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Salience modulates 20–30 Hz brain activity in Drosophila

Abstract

Fruit flies selectively orient toward the visual stimuli that are most salient in their environment. We recorded local field potentials (LFPs) from the brains of Drosophila melanogaster as they responded to the presentation of visual stimuli. Coupling of salience effects (odor, heat or novelty) to these stimuli modulated LFPs in the 20–30 Hz range by evoking a transient, selective increase. We demonstrated the association of these responses with behavioral tracking and initiated a genetic approach to investigating neural correlates of perception.

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Figure 1: Mapping the LFP signal to image position.
Figure 2: Attaching salience.
Figure 3: Selective 20–30 Hz response.
Figure 4: 20–30 Hz coherence.
Figure 5: Behavioral tracking and 20–30 Hz brain activity.
Figure 6: 20–30 Hz activity and tracking behavior in mutant strains.

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References

  1. Menzel, R. & Giurfa, M. Cognitive architecture of a mini-brain: the honeybee. Trends Cogn. Sci. 5, 62 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. Wadell, S. & Quinn, W.G. Flies, genes and learning. Annu. Rev. Neurosci. 24, 1283 (2001).

    Article  Google Scholar 

  3. Dill, M. & Heisenberg, M. Visual pattern memory without shape recognition. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 349, 143–152 (1994).

    Google Scholar 

  4. Liu, L., Wolf, R., Ernst, R. & Heisenberg, M. Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400, 753 (2001).

    Article  Google Scholar 

  5. Menzel, R. Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8, 53 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. Wang, Y. et al. Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body. Neuron 29, 267 (2001).

    Article  CAS  PubMed  Google Scholar 

  7. Fiala, A. et al. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr. Biol. 12, 1877 (2002).

    Article  CAS  PubMed  Google Scholar 

  8. Borst, A. & Haag, J. Neural networks in the cockpit of the fly. J. Comp. Physiol. A 188, 419 (2002).

    Article  CAS  Google Scholar 

  9. Egelhaaf, M. et al. Neural encoding of behaviourally relevant visual-motion information in the fly. Trends Neurosci. 25, 96 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Nitz, D.A., van Swinderen, B., Tononi, G. & Greenspan, R.J. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr. Biol. 12, 1934 (2002).

    Article  CAS  PubMed  Google Scholar 

  11. Lehmann, F. & Dickinson, M.H. The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. J. Exp. Biol. 200, 1133 (1997).

    CAS  PubMed  Google Scholar 

  12. Wolf, R. & Heisenberg, M. On the fine structure of yaw torque in visual flight orientation of Drosophila melanogaster. II. A temporally and spatially variable weighting function for the visual field. J. Comp. Physiol. A 140, 69 (1980).

    Article  Google Scholar 

  13. Guo, A. & Goetz, K.G. Association of visual objects and olfactory cues in Drosophila. Learn. Mem. 4, 192 (1997).

    Article  CAS  PubMed  Google Scholar 

  14. Wolf, R. & Heisenberg, M. Basic organization of operant behavior as revealed in Drosophila flight orientation. J. Comp. Physiol. A 169, 699 (1991).

    Article  CAS  PubMed  Google Scholar 

  15. Shaw, J., Cirelli, C., Greenspan, R.J. & Tononi, G. Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834 (2000).

    Article  CAS  PubMed  Google Scholar 

  16. Kaiser, W. & Steiner-Kaiser, J. Neuronal correlates of sleep, wakingness and arousal in a diurnal insect. Nature 301, 707 (1983).

    Article  CAS  PubMed  Google Scholar 

  17. Mimura, K. Discrimination of some visual patterns in Drosophila melanogaster. J. Comp. Physiol. 146, 229 (1982).

    Article  Google Scholar 

  18. Niebur, E., Hsiao, S.S. & Johnson, K.O. Synchrony: a neuronal mechanism for attentional selection? Curr. Opin. Neurobiol. 12, 190 (2002).

    Article  CAS  PubMed  Google Scholar 

  19. Chen, M.S. et al. Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583 (1991).

    Article  CAS  PubMed  Google Scholar 

  20. Kitamoto, T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81 (2001).

    Article  CAS  PubMed  Google Scholar 

  21. Hardie, R.C. et al. Calcium influx via TRP channels is required to maintain PIP2 levels in Drosophila photoreceptors. Neuron 30, 149 (2001).

    Article  CAS  PubMed  Google Scholar 

  22. Keller, A. et al. Targeted expression of tetanus neurotoxin interferes with behavioral responses to sensory input in Drosophila. J. Neurobiol. 50, 221 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. Loughney, K., Kreber, R. & Ganetzky, B. Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58, 1143 (1989).

    Article  CAS  PubMed  Google Scholar 

  24. Littleton, J.T. et al. Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron 21, 401 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Joiner, M.A. & Griffith, L.C. CaM kinase II and visual input modulate memory formation in the neuronal circuit controlling courtship conditioning. J. Neurosci. 17, 9384–9391 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kim, Y.T. & Wu, C.F. Allelic interactions at the shibire locus of Drosophila: effects on behavior. J. Neurogenet. 7, 1–14 (1990).

    Article  CAS  PubMed  Google Scholar 

  27. Gatti, S., Ferveur, J.F. & Martin, J.R. Genetic identification of neurons controlling a sexually dimorphic behaviour. Curr. Biol. 10, 667 (2000).

    Article  CAS  PubMed  Google Scholar 

  28. Connolly, J.B. et al. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104 (1996).

    Article  CAS  PubMed  Google Scholar 

  29. Joiner, M.A. & Griffith, L.C. Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn. Mem. 6, 177 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Wu, Z., Gong, Z., Feng, C. & Guo, A. An emergent mechanism of selective visual attention in Drosophila. Biol. Cyber. 82, 61 (2000).

    Article  CAS  Google Scholar 

  31. Wolf, R. et al. Drosophila mushroom bodies are dispensable for visual, tactile and motor learning. Learn. Mem. 5, 166 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Strausfeld, N.J. et al. Evolution, discovery and interpetations of arthropod mushroom bodies. Learn. Mem. 5, 11 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Collett, T.S. Some operating rules for the optomotor system of a hoverfly during voluntary flight. J. Comp. Physiol. A 138, 271 (1980).

    Article  Google Scholar 

  34. Goetz, K.G. Exploratory strategies in Drosophila. in Neural Basis of Behavioural Adaptations (eds. Schildberger, K. & Elsner, N.) 47–59 (International Symposium, Tutzing, Germany, 1994).

    Google Scholar 

  35. James, W. The Principles of Psychology (Henry Holt & Co., New York, 1890).

  36. Edelman, G.M. The Remembered Present (Basic Books, New York, 1989).

    Google Scholar 

  37. Crick, F.H.C. & Koch, C. Towards a neurobiological theory of consciousness. Semin. Neurosci. 2, 263 (1990).

    Google Scholar 

  38. Bushnell, P.J. Behavioral approaches to the assessment of attention in animals. Psychopharmacology (Berl.) 138, 231 (1998).

    Article  CAS  Google Scholar 

  39. Engel, A.K. & Singer, W. Temporal binding and the neural correlates of sensory awareness. Trends Cogn. Sci. 5, 16 (2001).

    Article  PubMed  Google Scholar 

  40. Hillyard, S.A. & Anllo-Vento, L. Event-related brain potentials in the study of visual selective attention. Proc. Natl. Acad. Sci. USA 95, 781 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lee, T.S., Yang, C.F., Romero, R.D. & Mumford, D. Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual salience. Nat. Neurosci. 5, 589 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Tass, P. et al. Detection of n:m phase locking from noisy data: application to magnetoencephalography. Phys. Rev. Lett. 81, 3291 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Wagner for technical assistance, E. Izhikevich, Y. Chen and D. Nitz for discussions, and R. Andretic, H. Dierick and J. Gally for comments on the manuscript. Multichannel silicon probes were provided by the U. Michigan Center for Neural Communication Technology and sponsored by NIH NCRR grant P41-RR09754. This work was supported by the Neurosciences Research Foundation.

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Correspondence to Ralph J Greenspan.

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van Swinderen, B., Greenspan, R. Salience modulates 20–30 Hz brain activity in Drosophila. Nat Neurosci 6, 579–586 (2003). https://doi.org/10.1038/nn1054

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