Cerebral Activation during Anal and Rectal Stimulation M. Lotze,* B. Wietek,† N. Birbaumer,* , ‡ J. Ehrhardt,* W. Grodd,§ and P. Enck† *Institute of Medical Psychology and Behavioral Neurobiology, †Department of General Surgery, and §Section of Experimental Magnetic Resonance of the CNS, Department of Neuroradiology, University of Tu ¨ bingen, D-72074 Tu ¨ bingen, Germany; and ‡Department of General Psychology, University of Padua, Padua, Italy Received January 2, 2001 While the rectum is innervated by visceral afferents, the anal canal is innervated by the somatosensory pu- dendal nerve. The representation of these two central domains of intestinal sensations in the human brain is largely unknown. Nonpainful pneumatic stimulation of the anal canal and the distal rectum using event-related functional magnetic resonance imaging (fMRI) was per- formed in eight healthy subjects. Subjective scaling of sensations revealed no differences in unpleasantness and pain during both stimuli. Both types of stimuli re- vealed fMRI activation in secondary somatosensory, in- sula, cingular gyrus, left inferior parietal, and right or- bitofrontal cortex. Anal stimulation resulted in additional activation of primary sensory and motor cor- tex, supplementary motor area, and left cerebellum. We concluded that viscerorectal and somatosensory anal stimulation predominantly differ in their primary sen- sory activation and additional activation in motor areas. This motor response following aversive somatosensory stimuli may be caused by a reflexive avoidance reaction which is not observed after the more diffuse experi- enced visceral stimulation. © 2001 Academic Press Key Words: visceral; rectal; anal; somatosensory; fMRI. INTRODUCTION Perception of information from the anorectum is cru- cial for maintenance of continence (Whitehead et al., 1981) and is frequently interrupted or blocked in pa- tients with incontinence due to traumatic spinal cord injury, systemic diseases, and neurological deficits. In- creased sensibility of this gastrointestinal compart- ment—also resulting in urge and incontinence—is the major pathomechanism of functional bowel disorders such as the irritable bowel syndrome but may also be a consequence of inflammatory diseases such as ulcer- ative colitis (Bielefeldt et al., 1990). Two major perceptive discriminative functions are involved: the rectal sensing of its filling and the anal identification of content and consistency. This discrim- ination is achieved by two distinctly different innerva- tions: The rectum is innervated by autonomic nerves with sympathetic fibers arising from the lumbar level of the spinal cord (fifth lumbar root) with their post- ganglionic fibers reaching the anal canal (internal anal sphincter) via the hypogastric and pelvic plexus, while parasympathetic fibers originate from the second to the fourth spinal root. In addition, the internal sphinc- ter muscle receives autonomic input from the myen- teric plexus of the rectum (enteric nervous system). In contrast, the anal canal receives sensory and motor projections through the pudendal nerve, which leave the spinal cord at the level of the second to the fourth spinal root bilaterally. The anal canal has a rich supply of nerve endings at the level of the anal skin, while the rectum senses mechanical distention through mech- anoreceptors deep in-between the muscle layers of the gut wall. In consequence, rectal perception has a high threshold and is diffuse in localization (Goligher et al., 1951), while anal sensation is precise in localization, possesses a low threshold, and allows precise discrim- ination (Duthie et al., 1963). While it is conceivable that such differences in peripheral processing of sen- sory information would result in differences in cortical processing of this information, this has not been inves- tigated for the anorectum so far. It is, however, known from the similar innervation pattern of the human bladder that cortical representation of sensations re- sulting in micturition and voiding resembles both so- matosensory and somatomotor components (primary somatosensory cortex, parietal operculum, cerebellum, premotor cortex) on the one hand and midbrain areas involved in processing of the aversive or emotional components of sensations (cingular gyrus, hypothala- mus) on the other hand (Nour et al., 2000; Athwal et al., 2001). Consequently, we would expect a similar network processing sensory information from the ano- rectum. Imaging studies of central processing of sensations arising from the rectum have rarely been undertaken and, if so, predominantly for the evaluation of experi- mental visceral pain in functional bowel disorders (Sil- vermann et al., 1997; Mertz et al., 2000). These authors NeuroImage 14, 1027–1034 (2001) doi:10.1006/nimg.2001.0901, available online at http://www.idealibrary.com on 1027 1053-8119/01 $35.00 Copyright © 2001 by Academic Press All rights of reproduction in any form reserved.