Elsevier

NeuroImage

Volume 49, Issue 1, 1 January 2010, Pages 177-184
NeuroImage

The somatosensory representation of the human clitoris: An fMRI study

https://doi.org/10.1016/j.neuroimage.2009.07.024Get rights and content

Abstract

We studied the central representation of pudendal afferents arising from the clitoral nerves in 15 healthy adult female subjects using electrical dorsal clitoral nerve stimulation and fMRI. As a control body region, we electrically stimulated the right hallux in eight subjects. In a block design experiment, we applied bilateral clitoral stimulation and unilateral (right) hallux stimulation. Activation maps were calculated for the contrasts ‘electrical dorsal clitoral nerve stimulation versus rest’ and ‘electrical hallux stimulation versus rest’.

A random-effect group analysis for the clitoral stimulation showed significant activations bilateral in the superior and inferior frontal gyri, insulae and putamen and in the postcentral, precentral and inferior parietal gyri (including the primary and secondary somatosensory cortices). No activation was found on the mesial surface of the postcentral gyrus. For the hallux, activations occurred in a similar neuronal network but the activation in the primary somatosensory cortex was localized in the inter-hemispheric fissure.

The results of this study demonstrate that the central representation of pudendal afferents arising from the clitoral nerves and sensory inputs from the hallux can be studied and distinguished from each other by fMRI. From the somatotopic order described in the somatosensory homunculus one would expect for electrical clitoral nerve stimulation activation of the mesial wall of the postcentral gyrus. In contrast, we found activations on the lateral surface of the postcentral gyrus.

Introduction

During the last 70 years the description of the sensory homunculus has been virtually a standard reference for various somatotopical studies (Penfield and Boldrey, 1937). This map consists of a detailed description of the functional cortical representation of different body parts obtained via electrical stimulation during open brain surgery. In their findings they relied on reported sensations of different body parts after electrical stimulation of the cortex. Assessment of the exact location was generally difficult and sometimes led to conflicting results. The genital region was especially hard to assess due to difficulties with sense of shame. The cortical representation of the genital region had been subject to discussion for years with diverse findings (Pfeifer, 1920).

Studies using various neuroimaging techniques came to contradicting conclusions regarding the location of the penile representation. Some studies reported activations evoked by dorsal penile stimulation either to the mesial wall (Allison et al., 1996, Makela et al., 2003, Nakagawa et al., 1998) or to the lateral surface of the postcentral gyrus (Bradley et al., 1998). Kell et al. (2005) demonstrated in an fMRI study an infringement of the somatotopic order, i.e. the localization of the penile representation in the continuity of the body and therefore in contrast to the model proposed by Penfield and Boldrey (1937). Specifically, they established a mediolateral sequence of somatosensory foot, penis, and lower abdominal wall representation in the contralateral primary sensory cortex (S1) and a bilateral secondary somatosensory (S2) representation in the parietal operculum (OP1 and OP4).

Though it can be assumed that the sensory representation of the clitoris is somehow similar to that of the penis, its cortical representation has been scarcely investigated. Using somatosensory evoked potentials (SEPs), Guerit and Opsomer (1991) suggested that the clitoris is located in the inter-hemispheric fissure though they were not able to clearly distinguish its location from that of the posterior tibial nerve SEPs, which can be probably explained by the low spatial resolution of SEPs. Recently, it has been demonstrated in a positron emission tomography study that orgasm – evoked by manual clitoris stimulation – activated bilaterally the lateral S1 (Georgiadis et al., 2006).

In the current study we investigated the neuronal correlates of clitoral stimulations in healthy females to reexamine somatotopy in the female homunculus by high-resolution functional magnetic resonance imaging (fMRI) technique and electrical dorsal clitoral nerve stimulation. Based on recent findings from penile stimulation, we hypothesized that clitoral stimulations will activate a lateral part of the postcentral gyrus rather than the mesial wall. The investigation of the neuronal representation of the clitoris, which is innervated by the dorsal clitoris nerve (Martin-Alguacil et al., 2008), was not only interesting, because a precise description of the anatomical localization is unclear but was rather motivated by a specific clinical question: electrical dorsal genital nerve (i.e. dorsal clitoral nerve) stimulation emerged as a promising therapeutic approach for improving neurogenic and non-neurogenic lower urinary tract dysfunctions such as sphincter weakness or overactive bladder (Brubaker, 2000, Craggs and McFarlane, 1999, Fall and Lindstrom, 1991, Goldman et al., 2008, Opisso et al., 2008, Reitz et al., 2003). Therefore, the exact localization of the stimulated area, i.e. the dorsal clitoral nerve, in healthy subjects would allow us to estimate cortical changes related to stimulation and training effects, e.g. in incomplete spinal cord injury patients.

Section snippets

Materials and methods

The experimental protocol was approved by the local ethics committee (Kantonale Ethikkommission Zürich), and all participants gave their written informed consent before the study. Subjects exclusion criteria were: pregnancy, any current medical condition, any current or past neurological disorders, any surgical interventions of the central nervous system or the urogenital region, and any current drug treatment. None of the subjects carried ferromagnetic materials during the scanning session.

Results

15 healthy right-handed female volunteers (mean age 26 years, range 22–34 years) provided written informed consent and were included in the study. Of those 15 data sets, two data sets had to be excluded from the post-processing and statistical analysis, due to strong head movements during scanning. Therefore all presented results are from 13 subjects with exception of the fMRI data from the hallux stimulation, which were additionally recorded from only 8 subjects.

Discussion

The somatotopic organization depicted in the sensory homunculus by Penfield and Boldrey (1937) has been more or less unchallenged for the last seventy years. Genital representation in S1 was assigned to the mesial wall of the paracentral lobule.

The discontinuous shape of the somatosensory homunculus concerning the location of the genitals apart from the rest of the body has been subject to discussion for a long time and several theories have been postulated to explain this finding, like the

Conclusion

In contrast to previous studies using SEPs that were not able to clearly discriminate the location of cortical sensory representation of the genitals in humans, we found a significant activation on the convexity of the postcentral and inferior parietal cortex (S1 and S2) for electrical clitoral stimulation. These findings support the assumption that the S1 representation of the clitoral afferents may be different from the somatosensory homunculus introduced decades ago. The distinct activation

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