Brain activation associated with changes in heart rate, heart rate variability, and plasma catecholamines during rectal distention.
OBJECTIVE
To test the hypothesis that gut stimulation provokes autonomic arousal via activation of regional cerebral cortices. How the human brain processes interoceptive signals and forms initial autonomic arousal is one of the key questions to be answered in research on emotion.


METHODS
Twelve healthy males participated in this study. A barostat bag was inserted in the rectum and intermittently inflated with 0, 20, or 40 mm Hg at random for 80 seconds. H(2)(15)O positron emission tomography (PET) of the brain, electrocardiography, and blood sampling for catecholamines were performed. Changes in regional cerebral blood flow were interpreted using statistical parametric mapping.


RESULTS
Rectal distention with 40 mm Hg induced a significant increase in heart rate, low frequency (LF)/high frequency (HF) ratio of heart rate variability, and plasma adrenaline. Activated brain areas that were associated with increased heart rate during rectal distention were the right insula, right operculum, right dorsolateral prefrontal cortex, putamen, thalamus, periaqueductal gray, and cerebellum (p < .001, uncorrected), whereas those that were associated with an increased LF/HF ratio were the bilateral insula, putamen, thalamus, midbrain, pons, and cerebellum (p < .001, uncorrected). Activated brain areas that were associated with increased plasma adrenaline were the right insula, right orbitofrontal cortex, right parahippocampal gyrus, putamen, thalamus, periaqueductal gray, pons, and cerebellum (p < .001, uncorrected).


CONCLUSIONS
Our results suggest that the right insula and the related body mapping regions may form the functional module of sympathetic arousal in response to gut stimulation.
Suzuki
Hideaki
H
Department of Behavioral Medicine, Tohoku University, Aoba, Sendai, Japan.
Watanabe
Satoshi
S
Hamaguchi
Toyohiro
T
Mine
Hirotaka
H
Terui
Takahiro
T
Kanazawa
Motoyori
M
Oohisa
Noriko
N
Maruyama
Mitsuya
M
Yambe
Tomoyuki
T
Itoh
Masatoshi
M
Fukudo
Shin
S
D001143:Arousal / Q000502:physiology*; D001341:Autonomic Nervous System / Q000502:physiology*; D001921:Brain / Q000000981:diagnostic imaging / Q000502:physiology*; D001931:Brain Mapping; D002395:Catecholamines / Q000097:blood*; D002404:Catheterization / Q000379:methods; D002531:Cerebellum / Q000502:physiology; D002540:Cerebral Cortex / Q000502:physiology; D003071:Cognition / Q000502:physiology; D004562:Electrocardiography / Q000706:statistics & numerical data; D004644:Emotions / Q000502:physiology; D004837:Epinephrine / Q000097:blood; D007839:Functional Laterality / Q000502:physiology; D006339:Heart Rate / Q000502:physiology*; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D049268:Positron-Emission Tomography / Q000706:statistics & numerical data; D017397:Prefrontal Cortex / Q000502:physiology; D012007:Rectum / Q000294:innervation / Q000502:physiology*; D013788:Thalamus / Q000502:physiology
D002395:Catecholamines; D004837:Epinephrine