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The Journal of Neuroscience, December 15, 2002, 22(24):10819-10828
Functional Heterogeneity in Human Olfactory Cortex: An
Event-Related Functional Magnetic Resonance Imaging Study
Jay A.
Gottfried,
Ralf
Deichmann,
Joel S.
Winston, and
Raymond J.
Dolan
Wellcome Department of Imaging Neuroscience, Institute of
Neurology, London, WC1N 3BG, United Kingdom
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.
Key words:
olfaction; odor; emotion; neuroimaging; fMRI; piriform
cortex; olfactory cortex; amygdala; orbitofrontal cortex
Copyright © 2002 Society for Neuroscience 0270-6474/02/222410819-10$05.00/0
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|