
Visual place learning in drosophila melanogaster
- Select a language for the TTS:
- UK English Female
- UK English Male
- US English Female
- US English Male
- Australian Female
- Australian Male
- Language selected: (auto detect) - EN
Play all audios:
ABSTRACT The ability of insects to learn and navigate to specific locations in the environment has fascinated naturalists for decades. The impressive navigational abilities of ants, bees,
wasps and other insects demonstrate that insects are capable of visual place learning1,2,3,4, but little is known about the underlying neural circuits that mediate these behaviours.
_Drosophila melanogaster_ (common fruit fly) is a powerful model organism for dissecting the neural circuitry underlying complex behaviours, from sensory perception to learning and memory.
_Drosophila_ can identify and remember visual features such as size, colour and contour orientation5,6. However, the extent to which they use vision to recall specific locations remains
unclear. Here we describe a visual place learning platform and demonstrate that _Drosophila_ are capable of forming and retaining visual place memories to guide selective navigation. By
targeted genetic silencing of small subsets of cells in the _Drosophila_ brain, we show that neurons in the ellipsoid body, but not in the mushroom bodies, are necessary for visual place
learning. Together, these studies reveal distinct neuroanatomical substrates for spatial versus non-spatial learning, and establish _Drosophila_ as a powerful model for the study of spatial
memories. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to
this journal Receive 51 print issues and online access $199.00 per year only $3.90 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy
now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer
support SIMILAR CONTENT BEING VIEWED BY OTHERS GENETIC ATLAS OF HYGRO-AND THERMOSENSORY CELLS IN THE VINEGAR FLY _DROSOPHILA MELANOGASTER_ Article Open access 14 September 2023
CONNECTOME-DRIVEN NEURAL INVENTORY OF A COMPLETE VISUAL SYSTEM Article Open access 26 March 2025 ETHANOL-GUIDED BEHAVIOR IN _DROSOPHILA_ LARVAE Article Open access 10 June 2021 REFERENCES *
Mizunami, M., Weibrecht, J. M. & Strausfeld, N. J. Mushroom bodies of the cockroach: their participation in place memory. _J. Comp. Neurol._ 402, 520–537 (1998) Article CAS PubMed
Google Scholar * Wessnitzer, J., Mangan, M. & Webb, B. Place memory in crickets. _Proc. R. Soc. B_ 275, 915–921 (2008) Article PubMed PubMed Central Google Scholar * Wehner, R.
& Raber, F. Visual spatial memory in desert ants, _Cataglyphis bicolor_ (Hymenoptera: Formicidae). _Experientia_ 35, 1569–1571 (1979) Article Google Scholar * Cartwright, B. A. &
Collett, T. S. How honey bees use landmarks to guide their return to a food source. _Nature_ 295, 560–564 (1982) Article ADS Google Scholar * Ernst, R. & Heisenberg, M. The memory
template in _Drosophila_ pattern vision at the flight simulator. _Vision Res._ 39, 3920–3933 (1999) Article CAS PubMed Google Scholar * Tang, S. & Guo, A. Choice behavior of
_Drosophila_ facing contradictory visual cues. _Science_ 294, 1543–1547 (2001) Article ADS CAS PubMed Google Scholar * Capaldi, E. A. & Dyer, F. C. The role of orientation flights
on homing performance in honeybees. _J. Exp. Biol._ 202, 1655–1666 (1999) CAS PubMed Google Scholar * Moser, E. I., Kropff, E. & Moser, M. B. Place cells, grid cells, and the brain’s
spatial representation system. _Annu. Rev. Neurosci._ 31, 69–89 (2008) Article CAS PubMed Google Scholar * Morris, R. G. M. Spatial localization does not require the presence of local
cues. _Learn. Motiv._ 12, 239–260 (1981) Article Google Scholar * Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T. & Bate, M. Altered electrical properties in _Drosophila_
neurons developing without synaptic transmission. _J. Neurosci._ 21, 1523–1531 (2001) Article CAS PubMed PubMed Central Google Scholar * McGuire, S. E., Mao, Z. & Davis, R. L.
Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in _Drosophila_ . _Sci. STKE_ 2004, pl6 (2004) PubMed Google Scholar * Waddell, S. & Quinn, W. G. What
can we teach _Drosophila_? What can they teach us? _Trends Genet._ 17, 719–726 (2001) Article CAS PubMed Google Scholar * de Belle, J. S. & Heisenberg, M. Associative odor learning
in _Drosophila_ abolished by chemical ablation of mushroom bodies. _Science_ 263, 692–695 (1994) Article ADS CAS PubMed Google Scholar * Wolf, R. et al. _Drosophila_ mushroom bodies are
dispensable for visual, tactile, and motor learning. _Learn. Mem._ 5, 166–178 (1998) CAS PubMed PubMed Central Google Scholar * Putz, G. & Heisenberg, M. Memories in _Drosophila_
heat-box learning. _Learn. Mem._ 9, 349–359 (2002) Article PubMed PubMed Central Google Scholar * Heisenberg, M. Mushroom body memoir: from maps to models. _Nature Rev. Neurosci._ 4,
266–275 (2003) Article CAS Google Scholar * Neuser, K., Triphan, T., Mronz, M., Poeck, B. & Strauss, R. Analysis of a spatial orientation memory in _Drosophila_ . _Nature_ 453,
1244–1247 (2008) Article ADS CAS PubMed Google Scholar * Strauss, R. The central complex and the genetic dissection of locomotor behaviour. _Curr. Opin. Neurobiol._ 12, 633–638 (2002)
Article CAS PubMed Google Scholar * Bernstein, S. & Bernstein, R. A. Relationships between foraging efficiency and size of head and component brain and sensory structures in red wood
ant. _Brain Res._ 16, 85–104 (1969) Article CAS PubMed Google Scholar * Fahrbach, S. E. & Robinson, G. E. Behavioral development in the honey bee: toward the study of learning under
natural conditions. _Learn. Mem._ 2, 199–224 (1995) Article CAS PubMed Google Scholar * Stocker, R. F. The organization of the chemosensory system in _Drosophila melanogaster_: a
review. _Cell Tissue Res._ 275, 3–26 (1994) Article CAS PubMed Google Scholar * Tully, T. & Quinn, W. G. Classical conditioning and retention in normal and mutant _Drosophila
melanogaster_ . _J. Comp. Physiol. A_ 157, 263–277 (1985) Article CAS PubMed Google Scholar * Wustmann, G., Rein, K., Wolf, R. & Heisenberg, M. A new paradigm for operant
conditioning of _Drosophila melanogaster_ . _J. Comp. Physiol. A_ 179, 429–436 (1996) Article CAS PubMed Google Scholar * Zars, T. Spatial orientation in _Drosophila_ . _J. Neurogenet._
23, 104–110 (2009) Article PubMed Google Scholar * Morris, R. G., Schenk, F., Tweedie, F. & Jarrard, L. E. Ibotenate lesions of hippocampus and/or subiculum: dissociating components
of allocentric spatial learning. _Eur. J. Neurosci._ 2, 1016–1028 (1990) Article PubMed Google Scholar * Seelig, J. D. et al. Two-photon calcium imaging from head-fixed _Drosophila_
during optomotor walking behavior. _Nature Methods_ 7, 535–540 (2010) Article CAS PubMed PubMed Central Google Scholar * Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L. &
Tank, D. W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. _Nature Neurosci._ 13, 1433–1440 (2010) Article CAS PubMed Google Scholar *
Foucaud, J., Burns, J. G. & Mery, F. Use of spatial information and search strategies in a water maze analog in Drosophila melanogaster. _PLoS ONE_ 5, e15231 (2010) Article ADS CAS
PubMed PubMed Central Google Scholar * Reiser, M. B. & Dickinson, M. H. A modular display system for insect behavioral neuroscience. _J. Neurosci. Methods_ 167, 127–139 (2008) Article
PubMed Google Scholar * Branson, K., Robie, A. A., Bender, J., Perona, P. & Dickinson, M. H. High-throughput ethomics in large groups of Drosophila. _Nature Methods_ 6, 451–457
(2009) Article CAS PubMed PubMed Central Google Scholar * Sayeed, O. & Benzer, S. Behavioral genetics of thermosensation and hygrosensation in Drosophila. _Proc. Natl Acad. Sci.
USA_ 93, 6079–6084 (1996) Article ADS CAS PubMed PubMed Central Google Scholar * Zars, T. Two thermosensors in Drosophila have different behavioral functions. _J. Comp. Physiol. A_
187, 235–242 (2001) Article CAS PubMed Google Scholar * Strauss, R., Schuster, S. & Gotz, K. G. Processing of artificial visual feedback in the walking fruit fly Drosophila
melanogaster. _J. Exp. Biol._ 200, 1281–1296 (1997) CAS PubMed Google Scholar * Wustmann, G. & Heisenberg, M. Behavioral manipulation of retrieval in a spatial memory task for
Drosophila melanogaster. _Learn. Mem._ 4, 328–336 (1997) Article CAS PubMed Google Scholar * Zars, T., Wolf, R., Davis, R. & Heisenberg, M. Tissue-specific expression of a type I
adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. _Learn. Mem._ 7, 18–31 (2000) Article CAS PubMed PubMed Central Google Scholar * Diegelmann, S.,
Zars, M. & Zars, T. Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila. _Learn. Mem._ 13, 72–83 (2006) Article PubMed
PubMed Central Google Scholar * Dickinson, M. H. Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster. _Phil. Trans R. Soc. B_ 354, 903–916 (1999) Article CAS
PubMed PubMed Central Google Scholar * de Belle, J. S. & Heisenberg, M. Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the
mushroom body miniature gene (mbm). _Proc. Natl Acad. Sci. USA_ 93, 9875–9880 (1996) Article ADS CAS PubMed PubMed Central Google Scholar * Pfeiffer, B. D. et al. Tools for
neuroanatomy and neurogenetics in Drosophila. _Proc. Natl Acad. Sci. USA_ 105, 9715–9720 (2008) Article ADS CAS PubMed PubMed Central Google Scholar * Martin, J. R., Raabe, T. &
Heisenberg, M. Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. _J. Comp. Physiol. A_ 185, 277–288 (1999) Article CAS PubMed
Google Scholar Download references ACKNOWLEDGEMENTS We particularly thank M. Gallio for help with thermosensation and the development of temperature behavioural tests. We also thank G.
Rubin for providing _GAL4_ lines before publication, A. Jenett for their anatomical annotation and M. Dickinson for discussions and advice. Brain images were provided by the Janelia Fly
Light Project. T. Laverty and the Janelia Fly Core assisted with _Drosophila_ maintenance. Additional support was provided by J. Osborne, C. Werner, D. Olbris and M. Bolstad. We also thank
V. Jayaraman, members of the Reiser and Zuker labs, Janelia Farm colleagues and the Janelia Fly Olympiad Project. This project was supported through the HHMI Janelia Farm Research Campus
visitor programmed (T.A.O. and C.S.Z., hosted by M.B.R.). C.S.Z. is a HHMI investigator and a Senior Fellow at Janelia Farm. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Janelia Farm
Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA , Tyler A. Ofstad, Charles S. Zuker & Michael B. Reiser * Department of Neurosciences,
Howard Hughes Medical Institute, University of California at San Diego, La Jolla, 92093-0649, California, USA Tyler A. Ofstad & Charles S. Zuker * Department of Neurobiology, Howard
Hughes Medical Institute, University of California at San Diego, La Jolla, 92093-0649, California, USA Charles S. Zuker * Department of Biochemistry and Molecular Biophysics, Howard Hughes
Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, 10032, New York, USA Charles S. Zuker * Department of Neuroscience, Howard Hughes Medical
Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, 10032, New York, USA Charles S. Zuker Authors * Tyler A. Ofstad View author publications You can also
search for this author inPubMed Google Scholar * Charles S. Zuker View author publications You can also search for this author inPubMed Google Scholar * Michael B. Reiser View author
publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS All authors designed the study and wrote the manuscript. T.A.O. carried out the experiments and data
analysis. CORRESPONDING AUTHORS Correspondence to Charles S. Zuker or Michael B. Reiser. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests.
SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION The file contains Supplementary Figures 1-8 with legends and Supplementary Movie legends. (PDF 5727 kb) SUPPLEMENTARY MOVIE 1 The movie
shows a typical trial of place learning in the thermal visual arena (see Supplementary Information file for full legend). (MOV 10627 kb) SUPPLEMENTARY MOVIE 2 The movie shows a typical probe
trial following training with a coupled visual panorama (see Supplementary Information file for full legend). (MOV 3707 kb) SUPPLEMENTARY MOVIE 3 This movie shows a typical probe trail
following training with an uncoupled visual panorama (see Supplementary Information file for full legend). (MOV 3414 kb) POWERPOINT SLIDES POWERPOINT SLIDE FOR FIG. 1 POWERPOINT SLIDE FOR
FIG. 2 POWERPOINT SLIDE FOR FIG. 3 POWERPOINT SLIDE FOR FIG. 4 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Ofstad, T., Zuker, C. & Reiser, M.
Visual place learning in _Drosophila melanogaster_. _Nature_ 474, 204–207 (2011). https://doi.org/10.1038/nature10131 Download citation * Received: 28 October 2010 * Accepted: 14 April 2011
* Published: 08 June 2011 * Issue Date: 09 June 2011 * DOI: https://doi.org/10.1038/nature10131 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content:
Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative