Heterotypic Gap Junctions between Two Neurons in the Drosophila Brain Are Critical for Memory

Wu, Chia‐Lin; Shih, Min-Yi; Lai, Jason Sih-Yu; Yang, Hsiang‐Yu; Turner, Glenn; Chen, Linyi; Chiang, Ann‐Shyn

doi:10.1016/j.cub.2011.02.041

Cited by 105 publications

(112 citation statements)

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“…Olfactory aversive learning and memory tests were performed using a standard T-maze paradigm (Tully and Quinn, 1985;Zhang et al, 2008). Briefly, 2-to 5-d-old flies were collected and grouped (ϳ100 per vial), and training and testing were performed the next day.…”

Section: Methodsmentioning

confidence: 99%

“…In addition, two pairs of MB intrinsic neurons, the dorsal paired medial (DPM) and the anterior paired lateral (APL) neurons, have been reported to play a role in the modulation of ASM (Waddell et al, 2000;Keene et al, 2006). DPM neurons are suggested to both receive from and transmit to MB neurons and are involved in 3 h memory consolidation (Keene et al, 2006), whereas APL-DPM heterotypic gap junctions are required for 3 h ASM formation (Wu et al, 2011). Whether there are other structures outside of the MB involved in the modulation of ASM is still unclear.…”

Section: Introductionmentioning

confidence: 99%

“…We thus wondered whether these GABAergic EB neurons modulate olfactory memory via direct connections with the MB, similar to GABAergic APL neurons (Liu et al, 2007(Liu et al, , 2009Pitman et al, 2011;Wu et al, 2011). To examine the spatial relationship in detail, we combined c819-GAL4ϾmEGFP with MB247-DsRED in one fly strain (Riemensperger et al, 2005) to express green and red fluorescent proteins in these two structures, respectively.…”

Section: Grasp Signals Suggest Direct Connections Between Mb247 and Cmentioning

confidence: 99%

“…The neural circuits of ASM As a component of MTM, ASM has been suggested to be stored in the MB and to be modulated by MB intrinsic APL and DPM neurons (Wu et al, 2011), of which the neural terminals are restricted to the MB (Tanaka et al, 2008). Here we report the EB, a brain structure separate from the MB, is also involved in the modulation of ASM.…”

Section: The Function Of Eb Gabaergic Neurons In Olfactory Memorymentioning

confidence: 99%

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Two Clusters of GABAergic Ellipsoid Body Neurons Modulate Olfactory Labile Memory inDrosophila

Zhang

Guo

et al. 2013

J. Neurosci.

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In Drosophila, aversive olfactory memory is believed to be stored in a prominent brain structure, the mushroom body (MB), and two pairs of MB intrinsic neurons, the dorsal paired medial (DPM) and the anterior paired lateral (APL) neurons, are found to regulate the consolidation of middle-term memory (MTM). Here we report that another prominent brain structure, the ellipsoid body (EB), is also involved in the modulation of olfactory MTM. Activating EB R2/R4m neurons does not affect the learning index, but specifically eliminates anesthesia-sensitive memory (ASM), the labile component of olfactory MTM. We further demonstrate that approximately two-thirds of these EB neurons are GABAergic and are responsible for the suppression of ASM. Using GRASP (GFP reconstitution across synaptic partners), we reveal potential synaptic connections between the EB and MB in regions covering both the presynaptic and postsynaptic sites of EB neurons, suggesting the presence of bidirectional connections between these two important brain structures. These findings suggest the existence of direct connections between the MB and EB, and provide new insights into the neural circuit basis for olfactory labile memory in Drosophila.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Grasp Signals Suggest Direct Connections Between Mb247 and Cmentioning

confidence: 99%

Section: The Function Of Eb Gabaergic Neurons In Olfactory Memorymentioning

confidence: 99%

See 2 more Smart Citations

Two Clusters of GABAergic Ellipsoid Body Neurons Modulate Olfactory Labile Memory inDrosophila

Zhang

Guo

et al. 2013

J. Neurosci.

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“…Although, to our knowledge, no evidence indicates different MB neurons can form any synaptic connection at MB lobe region, one recent study does show the output from Kenyon cells transmits back to other compartments of MB through the presynaptic sites in calyx (Christiansen et al, 2011). Also, MB α/β subdivisions might communicate with each other through feedback loops constructed by various MB extrinsic neurons, such as DPM neurons and APL neurons (Lee et al, 1999;Keene et al, 2006;Wu et al, 2011;Pitman et al, 2011). Another possibility is that MB α/β subdivisions, being parallel with each other, release neurotransmitters to their common downstream neurons suggested for LTM storage, such as the DAL neurons (Chen et al, 2012) MB-V2 neurons (Séjourné et al, 2011), MB-V3 neurons (Pai et al, 2013) and the ellipsoid body (Wu et al, 2007), to regulate formation, consolidation and retrieval of LTM separately.…”

Section: Discussionmentioning

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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Localization of the Contacts Between Kenyon Cells and Aminergic Neurons in the Drosophila melanogaster Brain Using SplitGFP Reconstitution

Pech

Pooryasin

Birman

et al. 2013

J of Comparative Neurology

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The mushroom body of the insect brain represents a neuronal circuit involved in the control of adaptive behavior, e.g., associative learning. Its function relies on the modulation of Kenyon cell activity or synaptic transmitter release by biogenic amines, e.g., octopamine, dopamine, or serotonin. Therefore, for a comprehensive understanding of the mushroom body, it is of interest not only to determine which modulatory neurons interact with Kenyon cells but also to pinpoint where exactly in the mushroom body they do so. To accomplish the latter, we made use of the GRASP technique and created transgenic Drosophila melanogaster that carry one part of a membrane-bound splitGFP in Kenyon cells, along with a cytosolic red fluorescent marker. The second part of the splitGFP is expressed in distinct neuronal populations using cell-specific Gal4 drivers. GFP is reconstituted only if these neurons interact with Kenyon cells in close proximity, which, in combination with two-photon microscopy, provides a very high spatial resolution. We characterize spatially and microstructurally distinct contact regions between Kenyon cells and dopaminergic, serotonergic, and octopaminergic/tyraminergic neurons in all subdivisions of the mushroom body. Subpopulations of dopaminergic neurons contact complementary lobe regions densely. Octopaminergic/tyraminergic neurons contact Kenyon cells sparsely and are restricted mainly to the calyx, the α'-lobes, and the γ-lobes. Contacts of Kenyon cells with serotonergic neurons are heterogeneously distributed over the entire mushroom body. In summary, the technique enables us to localize precisely a segmentation of the mushroom body by differential contacts with aminergic neurons.

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Heterotypic Gap Junctions between Two Neurons in the Drosophila Brain Are Critical for Memory

Cited by 105 publications

References 50 publications

Two Clusters of GABAergic Ellipsoid Body Neurons Modulate Olfactory Labile Memory inDrosophila

Two Clusters of GABAergic Ellipsoid Body Neurons Modulate Olfactory Labile Memory inDrosophila

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

Localization of the Contacts Between Kenyon Cells and Aminergic Neurons in the Drosophila melanogaster Brain Using SplitGFP Reconstitution

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