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Sparse odor representation and olfactory learning

Nature Neuroscience volume 11, pages 1177–1184 (2008)Cite this article

Abstract

Sensory systems create neural representations of environmental stimuli and these representations can be associated with other stimuli through learning. Are spike patterns the neural representations that get directly associated with reinforcement during conditioning? In the moth Manduca sexta, we found that odor presentations that support associative conditioning elicited only one or two spikes on the odor's onset (and sometimes offset) in each of a small fraction of Kenyon cells. Using associative conditioning procedures that effectively induced learning and varying the timing of reinforcement relative to spiking in Kenyon cells, we found that odor-elicited spiking in these cells ended well before the reinforcement was delivered. Furthermore, increasing the temporal overlap between spiking in Kenyon cells and reinforcement presentation actually reduced the efficacy of learning. Thus, spikes in Kenyon cells do not constitute the odor representation that coincides with reinforcement, and Hebbian spike timing–dependent plasticity in Kenyon cells alone cannot underlie this learning.

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Figure 1: Projection neurons respond reliably to odors, and different odors evoke different temporally structured patterns of activity.
Figure 2: Odor-elicited spiking in Kenyon cells is brief and sparse.
Figure 3: Kenyon cells responded only to the onset of brief odor pulses and to the onset and offset of long pulses.
Figure 4: Greater temporal overlap between odor-elicited spiking in Kenyon cells and reinforcement delivery did not lead to more learning.

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Acknowledgements

We are grateful to members of the Stopfer laboratory for helpful discussions. We especially thank K. Sun for her excellent animal care. Micrographs were made at the Microscopy and Imaging Core (US National Institute of Child Health and Development, NICHD) with the assistance of V. Schram. We thank C. Wu in the Biometry and Mathematical Statistics Branch, US National Institutes of Health (NIH)/NICHD for his advice on the statistical analysis of the behavioral experiments. This work was supported by grants from the Japan Society for the Promotion of Science (00169, 70510) to I.I., a joint NIH–National Institutes of Standards and Technology postdoctoral fellowship award by the National Research Council to B.R. and an intramural grant from NIH-NICHD to M.S.

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Author notes

  1. Iori Ito and Rose Chik-ying Ong: These authors contributed equally to this work.

Authors and Affiliations

  1. National Institute of Child Health and Human Development, US National Institutes of Health, Building 35, Room 3A-102, Bethesda, 20982, Maryland, USA

    Iori Ito, Rose Chik-ying Ong, Baranidharan Raman & Mark Stopfer

  2. Department of Biochemistry, Room 601, Mong Man Wai Building, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China

    Rose Chik-ying Ong

  3. Chemical Science and Technology Laboratory, National Institute of Standards and Technology, 100 Bureau Drive, Stop 8362, Gaithersburg, 20899-8362, Maryland, USA

    Baranidharan Raman

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Correspondence to Mark Stopfer.

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Ito, I., Ong, Ry., Raman, B. et al. Sparse odor representation and olfactory learning. Nat Neurosci 11, 1177–1184 (2008). https://doi.org/10.1038/nn.2192

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