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• W2076998521 abstract "Flies can form a visually-guided working memory. A new study shows that the gene termed ellipsoid body open influences multiple signals to regulate a competence factor in the ellipsoid body to support normal working memory. Flies can form a visually-guided working memory. A new study shows that the gene termed ellipsoid body open influences multiple signals to regulate a competence factor in the ellipsoid body to support normal working memory. It’s an age-old problem, trying to navigate through rough terrain with intermittent landmarks. You pick a target, say a tall tree, and walk toward it, only to have the tree disappear as you move down into a ravine. There is an idea of the right direction, and with some level of error, you can predict pretty well the proper track back to the target. Humans can do this. Impressively, some seemingly simple animals can also use a working memory to re-orient toward a lost target. A new study by Roland Strauss and colleagues [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar] reported in this issue of Current Biology demonstrates that the fruit fly Drosophila melanogaster can use visual landmarks to establish a seconds-long working memory and elucidates a novel cellular and neural circuit mechanism to support this type of memory. Here is the first sleight: tricking flies into showing that they have a visually-guided working memory. Evidence for this type of memory can be seen in individual flies in the so-called disappearing landmark paradigm. In this test, a single fly is put in a circular arena, about the size of an end table, which is lined with LED lights controlled by a computer [2Neuser K. Triphan T. Mronz M. Poeck B. Strauss R. Analysis of a spatial orientation memory in Drosophila.Nature. 2008; 453: 1244-1247Crossref PubMed Scopus (278) Google Scholar]. If the arena is uniformly lit, the fly will walk around in random directions [2Neuser K. Triphan T. Mronz M. Poeck B. Strauss R. Analysis of a spatial orientation memory in Drosophila.Nature. 2008; 453: 1244-1247Crossref PubMed Scopus (278) Google Scholar, 3Ofstad T.A. Zuker C.S. Reiser M.B. Visual place learning in Drosophila melanogaster.Nature. 2011; 474: 204-207Crossref PubMed Scopus (269) Google Scholar]. If, however, two vertical dark bars are placed at 180 degrees from each other, then the fly starts to walk back and forth between the two landmarks. A fly will walk between the landmarks in this modification of the Buridan Paradigm for hours, approaching first one landmark then turning around and going to the other [2Neuser K. Triphan T. Mronz M. Poeck B. Strauss R. Analysis of a spatial orientation memory in Drosophila.Nature. 2008; 453: 1244-1247Crossref PubMed Scopus (278) Google Scholar, 4Buelthoff H. Goetz K.G. Herre M. Recurrent inversion of visual orientation in the walking fly Drosophila melanogaster.J. Comp. Physiol. A. 1982; 148: 471-482Crossref Scopus (52) Google Scholar] (Figure 1A). Now, if a distracting landmark appears on the surface of the arena, a fly will orient toward the new stripe (Figure 1B). When the distracting landmark and the original target are then removed, analogous to walking down into the ravine, a fly will re-orient toward the original, but now absent target. Flies will go back to the original target if the distractor is present for less than four seconds, suggesting that a seconds-long working memory allows a fly to re-orient toward a disappeared landmark (Figure 1C). How does a fly form this visual working memory? A first clue to the neural mechanism for this type of memory came from a mutant fly type that had a grossly misformed part of the brain. A mutation that alters the structure of the ellipsoid body, called ellipsoid body open (ebo), has provided ideas about multiple behaviors, including premotor behaviors (for example [5Pan Y. Zhou Y. Guo C. Gong H. Gong Z. Liu L. Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory.Learn. Mem. 2009; 16: 289-295Crossref PubMed Scopus (126) Google Scholar, 6Strauss R. Heisenberg M. A higher control center of locomotor behavior in the Drosophila brain.J. Neurosci. 1993; 13: 1852-1861Crossref PubMed Google Scholar]). Among the abnormal behaviors of the mutant flies is a clear defect in visually guided working memory [2Neuser K. Triphan T. Mronz M. Poeck B. Strauss R. Analysis of a spatial orientation memory in Drosophila.Nature. 2008; 453: 1244-1247Crossref PubMed Scopus (278) Google Scholar]. What is surprising, however, is that although the ebo gene is acting in the ellipsoid body (more on this brain structure next), its critical role in working memory is independent of the structural change in this brain structure seen in the mutant flies [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar]. It turns out that the structural change in the ellipsoid body of the ebo mutant brain, which suggested a function for the ebo gene in maintaining a normal neural structure for this working memory (Figure 1D), was a false lead. But nevertheless, the new work [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar] has revealed a novel mechanism for ebo function in behavior, providing insights into how a brain structure can function in visual working memory. The Drosophila central brain has on the order of a hundred thousand neurons, many of which can be recognized in organized neural structures [7Shinomiya K. Matsuda K. Oishi T. Otsuna H. Ito K. Flybrain neuron database: a comprehensive database system of the Drosophila brain neurons.J. Comp. Neurol. 2011; 519: 807-833Crossref PubMed Scopus (33) Google Scholar]. In addition to the mushroom bodies, a part of the fruit fly brain most commonly associated with olfactory memory, the central complex is a readily recognized core part of the brain [7Shinomiya K. Matsuda K. Oishi T. Otsuna H. Ito K. Flybrain neuron database: a comprehensive database system of the Drosophila brain neurons.J. Comp. Neurol. 2011; 519: 807-833Crossref PubMed Scopus (33) Google Scholar, 8Zars T. Short-term memories in Drosophila are governed by general and specific genetic systems.Learn. Mem. 2010; 17: 246-251Crossref PubMed Scopus (26) Google Scholar, 9Heisenberg M. Mushroom body memoir: from maps to models.Nat. Rev. Neurosci. 2003; 4: 266-275Crossref PubMed Scopus (930) Google Scholar]. The central complex is composed of four parts: the ellipsoid body, the fan-shaped body, the protocerebral bridge and the noduli. These structures are connected to each other and other parts of the brain via large-field neurons, suggesting that the central complex has some level of integrated function. Important in understanding the new results, the ellipsoid body is a ring-like structure, where the ring is formed by the dendritic arborization of a set of neurons called Ring (R) neurons, roughly divided into the R1–R4 neurons [10Renn S.C. Armstrong J.D. Yang M. Wang Z. An X. Kaiser K. Taghert P.H. Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex.J. Neurobiol. 1999; 41: 189-207Crossref PubMed Scopus (160) Google Scholar]. So, ebo mutant flies have a defective visually-guided working memory. What are the genetic and cellular bases for this deficit? The ebo gene has been shown to encode a nuclear export receptor protein called exportin 6 [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar]. A key feature of exportin 6 proteins is that they regulate the translocation of actin–profilin complexes from the nucleus to the cytoplasm [11Stuven T. Hartmann E. Gorlich D. Exportin 6: a novel nuclear export receptor that is specific for profilin.actin complexes.EMBO J. 2003; 22: 5928-5940Crossref PubMed Scopus (237) Google Scholar]. When examined, the ebo mutant flies had a higher level of actin in the nuclei of multiple cell types, including the R-neurons of the ellipsoid body. Remarkably, expression of exportin 6 in any of the R neuron types in otherwise ebo mutant flies restored the visual working memory to normal levels. That is, ebo mutant flies were shown to have a defective visual working memory; then 24 hours later with induction of expression of a normal version of the ebo gene in R neurons, the same flies had a normal memory. When the brains of the behaviorally rescued flies were examined, the gross structure of the ellipsoid body was found to be either normal or still aberrant. Thus, the structural abnormality of the ebo flies’ ellipsoid bodies is dissociated from the behavioral deficit, suggesting that a non-structural mechanism must be involved in ebo/exportin 6 regulation of visual working memory. It has been shown previously that accumulation of actin in the nucleus can interfere with transcriptional activity of the transcription regulator Serum Response Factor (SRF) by forming a complex with Myocardin-Related Transcription Factor (MTRF) [12Vartiainen M.K. Guettler S. Larijani B. Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL.Science. 2007; 316: 1749-1752Crossref PubMed Scopus (480) Google Scholar]. Moreover, SRF in mice and flies is important in consolidating memories in the tens of minutes to days range [13Donlea J.M. Ramanan N. Shaw P.J. Use-dependent plasticity in clock neurons regulates sleep need in Drosophila.Science. 2009; 324: 105-108Crossref PubMed Scopus (187) Google Scholar, 14Etkin A. Alarcon J.M. Weisberg S.P. Touzani K. Huang Y.Y. Nordheim A. Kandel E.R. A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context.Neuron. 2006; 50: 127-143Abstract Full Text Full Text PDF PubMed Scopus (176) Google Scholar]. Whether or not the Drosophila ortholog of SRF (dSRF), encoded by a gene termed blistered (bs), plays a role in visual working memory was tested [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar], and the bs mutant flies showed a severe deficit in a working memory. Additionally, as with the ebo mutants, it was possible to rescue the seconds-long memory defect of bs mutants by expressing the wild-type dSRF in any of the ellipsoid body R neurons. Consistent with this type of memory mechanism being independent of a structural change in the brain, the bs mutant flies have a normal ellipsoid body. Finally, a genetic interaction between mutations of the ebo and MRTF genes was tested [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar]. Double heterozygous mutant flies for these genes were found to have reduced visual working memory. Again, these double mutants had normal looking ellipsoid bodies. Thus, the ebo/exportin 6 gene led to the discovery that dSRF and MRTF gene products are also important for a seconds-long working memory. The discovery that the ebo/exportin 6 and dSRF proteins function in redundant sets of R-neurons in the ellipsoid body for a visual working memory suggests that the R-neurons provide a competence factor that allows the ellipsoid body to function correctly (Figure 1E,F) [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar]. The discovery of a redundant sufficient action of ebo/exportin 6 and dSRF in different sets of neurons for a behavior is a rare finding, and suggests that the typical search for cell-autonomous gene action for behaviors only provides a part of the story for how the brain works. Identification of the competence factor will be of high interest in determining how neurons within a structure can make the whole structure functionally normal. That the ebo/exportin 6, dSRF, and MRTF signaling cassette is important for a seconds-long visual working memory is also of note. Previous studies in mouse and fly had shown that these gene products are critical for memory in a much longer time domain [13Donlea J.M. Ramanan N. Shaw P.J. Use-dependent plasticity in clock neurons regulates sleep need in Drosophila.Science. 2009; 324: 105-108Crossref PubMed Scopus (187) Google Scholar, 14Etkin A. Alarcon J.M. Weisberg S.P. Touzani K. Huang Y.Y. Nordheim A. Kandel E.R. A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context.Neuron. 2006; 50: 127-143Abstract Full Text Full Text PDF PubMed Scopus (176) Google Scholar]. Although there are only a few examples so far, it may become more common that the time domain in which a gene acts depends on the behavioral test under investigation (for example [1Thran J. Poeck B. Strauss R. Serum response factor (SRF) mediated gene regulation in a Drosophila visual working memory.Curr. Biol. 2013; 23: 1756-1763Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar, 15LaFerriere H. Speichinger K. Stromhaug A. Zars T. The radish gene reveals a memory component with variable temporal properties.PLoS ONE. 2011; 6: e24557Crossref PubMed Scopus (10) Google Scholar, 16Krashes M.J. Waddell S. Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila.J. Neurosci. 2008; 28: 3103-3113Crossref PubMed Scopus (196) Google Scholar]). Finally, the discovery of the ebo/exportin 6 signaling mechanism should be reconciled with the other known signaling mechanisms in visual working memory. An S6 kinase II (S6KII) and a cGMP-dependent protein kinase (PKG) have been shown previously to work in R-neurons of the ellipsoid body for a visual working memory [2Neuser K. Triphan T. Mronz M. Poeck B. Strauss R. Analysis of a spatial orientation memory in Drosophila.Nature. 2008; 453: 1244-1247Crossref PubMed Scopus (278) Google Scholar, 17Kuntz S. Poeck B. Sokolowski M.B. Strauss R. The visual orientation memory of Drosophila requires Foraging (PKG) upstream of Ignorant (RSK2) in ring neurons of the central complex.Learn. Mem. 2012; 19: 337-340Crossref PubMed Scopus (44) Google Scholar]. Do the S6KII and PKG signals influence exportin 6 activity, or other components of this pathway? Or, could the postulated competence factor be acting on these kinase signals? Regardless of the open questions, the discovery of ebo/exportin 6, dSRF, and MRTF mechanisms of influencing a visual working memory will change our understanding of working memory mechanisms, timing properties for signaling cascades in behavior, and the organizational features of brain structures. Serum Response Factor-Mediated Gene Regulation in a Drosophila Visual Working MemoryThran et al.Current BiologySeptember 5, 2013In BriefNavigation through the environment requires a working memory for the chosen target and path integration facilitating an approach when the target becomes temporarily hidden. We have previously shown that this visual orientation memory resides in the ellipsoid body, which is part of the central complex in the Drosophila brain. Former analysis of foraging and ignorant mutants have revealed that a hierarchical PKG and RSKII kinase signaling cascade in a subset of the ellipsoid-body ring neurons is required for this type of working memory in flies. Full-Text PDF Open Archive" @default.
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• W2076998521 title "Visual Working Memory: Now You See It, Now You Don’t" @default.
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