Impaired odour discrimination on desynchronization of odour-encoding neural assemblies (original) (raw)

Nature volume 390, pages 70–74 (1997)Cite this article

Abstract

Stimulus-evoked oscillatory synchronization of neural assemblies has been described in the olfactory1,2,3,4,5 and visual6,7,8 systems of several vertebrates and invertebrates. In locusts, information about odour identity is contained in the timing of action potentials in an oscillatory population response9,10,11, suggesting that oscillations may reflect a common reference for messages encoded in time. Although the stimulus-evoked oscillatory phenomenon is reliable, its roles in sensation, perception, memory formation and pattern recognition remain to be demonstrated — a task requiring a behavioural paradigm. Using honeybees, we now demonstrate that odour encoding involves, as it does in locusts, the oscillatory synchronization of assemblies of projection neurons and that this synchronization is also selectively abolished by picrotoxin, an antagonist of the GABAA (γ-aminobutyric acid) receptor. By using a behavioural learning paradigm, we show that picrotoxin-induced desynchronization impairs the discrimination of molecularly similar odorants, but not that of dissimilar odorants. It appears, therefore, that oscillatory synchronization of neuronal assemblies is functionally relevant, and essential for fine sensory discrimination. This suggests that oscillatory synchronization and the kind of temporal encoding it affords provide an additional dimension by which the brain could segment spatially overlapping stimulus representations.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

References

  1. Adrian, E. D. Olfactory reactions in the brain of the hedgehog. J. Physiol. (Lond.) 100, 459–473 ( 1942).
    Article CAS Google Scholar
  2. Gray, C. M. & Skinner, J. E. Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Exp. Brain Res. 69, 378–386 (1988).
    Article CAS Google Scholar
  3. Gelperin, A. & Tank, D. W. Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345, 437–440 (1990).
    Article ADS CAS Google Scholar
  4. Delaney, K. R. et al . Waves and stimulus-modulated dynamics in an oscillating olfactory network. Proc. Natl Acad. Sci. USA 91, 669–674 (1994).
    Article ADS CAS Google Scholar
  5. Laurent, G. & Davidowitz, H. Encoding of olfactory information with oscillating neural assemblies. Science 265, 1872–1875 (1994).
    Article ADS CAS Google Scholar
  6. Gray, C. M. & Singer, W. Stimulus specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl Acad. Sci. USA 86, 1698–1702 ( 1989).
    Article ADS CAS Google Scholar
  7. Singer, W. & Gray, C. M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).
    Article CAS Google Scholar
  8. Neuenschwander, S. & Varela, F. J. Visually triggered neuronal oscillations in the pigeon — an autocorrelation study of tectal activity. Eur. J. Neurosci. 7, 870–881 (1993).
    Article Google Scholar
  9. Laurent, G., Wehr, M. & Davidowitz, H. Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837– 3847 (1996).
    Article CAS Google Scholar
  10. Wehr, M. & Laurent, G. Temporal combinatorial encoding of odours with oscillations. Nature 384, 162–166 (1996).<!--384162a0-->
    Article ADS CAS Google Scholar
  11. Laurent, G. Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci. 19, 489– 496 (1996).
    Article CAS Google Scholar
  12. 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
  13. Kuwabara, M. Bildung des bedingten reflexes von pavlovs typus bei der honigbiene, Apis mellifica. J. Fac. Sci. Hokkaido Univ. (Ser. VI Zool.) 13, 458–464 (1957).
    Google Scholar
  14. Bitterman, M. E., Menzel, R., Fietz, A. & Schäfer, S. Classical conditioning of proboscis extension in honeybees (Apis mellifera ). J. Comp. Psychol. 97, 107– 119 (1983).
    Article CAS Google Scholar
  15. Menzel, R. & Bitterman, M. E. in Neuroethology and Behavioral Physiology (eds Huber, F. &Markl, H.) 206– 215 (Springer, New York, (1983)).
    Book Google Scholar
  16. Smith, B. H. & Menzel, R. The use of electromyogram recordings to quantify odorant discrimination in the honey bee, Apis mellifera. J. Insect Physiol. 35, 369– 375 (1989).
    Article CAS Google Scholar
  17. Menzel, R. in Neurobiology of Comparative Cognition (eds Kesner, R. P. &Olton, D. S.) 237–292 (Erlbaum, New Jersey, (1990)).
    Google Scholar
  18. Menzel, R., Michelson, B., Rüffer, P. & Sugawa, M. in Modulation of Synaptic Plasticity in Nervous Systems NATO ASI series, Vol. H19(eds Hertung, G. &Spatz, H.-C.) 335– 350 (Springer, Berlin, (1988)).
    Google Scholar
  19. Yokoi, M., Mori, K. & Nakanishi, S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl Acad. Sci. USA 92, 3371–3375 ( 1995).
    Article ADS CAS Google Scholar
  20. Joerges, J., Kuttner, A., Galizia, C. G. & Menzel, R. Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285–288 (1997).<!--387285a0-->
    Article ADS CAS Google Scholar
  21. Murthy, V. N. & Fetz, E. E. Coherent 25 Hz to 35 Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc. Natl Acad. Sci. USA 89, 5670– 5674 (1992).
    Article ADS CAS Google Scholar
  22. Gray, C. M. Synchronous oscillations in neuronal systems: mechanisms and functions. J. Comput. Neurosci. 1, 11–38 (1994).
    Article CAS Google Scholar
  23. Mauelshagen, J. Neural correlates of olfactory learning-paradigms in an identified neuron in the honeybee brain. J. Neurophysiol. 69, 609–625 (1993).
    Article CAS Google Scholar
  24. Bhagavan, S. & Smith, B. H. Olfactory conditioning in the honey-bee, Apis mellifera –effects of odor intensity. Physiol. Behav. 61, 107–117 ( 1997).
    Article CAS Google Scholar
  25. Smith, B. H. An analysis of blocking in binary odorant mixtures: An increase but not a decrease in intensity of reinforcement produces unblocking. Behav. Neurosci. 111, 57–69 (1997).
    Article CAS Google Scholar
  26. Macmillan, C. S. & Mercer, A. R. An investigation of the role of dopamine in the antennal lobes of the honeybee, Apis mellifera . J. Comp. Physiol. A 160, 359– 366 (1987).
    Article Google Scholar

Download references

Acknowledgements

We thank K. MacLeod, L. Kay, M. Wehr, A. Hershowitz and H. Krapp for their helpful comments. Supported by an NRSA (NIDCD) fellowship (M.S.), +an NIMH grant (B.H.S.), an NSF grant, an NSF Presidential Faculty Fellow award, and a grant from the Sloan Center for Theoretical Neuroscience at Caltech (G.L.).

Author information

Author notes

  1. Seetha Bhagavan
    Present address: GICCS, Georgetown University Medical Center, Research Building Room WP-18, 3970 Reservoir Rd, N.W., Washington, DC, 20007-2197, USA

Authors and Affiliations

  1. California Institute of Technology Biology Division, 139-74, Pasadena, California , 91125, USA
    Mark Stopfer & Gilles Laurent
  2. Department of Entomology, Ohio State University, 1735 Neil Avenue, Columbus, 4210-1220, Ohio, USA
    Seetha Bhagavan & Brian H. Smith

Authors

  1. Mark Stopfer
    You can also search for this author inPubMed Google Scholar
  2. Seetha Bhagavan
    You can also search for this author inPubMed Google Scholar
  3. Brian H. Smith
    You can also search for this author inPubMed Google Scholar
  4. Gilles Laurent
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toGilles Laurent.

Rights and permissions

About this article

Cite this article

Stopfer, M., Bhagavan, S., Smith, B. et al. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies.Nature 390, 70–74 (1997). https://doi.org/10.1038/36335

Download citation

This article is cited by