies (MBs), the olfactory learning and memory center in Drosophila: (i) DPM neurons were 5HT-antibody immunopositive; (ii) temporal inhibition of 5HT synthesis or release from DPM neurons, but not from other serotonergic neurons, impaired ARM formation; (iii) knocking down the expression of d5HT1A serotonin receptors in α/β MB neurons, which are innervated by DPM neurons, inhibited ARM formation. Thus, in addition to the Amnesiac peptide required for anesthesia-sensitive memory formation, the two DPM neurons also release 5HT acting on MB neurons for ARM formation.brain | olfaction | aversive conditioning | neurotransmitter P avlovian olfactory learning in Drosophila involves coincidence detection of a conditioned stimulus (CS), an odor, and an unconditioned stimulus (US), an electric shock (1). After one session of aversive olfactory conditioning, flies can form short-and intermediate-term memories but not long-term memory (LTM), which requires repetitive spaced training and is dependent on protein synthesis (2, 3). The intermediate-term memory has been dissected further into an anesthesia-sensitive form (ASM) that requires a gene called "amnesiac" and an anesthesia-resistant form (ARM) that requires the radish gene (4-6). Three hours after one session of training, ARM and ASM contribute equally to performance and can be distinguished by application of a short cold shock-induced anesthesia that impairs ASM but not ARM. Importantly, although ARM is consolidated, in the sense that it is resistant to cold shock, it is not thought to be a protein synthesisdependent memory because it is resistant to cycloheximide (CXM) (2). One day after repetitive spaced training, both ARM and LTM are thought to contribute to memory performance. In contrast, repetitive massed training without rest intervals induces only radish-dependent ARM without detectable cAMP response element binding protein-dependent LTM measured 1 d after training (2, 3) (but see ref.2 for an alternative model). Thus, more than one genetically distinct memory-storage system contributes to performance both at intermediate time points (e.g., 3 h after one training session) and at later time points (e.g., 24 h after repetitive training). Given the complexity of memory consolidation observed at the genetic level, much effor...

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Section: Resultsmentioning

confidence: 85%

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Lee

Lin

Chang

et al. 2011

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

133

151

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“…In vivo GCaMP imaging is as previously described in Wang et al (1). Please see SI Methods for more details.…”

Section: Methodsmentioning

confidence: 99%

“…CPEB | CREB | fragile X mental retardation | STAU | PUM 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)(2)(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).…”

mentioning

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.

120

135

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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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“…With the increasing knowledge concerning the anatomy and physiology of the mushroom body, we are making good progress towards an understanding of memory formation and retrieval. Recent functional imaging studies of the mushroom body of D. melanogaster, have, for example, revealed memory traces, manifested as Ca 2+ activity, in specific subtypes of Kenyon cells (Wang et al 2008, Yu et al 2006. If the predictions by Turner et al (2008) are correct, i.e.…”

Section: Anatomy and Function Of Higher Olfactory Centresmentioning

confidence: 99%

Olfaction in vector-host interactions

Takken¹,

Knols²

2010

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Imaging of an Early Memory Trace in theDrosophilaMushroom Body

Cited by 127 publications

References 41 publications

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

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

Olfaction in vector-host interactions

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