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Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts

Abstract

Odour representations in insects undergo progressive transformations and decorrelation1,2,3 from the receptor array to the presumed site of odour learning, the mushroom body4,5,6,7. There, odours are represented by sparse assemblies of Kenyon cells in a large population2. Using intracellular recordings in vivo, we examined transmission and plasticity at the synapse made by Kenyon cells onto downstream targets in locusts. We find that these individual synapses are excitatory and undergo hebbian spike-timing dependent plasticity (STDP)8,9,10 on a ±25 ms timescale. When placed in the context of odour-evoked Kenyon cell activity (a 20-Hz oscillatory population discharge), this form of STDP enhances the synchronization of the Kenyon cells’ targets and thus helps preserve the propagation of the odour-specific codes through the olfactory system.

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Figure 1: Synaptic connections between individual Kenyon cells and β-LNs are excitatory, powerful and varied in gain.
Figure 2: β-LN tuning and spike-time precision during responses to odours.
Figure 3: Hebbian spike-time-dependent plasticity at the KC–β-LN synapse.
Figure 4: The effect of STDP on β-LN spike timing.

References

  1. Mazor, O. & Laurent, G. Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661–673 (2005)

    Article  CAS  Google Scholar 

  2. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359–365 (2002)

    Article  ADS  CAS  Google Scholar 

  3. Wilson, R. I., Turner, G. C. & Laurent, G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366–370 (2004)

    Article  ADS  CAS  Google Scholar 

  4. deBelle, J. S. & Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692–695 (1994)

    Article  ADS  CAS  Google Scholar 

  5. Dubnau, J., Grady, L., Kitamoto, T. & Tully, T. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411, 476–480 (2001)

    Article  ADS  CAS  Google Scholar 

  6. Yu, D., Keene, A. C., Srivatsan, A., Waddell, S. & Davis, R. L. Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123, 945–957 (2005)

    Article  CAS  Google Scholar 

  7. Zars, T., Fischer, M., Schulz, R. & Heisenberg, M. Localization of a short-term memory in Drosophila. Science 288, 672–675 (2000)

    Article  ADS  CAS  Google Scholar 

  8. Bi, G. Q. & Poo, M.-M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464–10472 (1998)

    Article  CAS  Google Scholar 

  9. Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213–215 (1997)

    Article  CAS  Google Scholar 

  10. Roberts, P. D. & Bell, C. C. Spike timing dependent synaptic plasticity in biological systems. Biol. Cybern. 87, 392–403 (2002)

    Article  Google Scholar 

  11. Clyne, P. J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327–338 (1999)

    Article  CAS  Google Scholar 

  12. Vosshall, L. B., Wong, A. M. & Axel, R. An olfactory sensory map in the fly brain. Cell 102, 147–159 (2000)

    Article  CAS  Google Scholar 

  13. The. Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949 (2006)

  14. MacLeod, K. & Laurent, G. Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274, 976–979 (1996)

    Article  ADS  CAS  Google Scholar 

  15. Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162–166 (1996)

    Article  ADS  CAS  Google Scholar 

  16. Jortner, R., Farivar, S. S. & Laurent, G. A simple connectivity scheme for sparse coding in an olfactory system. J. Neurosci. 27, 1659–1669 (2007)

    Article  CAS  Google Scholar 

  17. MacLeod, K., Backer, A. & Laurent, G. Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395, 693–698 (1998)

    Article  ADS  CAS  Google Scholar 

  18. Diesmann, M., Gewaltig, M. O. & Aertsen, A. Stable propagation of synchronous spiking in cortical neural networks. Nature 402, 529–533 (1999)

    Article  ADS  CAS  Google Scholar 

  19. Vogels, T. P., Rajan, K. & Abbott, L. F. Neural network dynamics. Annu. Rev. Neurosci. 28, 357–376 (2005)

    Article  CAS  Google Scholar 

  20. Arthur, J. V. & Boahen, K. Advances in Neural Information Processing. (eds Sholkopf, B. & Weiss, Y.) 75–82 (MIT Press, 2006)

    Google Scholar 

  21. Suri, R. E. & Sejnowski, T. J. Spike propagation synchronized by temporally asymmetric Hebbian learning. Biol. Cybern. 87, 440–445 (2002)

    Article  Google Scholar 

  22. Zhigulin, V. P., Rabinovich, M. I., Huerta, R. & Abarbanel, H. D. Robustness and enhancement of neural synchronization by activity-dependent coupling. Phys. Rev. E 67, 021901 (2003)

    Article  ADS  MathSciNet  CAS  Google Scholar 

  23. Ultsch, A., Schuster, C. M., Laube, B., Betz, H. & Schmitt, B. Glutamate receptors of Drosophila melanogaster. Primary structure of a putative NMDA receptor protein expressed in the head of the adult fly. FEBS Lett. 324, 171–177 (1993)

    Article  CAS  Google Scholar 

  24. Tanimoto, H., Heisenberg, M. & Gerber, B. Experimental psychology: event timing turns punishment to reward. Nature 430, 983 (2004)

    Article  ADS  CAS  Google Scholar 

  25. Drew, P. J. & Abbott, L. F. Extending the effects of spike-timing-dependent plasticity to behavioral timescales. Proc. Natl Acad. Sci. USA 103, 8876–8881 (2006)

    Article  ADS  CAS  Google Scholar 

  26. Frey, U. & Morris, R. G. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21, 181–188 (1998)

    Article  CAS  Google Scholar 

  27. Leitch, B. & Laurent, G. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J. Comp. Neurol. 372, 487–514 (1996)

    Article  CAS  Google Scholar 

  28. Nowotny, T., Rabinovich, M. I., Huerta, R. & Abarbanel, H. D. Decoding temporal information through slow lateral excitation in the olfactory system of insects. J. Comput. Neurosci. 15, 271–281 (2003)

    Article  Google Scholar 

  29. Blum, K. I. & Abbott, L. F. A model of spatial map formation in the hippocampus of the rat. Neural Comput. 8, 85–93 (1996)

    Article  CAS  Google Scholar 

  30. Mehta, M. R., Lee, A. K. & Wilson, M. A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741–746 (2002)

    Article  ADS  CAS  Google Scholar 

  31. Perez-Orive, J., Bazhenov, M., Stopfer, M. & Laurent, G. Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. J. Neurosci. 24, 6037–6047 (2004)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by an NIH training grant, grants from the NIDCD, and the Lawrence Hanson Fund. We thank E. Schuman, I. Fiete, M. Murthy, M. Papadopoulou, O. Mazor, V. Jayaraman and the reviewers for their helpful comments.

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Correspondence to Gilles Laurent.

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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figure S1 with Legend which shows morphology of one bLN in the population studied (whole-mount). (PDF 1833 kb)

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Cassenaer, S., Laurent, G. Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448, 709–713 (2007). https://doi.org/10.1038/nature05973

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