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Sniffing and smelling: separate subsystems in the human olfactory cortex

Nature volume 392, pages 282–286 (1998)Cite this article

Abstract

The sensation and perception of smell (olfaction) are largely dependent on sniffing, which is an active stage of stimulus transport and therefore an integral component of mammalian olfaction1,2. Electrophysiological data obtained from study of the hedgehog, rat, rabbit, dog and monkey indicate that sniffing (whether or not an odorant is present) induces an oscillation of activity in the olfactory bulb, driving the piriform cortex in the temporal lobe, in other words, the piriform is driven by the olfactory bulb at the frequency of sniffing3,4,5,6. Here we use functional magnetic resonance imaging (fMRI) that is dependent on the level of oxygen in the blood to determine whether sniffing can induce activation in the piriform of humans, and whether this activation can be differentiated from activation induced by an odorant. We find that sniffing, whether odorant is present or absent, induces activation primarily in the piriform cortex of the temporal lobe and in the medial and posterior orbito-frontal gyri of the frontal lobe. The source of the sniff-induced activation is the somatosensory stimulation that is induced by air flow through the nostrils. In contrast, a smell, regardless of sniffing, induces activation mainly in the lateral and anterior orbito-frontal gyri of the frontal lobe. The dissociation between regions activated by olfactory exploration (sniffing) and regions activated by olfactory content (smell) shows a distinction in brain organization in terms of human olfaction.

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Figure 1: Brain regions activated by sniffing and smelling.
Figure 2: Fourier transform of activity within the temporal piriform during four different scans in the same subject.
Figure 3: The component of sniffing that activates the piriform.
Figure 4: The dissociation between sniff-induced and odour-induced activity can be seen within the same subject at the same time (during the same scan).

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Acknowledgements

This work was supported by the Stanford Program in Neuroscience (S.G.F.), Phil & Allen Trust, NIAAA, & NIMH. We thank L. Stryer, B. Wandell, D. Heeger, A. Pfefferbaum, G. Boynton, J.Demb, D. Peterson, G. Heit and J. Wine.

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Authors and Affiliations

  1. Program in Neuroscience, Standford University, Standford, 94305, California, USA

    N. Sobel, V. Prabhakaran, E. V. Sullivan & J. D. E. Gabrieli

  2. Departments of Psychology, Standford University, Standford, 94305, California, USA

    J. E. Desmond & J. D. E. Gabrieli

  3. Departments of Radiology, Standford University, Standford, 94305, California, USA

    G. H. Glover

  4. ENT Surgery, Palo Alto VA Hospital , Palo Alto, 94305, California, USA

    R. L. Goode

  5. Psychiatry & Behavioral Sciences, Standford University, 94305, California, USA

    E. V. Sullivan

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  1. N. Sobel
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Correspondence to N. Sobel.

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Sobel, N., Prabhakaran, V., Desmond, J. et al. Sniffing and smelling: separate subsystems in the human olfactory cortex . Nature 392, 282–286 (1998). https://doi.org/10.1038/32654

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