Cerebral cortical representation of external anal sphincter contraction: effect of effort

Abstract

The external anal sphincter (EAS) plays a critical role in maintaining fecal continence; however, cerebral cortical control of voluntary EAS contraction is not completely understood. Our aims were to determine the cortical areas associated with voluntary EAS contraction and to determine the effect of two levels of sphincter contraction effort on brain activity. Seventeen asymptomatic adults (ages 21-48, 9 male) were studied using functional magnetic resonance imaging (fMRI) to detect brain activity. Studies were done in two stages. In stage 1 (10 subjects, 5 male), anal sphincter pressure was monitored from a catheter-affixed bag. Subjects performed maximal and submaximal EAS contractions during two fMRI scanning sessions consisting of alternating 10-s intervals of sustained contraction and rest. In stage 2 studies, seven subjects (4 male) performed only maximum effort sphincter contractions without a catheter. EAS contraction was associated with multifocal fMRI activity in sensory/motor, anterior cingulate, prefrontal, parietal, occipital, and insular regions. Total cortical activity volume was significantly larger (P Ͻ 0.05) for maximal (5,175 Ϯ 720 l) compared with submaximal effort contractions (2,558 Ϯ 306 l). Similarly, percent fMRI signal change was significantly higher (P Ͻ 0.05) for maximal (4.8 Ϯ 0.1%) compared with submaximal effort contractions (2.2 Ϯ 0.1%). Cortical region-of-interest analysis showed the incidence of insular activation to be more common in women compared with men. Other cortical regions showed no such gender differences. fMRI activity detected in stage 2 showed similar regions of cortical activation to those of the stage 1 study. Willful contraction of the EAS is associated with multifocal cerebral cortical activity. The volume and intensity of cerebral cortical activation is commensurate with the level of contractile effort. fecal continence; functional magnetic resonance imaging VOLUNTARY CONTROL OF THE EXTERNAL anal sphincter plays an essential role in maintaining fecal continence. This sphincter is comprised of deep, superficial, and subcutaneous striated muscle groups located around the terminus of the gastrointestinal tract (47). Innervation to this sphincter is provided by the somatic fibers of the second, third, and fourth sacral routes through the pudendal nerves (3, 27). Considerable information exists about the peripheral and reflex control of the external anal sphincter (6,18,26,35,41). Information about the central control of voluntary contraction of this sphincter in humans, however, is scarce and mostly addresses its contraction response to experimental electrical or magnetic stimulation of the motor cortex (1,12,15,19,29,44). Although these studies have shown contractile response of the external anal sphincter or pelvic floor to direct stimulation of the motor cortex, the cerebral cortical activity map related to voluntary contraction of this sphincter could be quite different from the cortical topography of its control determined by direct cortical stimulation.In ad...

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“…Most studies have dealt with transcranial magnetic or electrical stimulation of the motor cortex, which could trigger contractions of the external sphincter and the pelvic floor 35 -38 . Only Kern et al 39 have described the cortical activation pattern of voluntary anal sphincter contraction in a recently published fMRI study. Their findings, in keeping with the present study, showed that repeated contraction of the external anal sphincter produced activation of the motor as well as the supplementary motor cortex and, in addition, activation of the primary and secondary somatosensory cortex and the insula.…”

“…Activation of centres other than the primary motor cortex was attributed to the necessary design and control of sphincter contraction 39 . However, of particular interest is the intense activation of the insula in the present study and in that by Kern et al 39 , since the role of the insula in voluntary motor activity still remains unclear. Interestingly, Kern et al 39 observed more intense activation of the insula in females.…”