For Publishers
DiscoveryMetadataPeer reviewHostingPublishing
For Researchers
JoinPublishReviewCollect
Register
Blog
About
Search
Advanced search
My ScienceOpen
Search
For Publishers
For Researchers
Blog
About
14
views
35
references
 Top references
cited by
25
    
0 reviews
 Review
0
comments
 Comment
0
recommends
+1 Recommend
0 collections
    0
    shares
      109
      similar
       All similar
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Gap junction networks in mushroom bodies participate in visual learning and memory in Drosophila

      research-article

      Read this article at

      ScienceOpenPublisherPMC
      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Gap junctions are widely distributed in the brains across species and play essential roles in neural information processing. However, the role of gap junctions in insect cognition remains poorly understood. Using a flight simulator paradigm and genetic tools, we found that gap junctions are present in Drosophila Kenyon cells (KCs), the major neurons of the mushroom bodies (MBs), and showed that they play an important role in visual learning and memory. Using a dye coupling approach, we determined the distribution of gap junctions in KCs. Furthermore, we identified a single pair of MB output neurons (MBONs) that possess a gap junction connection to KCs, and provide strong evidence that this connection is also required for visual learning and memory. Together, our results reveal gap junction networks in KCs and the KC-MBON circuit, and bring new insight into the synaptic network underlying fly’s visual learning and memory.

          DOI: http://dx.doi.org/10.7554/eLife.13238.001

          Related collections

          Most cited references35

          • Record: found
          • Abstract: found
          • Article: not found

          Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast.

          Lobin Lee, Yu Luo, Belinda Lee (1999)
          The mushroom bodies (MBs) are prominent structures in the Drosophila brain that are essential for olfactory learning and memory. Characterization of the development and projection patterns of individual MB neurons will be important for elucidating their functions. Using mosaic analysis with a repressible cell marker (Lee, T. and Luo, L. (1999) Neuron 22, 451-461), we have positively marked the axons and dendrites of multicellular and single-cell mushroom body clones at specific developmental stages. Systematic clonal analysis demonstrates that a single mushroom body neuroblast sequentially generates at least three types of morphologically distinct neurons. Neurons projecting into the (gamma) lobe of the adult MB are born first, prior to the mid-3rd instar larval stage. Neurons projecting into the alpha' and beta' lobes are born between the mid-3rd instar larval stage and puparium formation. Finally, neurons projecting into the alpha and beta lobes are born after puparium formation. Visualization of individual MB neurons has also revealed how different neurons acquire their characteristic axon projections. During the larval stage, axons of all MB neurons bifurcate into both the dorsal and medial lobes. Shortly after puparium formation, larval MB neurons are selectively pruned according to birthdays. Degeneration of axon branches makes early-born gamma neurons retain only their main processes in the peduncle, which then project into the adult gamma lobe without bifurcation. In contrast, the basic axon projections of the later-born (alpha'/beta') larval neurons are preserved during metamorphosis. This study illustrates the cellular organization of mushroom bodies and the development of different MB neurons at the single cell level. It allows for future studies on the molecular mechanisms of mushroom body development.
          Article 0 comments Cited 154 times – based on 0 reviews     Review now
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe.

            Rachel Wilson, Gilles Laurent (2005)
            Drosophila olfactory receptor neurons project to the antennal lobe, the insect analog of the mammalian olfactory bulb. GABAergic synaptic inhibition is thought to play a critical role in olfactory processing in the antennal lobe and olfactory bulb. However, the properties of GABAergic neurons and the cellular effects of GABA have not been described in Drosophila, an important model organism for olfaction research. We have used whole-cell patch-clamp recording, pharmacology, immunohistochemistry, and genetic markers to investigate how GABAergic inhibition affects olfactory processing in the Drosophila antennal lobe. We show that many axonless local neurons (LNs) in the adult antennal lobe are GABAergic. GABA hyperpolarizes antennal lobe projection neurons (PNs) via two distinct conductances, blocked by a GABAA- and GABAB-type antagonist, respectively. Whereas GABAA receptors shape PN odor responses during the early phase of odor responses, GABAB receptors mediate odor-evoked inhibition on longer time scales. The patterns of odor-evoked GABAB-mediated inhibition differ across glomeruli and across odors. Finally, we show that LNs display broad but diverse morphologies and odor preferences, suggesting a cellular basis for odor- and glomerulus-dependent patterns of inhibition. Together, these results are consistent with a model in which odors elicit stimulus-specific spatial patterns of GABA release, and as a result, GABAergic inhibition increases the degree of difference between the neural representations of different odors.
            Article 0 comments Cited 133 times – based on 0 reviews     Review now
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons.

              G Tamas, E Buhl, A Lorincz … (2000)
              Networks of GABAergic interneurons are implicated in synchronizing cortical activity at gamma frequencies (30-70 Hz). Here we demonstrate that the combined electrical and GABAergic synaptic coupling of basket cells instantaneously entrained gamma-frequency postsynaptic firing in layers 2/3 of rat somatosensory cortex. This entrainment was mediated by rapid curtailment of gap junctional coupling potentials by GABAA receptor-mediated IPSPs. Electron microscopy revealed spatial proximity of gap junctions and GABAergic synapses on somata and dendrites. Electrical coupling alone entrained postsynaptic firing with a phase lag, whereas unitary GABAergic connections were ineffective in gamma-frequency phasing. These observations demonstrate precise spatiotemporal mechanisms underlying action potential timing in oscillating interneuronal networks.
              Article 0 comments Cited 129 times – based on 0 reviews     Review now
                Bookmark
                All references

                Author and article information

                Contributors
                K VijayRaghavan: Role: Reviewing editor
                Journal
                Journal ID (nlm-ta): eLife
                Journal ID (iso-abbrev): Elife
                Journal ID (hwp): eLife
                Journal ID (publisher-id): eLife
                Title: eLife
                Publisher: eLife Sciences Publications, Ltd
                ISSN (Electronic): 2050-084X
                Publication date (Electronic, pub): 24 May 2016
                Publication date Collection: 2016
                Volume: 5
                Electronic Location Identifier: e13238
                Affiliations
                [1 ]deptState Key Laboratory of Brain and Cognitive Science, Institute of Biophysics , Chinese Academy of Sciences , Beijing, China
                [2 ]University of Chinese Academy of Sciences , Beijing, China
                [3 ]deptInstitute of Neuroscience, State Key Laboratory of Neuroscience , CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, CAS , Shanghai, China
                [4]Tata Institute of Fundamental Research , India
                [5]Tata Institute of Fundamental Research , India
                Author notes
                [†]

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-6710-0012
                http://orcid.org/0000-0002-6515-7944
                Article
                Publisher ID: 13238
                DOI: 10.7554/eLife.13238
                PMC ID: 4909397
                PubMed ID: 27218450
                SO-VID: fcf7bb99-f300-403f-8845-ea75e750ff86
                Copyright © © 2016, Liu et al
                License:

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                Date received : 20 November 2015
                Date accepted : 20 May 2016
                Funding
                No external funding was received for this work.
                Categories
                Subject: Neuroscience
                Subject: Research Article
                Custom metadata
                elife-xml-version 2.5
                Author impact statement Gap junctions exist in Kenyon cells and Kenyon cell-mushroom body output neuron neural networks, and are also critical in visual learning and memory in Drosophila

                ScienceOpen disciplines: Life sciences
                Keywords: gap junctions,optogenetics,visual learning and memory,d. melanogaster
                Data availability:
                ScienceOpen disciplines: Life sciences
                Keywords: gap junctions, optogenetics, visual learning and memory, d. melanogaster

                Comments

                Comment on this article

                scite_

                Similar content109

                See all similar

                Cited by25

                See all cited by

                Most referenced authors499

                See all reference authors