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Brain Activation Associated With Changes in Heart Rate, Heart Rate Variability, and Plasma Catecholamines During Rectal Distention

From the Department of Behavioral Medicine (H.S., S.W., T.H., H.M., T.T., M.K., S.F.); Institute of Development, Aging and Cancer (M.M., T.Y.); Tohoku University, Sendai, Japan; and Post-Graduate Education Center (H.S.) and Department of Laboratory Examination (N.O.), Tohoku University Hospital, Sendai, Japan.

Address correspondence and reprint requests to Shin Fukudo, MD, PhD, Professor, Department of Behavioral Medicine, Tohoku University, 2-1 Seiryo, Aoba, Sendai 980-8575, Japan. E-mail: sfukudo{at}mail.tains.tohoku.ac.jp

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. H₂¹⁵O 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).

Conclusion: 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.

Key Words: positron emission tomography • heart rate • heart rate variability • catecholamine • visceral perception • rectal distention

Abbreviations: PET = positron emission tomography; rCBF = regional cerebral blood flow; SPM = statistical parametric mapping; BA = Brodmann’s area; ECG = electrocardiogram; HRV = heart rate variability; HF = high frequency component of HRV; LF = low frequency component of HRV; LF/HF = ratio of LF to HF; ANOVA = analysis of variance; MRI = magnetic resonance imaging.