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The Journal of Neurophysiology Vol. 88 No. 3 September 2002, pp. 1500-1511
Copyright ©2002 by the American Physiological Society
1Physiology Program, Harvard School of Public Health, Boston, Massachusetts 02115; 2Department of Respiratory Medicine, National Heart and Lung Institute, Imperial College School of Medicine Charing Cross Campus, London W6 8RP; 3Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom; and 4Department of Medicine, Harvard Medical School, Boston, Massachusetts 02115
Evans, Karleyton C.,
Robert
B. Banzett,
Lewis Adams,
Leanne McKay,
Richard S. J. Frackowiak, and
Douglas R. Corfield.
BOLD fMRI Identifies Limbic, Paralimbic, and Cerebellar
Activation During Air Hunger. J. Neurophysiol. 88: 1500-1511, 2002. Air hunger
(uncomfortable urge to breathe) is a component of dyspnea (shortness of
breath). Three human H215O
positron emission tomography (PET) studies have identified activation of phylogenetically ancient structures in limbic and paralimbic regions
during dyspnea. Other studies have shown activation of these structures
during other sensations that alert the organism to urgent homeostatic
imbalance: pain, thirst, and hunger for food. We employed blood oxygen
level dependent (BOLD) functional magnetic resonance imaging (fMRI) to
examine activation during air hunger. fMRI conferred several advantages
over PET: enhanced signal-to-noise, greater spatial resolution, and
lack of ionizing radiation, enabling a greater number of trials in each
subject. Six healthy men and women were mechanically ventilated at
12-14 breaths/min. The primary experiment was conducted at mean
end-tidal PCO2 of 41 Torr. Moderate
to severe air hunger was evoked during 42-s epochs of lower tidal
volume (mean = 0.75 L). Subjects described the sensation as
"like breath-hold," "urge to breathe," and "starved for
air." In the baseline condition, air hunger was consistently relieved
by epochs of higher tidal volume (mean = 1.47 L). A control experiment in the same subjects under a background of mild hypocapnia (mean end-tidal PCO2 = 33 Torr) employed similar
tidal volumes but did not evoke air hunger, controlling for stimulus
variables not related to dyspnea. During each experiment, we maintained constant end-tidal PCO2 and
PO2 to avoid systematic changes in global
cerebral blood flow. Whole-brain images were acquired every 5 s
(T2*, 56 slices, voxel resolution 3 × 3 × 3 mm).
Activations associated with air hunger were determined using
voxel-based interaction analysis of covariance that compared data
between primary and control experiments (SPM99). We detected
activations not seen in the earlier PET study using a similar air
hunger stimulus (Banzett et al. 2000). Limbic and
paralimbic loci activated in the present study were within anterior
insula (seen in all 3 published studies of dyspnea), anterior
cingulate, operculum, cerebellum, amygdala, thalamus, and basal
ganglia. Elements of frontoparietal attentional networks were also
identified. The consistency of anterior insular activation across
subjects in this study and across published studies suggests that the
insula is essential to dyspnea perception, although present data
suggest that the insula acts in concert with a larger neural network.
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