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Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study - PubMed

  • ️Tue Jan 01 2002

Comparative Study

Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study

Jay A Gottfried et al. J Neurosci. 2002.

Abstract

Studies of patients with focal brain injury indicate that smell perception involves caudal orbitofrontal and medial temporal cortices, but a more precise functional organization has not been characterized. In addition, although it is believed that odors are potent triggers of emotion, support for an anatomical association is scant. We sought to define the neural substrates of human olfactory information processing and determine how these are modulated by affective properties of odors. We used event-related functional magnetic resonance imaging (fMRI) in an olfactory version of a classical conditioning paradigm, whereby neutral faces were paired with pleasant, neutral, or unpleasant odors, under 50% reinforcement. By comparing paired (odor/face) and unpaired (face only) conditions, odor-evoked neural activations could be isolated specifically. In primary olfactory (piriform) cortex, spatially and temporally dissociable responses were identified along a rostrocaudal axis. A nonhabituating response in posterior piriform cortex was tuned to all odors, whereas activity in anterior piriform cortex reflected sensitivity to odor affect. Bilateral amygdala activation was elicited by all odors, regardless of valence. In posterior orbitofrontal cortex, neural responses evoked by pleasant and unpleasant odors were segregated within medial and lateral segments, respectively. The results indicate functional heterogeneity in areas critical to human olfaction. They also show that brain regions mediating emotional processing are differentially activated by odor valence, providing evidence for a close anatomical coupling between olfactory and emotional processes.

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Figures

Fig. 1.
Fig. 1.

Task and imaging protocol. A, A series of neutral faces (top row) was paired with odors (middle row) that varied in pleasantness. Under 50% reinforcement, only one-half of all faces were paired with odor. A brightening of a cross-hair (bottom row, +) was used to prompt the subject to sniff. The four faces and three odors comprised seven different event types and are depicted schematically. See Materials and Methods for abbreviations and further details.B, Functional images were acquired in an oblique orientation tilted at 30°. On the left, the plane of acquisition and the effective brain coverage are shown overlaid on a subject's sagittal T1-weighted scan. The resulting echoplanar image (z = −22) averaged from 15 subjects is shown beside an image obtained using a standard (untilted) acquisition sequence (average of 11 subjects). Preservation of signal is apparent in the basal frontal and medial temporal lobes. Signal dropout is also diminished in lateral posterior temporal areas.

Fig. 2.
Fig. 2.

Behavioral results. A, Subjective ratings of odor valence for pleasant (VAN), neutral (PEA), and unpleasant (4MP) odors (mean ± SEM; n = 15 subjects).B, Mean subjective ratings of odor intensity (±SEM;n = 15). C, Single-subject sniff waveforms, time-locked to trial onset, averaged over each of the seven condition types, and normalized to the CS− peak. An intervening respiration can be seen between two cued sniffs (marked byasterisk). D, Group mean sniff amplitudes (normalized to CS−) for each condition type and collapsed across all subjects (±SEM). Note that there are no error bars for the CS− condition because this was normalized to 1.0 for all subjects.P, Paired; U, unpaired. E, Group mean sniff latency (time-to-peak) for each condition (±SEM).

Fig. 3.
Fig. 3.

Valence-independent neural activations.A, Piriform cortex. i, The SPM (threshold, p < 0.005) is superimposed on a subject's normalized T1-weighted scan and depicts bilateral activations in posterior piriform cortex. Note in this and all subsequent figures that the left side of the brain corresponds to theleft side of the figure (neurological convention).ii, iii, The region bounded by therectangle in i is shown magnified inii for comparison with a high-resolution anatomical image of posterior piriform cortex (iii) [modified fromMai et al. (1997) and used with permission of Academic Press and the author]. Fp, Frontal piriform cortex;Tp, temporal piriform cortex; A, amygdala; C, caudate; P, putamen,I, insula. B, Amygdala. Neural responses in bilateral dorsomedial amygdala are shown (threshold,p < 0.001). C, Orbitofrontal cortex. Caudal central regions of orbitofrontal cortex were bilaterally activated by all odors (threshold, p < 0.001).D, Contrasts of parameter estimates (β, arbitrary units) were derived from each subject for each of the main effects in posterior piriform cortex (i) (at −26, 2, −26), posterior amygdala (ii) (at −14, −10, −18), and centroposterior OFC (iii) (at 20, 30, −20) and collapsed across all subjects (means ± SEM). Each of the odors, regardless of valence, elicits significant activation.

Fig. 4.
Fig. 4.

Neural activations evoked by unpleasant odor.A, Orbitofrontal cortex. i, The main effect of unpleasant odor (avCS+P − avCS+U) showed significant BOLD increases within left lateral posterior orbitofrontal cortex, which is superimposed on a T1-weighted scan (threshold, p < 0.001).ii, The contrasts of parameter estimates for each main effect are plotted for this region and highlight significantly greater responses to negative odor valence. B, Piriform cortex.i, Habituating neural activations in left anterior piriform cortex were revealed by contrasting the condition × time interactions (avCS+P − avCS+U) (threshold, p < 0.005). ii, Contrasts of parameter estimates in anterior piriform cortex are plotted for each odor. iii, iv, The brain region outlined in i is magnified in iiiand can be compared with a high-resolution atlas image of anterior piriform cortex in iv [modified from Mai et al. (1997), and used with permission of Academic Press and the author].

Fig. 5.
Fig. 5.

Neural activations evoked by pleasant odor.A, Piriform cortex. i, The main effect of pleasant odor (appCS+P − appCS+U) showed nonhabituating responses in right anterior piriform cortex that are overlaid on a normalized T1-weighted scan (threshold,p < 0.005). ii, Contrasts of parameter estimates in this anterior piriform region (at 24, −12, −30) are depicted for each of the main effects. B, Orbitofrontal cortex. i, Significant neural activations were also observed in right caudomedial orbitofrontal cortex (at 18, 16, −16) (threshold, p < 0.001).ii, The corresponding plots of parameter estimates are charted.

Fig. 6.
Fig. 6.

Temporal dynamics of olfactory processing are modulated by odor valence within anterior piriform cortex.A, C, Habituating neural response to unpleasant odor. A, The response profile in anterior piriform cortex (at −30, 10, −28) from a representative subject is depicted three-dimensionally. With successive stimulus repetitions, the percentage change in (fitted) signal activity (avCS+P− avCS+U) declined progressively. C, The contrasts of parameter estimates for unpleasant odor were computed over three successive experimental blocks and averaged over all subjects. The BOLD activity was significantly increased during the first third of the experiment but declined markedly in the remaining two-thirds. B, D, Sustained neural response to pleasant odor. B, The response profile in anterior piriform cortex (at 24, 12, −30) is shown three-dimensionally from the same subject as in A and reveals no decline in signal with repetitions of pleasant odor (appCS+P − appCS+U). D, Contrasts of parameter estimates show persistence of neural activity over the experiment.

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