Attentional modulation in human primary olfactory cortex

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Abstract

Central to the concept of attention is the fact that identical stimuli can be processed in different ways. In olfaction, attention may designate the identical flow of air through the nose as either respiration or olfactory exploration. Here we have used functional magnetic resonance imaging (fMRI) to probe this attentional mechanism in primary olfactory cortex (POC). We report a dissociation in POC that revealed attention-dependent and attention-independent subregions. Whereas a temporal subregion comprising temporal piriform cortex (PirT) responded equally across conditions, a frontal subregion comprising frontal piriform cortex (PirF) and the olfactory tubercle responded preferentially to attended sniffs as opposed to unattended sniffs. In addition, a task-specific anticipatory response occurred in the attention-dependent region only. This dissociation was consistent across two experimental designs: one focusing on sniffs of clean air, the other focusing on odor-laden sniffs. Our findings highlight the role of attention at the earliest cortical levels of olfactory processing.

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Figure 1: Structural outline of piriform cortex.
Figure 2: Experimental design.
Figure 3: Activity in piriform cortex.
Figure 4: Activity in piriform subdivisions.
Figure 5: Control analyses.
Figure 6: Study controlling for effort.

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Acknowledgements

We thank Arak Elite. This work was supported by a grant from the National Institute of Deafness and Communication Disorders (R01 DC005958). C.Z. is supported by a predoctoral fellowship from the National Science Foundation.

Author information

Correspondence to Christina Zelano or Noam Sobel.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

An example of the progression of the piriform ROI from the anterior commisure and six slices forward. (PDF 4778 kb)

Supplementary Fig. 2

The rules for delineating the structural ROIs. To separate PirF from the olfactory tubercle, we drew a vertical line on the coronal image at the medial border of the uncus, and this line split PirF from TU at its dorsal intersection (line A). To separate between the temporal (PirT) and frontal (PirF) portions of piriform, for each subject we drew a line on the coronal image, at the limen insulae (line B). (PDF 1222 kb)

Supplementary Fig. 3

This figure shows a relation of nasal airflow to MR signal. It shows that differences in nasal airflow across conditions were not reflected in the differing activity across conditions, thus alleviating concerns of airflow. (PDF 191 kb)

Supplementary Fig. 4

FMRI derived Latency differences in BOLD response. This figure shows the mean relative latencies of the BOLD responses of the 3 POC sub-regions. For each condition for each subject, the latency of each trial was calculated as the time from odor onset to peak response. Latency values are shown in units of TR. One TR is 0.5 seconds. Error bars indicate standard error of the mean. There were significantly different latency values across conditions in PirT and PirF (PirT: F(978) = 6.49, p < .0002; PirF: F(978) = 4.17, p < .0061) but not in Tu (F(978) = 1.97, p < 0.1162). As for regional differences, the only significant difference in latency between regions was between PirT and PirF under condition ‘Inhalation2’. The BOLD response in PirT peaked faster in response to ‘Inhalation2’ than did the BOLD response in PirF (F(438) = 4.17, p < .0417). (PDF 65 kb)

The temporal characteristics of fMRI have been explored previously by looking at both time to peak and at the inflection point of the initial BOLD response from baseline (Formisano et al 2002, Menon et al 1998). In both cases, the feasibility of addressing some functional questions in terms of chronometry of human brain functions was confirmed. Although this study was not specifically designed for the purpose of examining temporal aspects of the BOLD signal, differences were observed across conditions. We found that within PirT and PirF, the response to condition ‘Odor’ peaked significantly later than did the response to conditions ‘NoOdor’ and ‘Inhalation2’. In addition, in PirF, condition ‘Odor’ peaked significantly later than did condition ‘Inhalation’. Finally, we observed that the response to condition inhalation2 peaked earlier in PirT than it did in PirF.

Interpretation of these results requires caution, as the exact cause of latency differences of the BOLD signal is not known. However, some speculation can be made. The finding of relatively early activation of PirT in response to ‘Inhalation2’ might implicate the region in early sensory driven processing, while the slower activation of PirF under this condition might imply that it is involved in higher order functions. The finding that condition ‘Odor’ was always the slowest condition could reflect the slow temporal patterning that has been observed in locusts and in mammals in single-cell recordings (Laurent 2002, Laurent G et al 2001, Fletcher et al 2003). These studies have observed responses to a single sniff lasting up to several seconds.

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Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD. Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci. 2001;24:263-97.

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Formisano E et al, Tracking the mind’s image in the brain I: Time resolved fMRI during Visuospatial mental imagery. Neuron, Vol 35, 185-194, July 3, 2002.

Supplementary Fig. 5

This figure shows the mean sniff volume, max flow, mean flow, and duration for all subjects across conditions olfaction vs. audition. Sniffs did not differ significantly for the two tasks, relieving concerns of airflow effects. (PDF 299 kb)

Supplementary Methods

This section contains a detailed description of our methods. (PDF 113 kb)

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Zelano, C., Bensafi, M., Porter, J. et al. Attentional modulation in human primary olfactory cortex. Nat Neurosci 8, 114–120 (2005) doi:10.1038/nn1368

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