Neural dynamics for landmark orientation and angular path integration

Nature

Volumn 521, Issue 7551, 2015, Pages 186-191

  Seelig, Johannes D ^a   Jayaraman, Vivek ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BRAIN; CALCIUM; DARK; FLY; MAMMAL; MEMORY;

ANGULAR PATH INTEGRATION; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BRAIN NERVE CELL; DENDRITE; DROSOPHILA MELANOGASTER; LANDMARK ORIENTATION; MENTAL FUNCTION; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; SHORT TERM MEMORY; VISION; WALKING; ANIMAL; BRAIN; CYTOLOGY; DARKNESS; DEPTH PERCEPTION; FEMALE; HEAD; METABOLISM; NERVE CELL; PHOTOSTIMULATION; PHYSIOLOGY; ROTATION; SPATIAL ORIENTATION;

ANIMALIA; DROSOPHILA MELANOGASTER; MAMMALIA;

CALCIUM;

ANIMALS; BRAIN; CALCIUM; CUES; DARKNESS; DENDRITES; DROSOPHILA MELANOGASTER; FEMALE; HEAD; NEURONS; ORIENTATION; PHOTIC STIMULATION; ROTATION; SPACE PERCEPTION; SPATIAL NAVIGATION; WALKING;

EID: 84929379914     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14446     Document Type: Article

References (47)

1. Collett, T. S. & Graham, P. Animal navigation: Path integration, visual landmarks and cognitive maps. Curr. Biol. 14, R475-R477 (2004).
2. Mittelstaedt, M. L. & Mittelstaedt, H. Homing by path integration in a mammal. Naturwissenschaften 67, 566-567 (1980).
3. Taube, J. S., Muller, R. U. & Ranck, J. B. Head-direction cells recorded from the postsubiculum in freely moving rats. 1. Description and quantitative analysis. J. Neurosci. 10, 420-435 (1990).
4. Taube, J. S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181-207 (2007).
5. Huston, S. J. & Jayaraman, V. Studying sensorimotor integration in insects. Curr. Opin. Neurobiol. 21, 527-534 (2011).
6. Wehner, R. Desert ant navigation: how miniature brains solve complex tasks. J. Comp. Physiol. A 189, 579-588 (2003).
7. Collett, T. S. & Collett, M. Path integration in insects. Curr. Opin. Neurobiol. 10, 757-762 (2000).
8. Neuser, K., Triphan, T., Mronz, M., Poeck, B. & Strauss, R. Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244-1247 (2008).
9. Liu, G. et al. Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551-556 (2006).
10. Ofstad, T. A., Zuker, C. S. & Reiser, M. B. Visual place learning in Drosophila melanogaster. Nature 474, 204-207 (2011).
11. Strauss, R. The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12, 633-638 (2002).
12. Heinze, S. & Homberg, U. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315, 995-997 (2007).
13. Heinze, S. & Reppert, S. M. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345-358 (2011).
14. Pfeiffer, K. & Homberg, U. Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59, 165-184 (2014).
15. Guo, P. & Ritzmann, R. E. Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J. Exp. Biol. 216, 992-1002 (2013).
16. Kathman, N. D., Kesavan, M. & Ritzmann, R. E. Encoding wide-field motion and direction in the central complex of the cockroach Blaberus discoidalis. J. Exp. Biol. 217, 4079-4090 (2014).
17. Dombeck, D. A. & Reiser, M. B. Real neuroscience in virtual worlds. Curr. Opin. Neurobiol. 22, 3-10 (2012).
18. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
19. Seelig, J. D. et al. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nature Methods 7, 535-540 (2010).
20. Seelig, J. D. & Jayaraman, V. Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262-266 (2013).
21. Bausenwein, B., Muller, N. R. & Heisenberg, M. Behavior-dependent activity labeling in the central complex of Drosophila during controlled visual stimulation. J. Comp. Neurol. 340, 255-268 (1994).
22. Strauss, R. & Pichler, J. Persistence of orientation toward a temporarily invisible landmark in Drosophila melanogaster. J. Comp. Physiol. A 182, 411-423 (1998).
23. Jenett, A. et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2, 991-1001 (2012).
24. Wolff, T., Iyer, N. A. & Rubin, G. M. Neuroarchitecture and neuroanatomy of the Drosophila central complex: a GAL4-based dissection of protocerebral bridge neurons and circuits. J. Comp. Neurol. 523, 997-1037 (2015).
25. Hanesch, U., Fischbach, K. F. & Heisenberg, M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257, 343-366 (1989).
26. Lin, C. Y. et al. A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. Cell Rep. 3, 1739-1753 (2013).
27. Heinze, S., Gotthardt, S. & Homberg, U. Transformation of polarized light information in the central complex of the locust. J. Neurosci. 29, 11783-11793 (2009).
28. Mizumori, S. J. Y. & Williams, J. D. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 13, 4015-4028 (1993).
29. Laughlin, S. B. The role of sensory adaptation in the retina. J. Exp. Biol. 146, 39-62 (1989).
30. Bockhorst, T. & Homberg, U. Amplitude and dynamics of polarization-plane signaling in the central complex of the locust brain. J. Neurophysiol. http://dx.doi.org/10.1152/jn.00742.2014 (2015).
31. Young, J. M. & Armstrong, J. D. Structure of the adult central complex in Drosophila: organizationofdistinct neuronalsubsets. J. Comp. Neurol. 518, 1500-1524 (2010).
32. Zeil, J. Visual homing: an insect perspective. Curr. Opin. Neurobiol. 22, 285-293 (2012).
33. Koch, C. & Ullman, S. Shifts in selective visual attention: towards the underlying neural circuitry. Hum. Neurobiol. 4, 219-227 (1985).
34. Strausfeld, N. J. & Hirth, F. Deep homology of arthropod central complex and vertebrate basal ganglia. Science 340, 157-161 (2013).
35. Aksay, E. et al. Functional dissection of circuitry in a neural integrator. Nature Neurosci. 10, 494-504 (2007).
36. Durstewitz, D., Seamans, J. K. & Sejnowski, T. J. Neurocomputational models of working memory. Nature Neurosci. 3, 1184-1191 (2000).
37. Knierim, J. J. & Zhang, K. C. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35, 267-285 (2012).
38. Peyrache, A., Lacroix, M. M., Petersen, P. C. & Buzsaki, G. Internally organized mechanisms of the head direction sense. Nature Neurosci. 18, 569-575 (2015).
39. Arena, P., Maceo, S., Patané, L. & Strauss, R. A spiking network for spatial memory formation: towards a fly-inspired ellipsoid body model. Intl. Joint Conf. Neural Networks http://dx.doi.org/10.1109/IJCNN.2013.6706882 (2013).
40. Haferlach, T., Wessnitzer, J., Mangan, M. & Webb, B. Evolving a neural model of insect path integration. Adapt. Behav. 15, 273-287 (2007).
41. Yoshida, M. & Hasselmo, M. E. Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J. Neurosci. 29, 4945-4952 (2009).
42. Major, G. & Tank, D. Persistent neural activity: prevalence and mechanisms. Curr. Opin. Neurobiol. 14, 675-684 (2004).
43. Maimon, G., Straw, A. D. & Dickinson, M. H. Activeflight increases the gainofvisual motion processing in Drosophila. Nature Neurosci. 13, 393-399 (2010).
44. Pologruto, T. A., Sabatini, B. L. & Svoboda, K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003).
45. Reiser, M. B. & Dickinson, M. H. A modular display system for insect behavioral neuroscience. J. Neurosci. Methods 167, 127-139 (2008).
46. Bahl, A., Ammer, G., Schilling, T. & Borst, A. Object tracking in motion-blind flies. Nature Neurosci. 16, 730-738 (2013).
47. Berens, P. CircStat: A MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1-21 (2009).