Dynamics of male sexual arousal: distinct components of brain activation revealed by fMRI

Abstract

The peripheral mechanisms of male sexual arousal are well known. Recently, neuroimaging techniques, such as PET or fMRI, allowed the investigation of the subjacent cerebral mechanisms. In ten healthy subjects, we have simultaneously recorded fMRI images of brain activation elicited by viewing erotic scenes, and the time course of penile tumescence by means of a custom-built MRI-compatible pneumatic cuff. We have compared activation elicited by video clips with a long duration, that led to sexual arousal and penile erection, and activation elicited by briefly presented still images, that did induce sexual arousal without erection. This comparison and the use of the time course of penile tumescence in video clips allowed to perform a time resolved data analysis and to correlate different patterns of brain activation with different phases of sexual response. The activation maps highlighted a complex neural circuit involved in sexual arousal. Of this circuit, only a few areas (anterior cingulate, insula, amygdala, hypothalamus, and secondary somatosensory cortices) were specifically correlated with penile erection. Finally, these areas showed distinct dynamic relationships with the time course of sexual response. These differences might correspond to different roles in the development and appraisal of the sexual response. These findings shed light on the psychophysiology of male sexuality and open new perspectives for the diagnosis, therapy, and possible rehabilitation of sexual dysfunction.

Introduction

Human sexual arousal is a multidimensional experience comprising physiological and psychological processes. Studies on sexual behavior have mainly focused on the peripheral mechanisms of sexual response. The neurovascular, autonomic, and hormonal mechanisms involved in the sexual response in man have been for the largest part established (Anderson, 2003, Morrel et al., 1994, Simonsen et al., 2002). However, relatively little is known about the brain areas supporting the psychological mechanisms involved in sexual response and of the hierarchical organization along with the different stages characterizing sexual arousal, penile tumescence, and erection.

Modern techniques dealing with mapping procedures of brain function in time and space allow the in vivo observation of brain activation correlated with sensory or cognitive processing and emotional states. Previous studies (Arnow et al., 2002, Beauregard et al., 2001, Bocher et al., 2001, Hamann et al., 2004, Holstege et al., 2003, Karama et al., 2002, Mouras et al., 2003, Park et al., 2001a, Park et al., 2001b, Redouté et al., 2000, Redouté et al., 2005, Stoleru et al., 1999) using functional magnetic resonance imaging (fMRI) or positron emission tomography (PET), and remote sexual stimuli such as visual erotica, have shown increased neural activity in several areas including the inferior right frontal cortex, the inferior temporal cortex, the left anterior cingulate cortex, and the right insula, possibly representing a distributed network.

The aim of this study was to disentangle the spatiotemporal characteristics of relationships among brain areas during the various phases of a behavioral response to visual erotic stimuli leading to a complete erection, and distinguishing them from each other and from non-sexual arousal and attention. Since there is general consensus that penile erection in a sexual context is the best index of sexual arousal, we simultaneously recorded both the BOLD response and the level of penile tumescence during visual erotic stimulation in two different fMRI experimental paradigms. In the first paradigm, participants were presented with prolonged erotic video clips, while in the second paradigm they were briefly presented with erotic still images. The on-line continuous measurement of penile tumescence allowed: (1) to identify, in the former paradigm, the linkage between successive phases of behavioral response and the hierarchy of the distributed brain network supporting it; and (2) to verify that the latter paradigm never led participants to penile erection while the former always did. The hypothesis was that brain areas activated only in the former condition should be related to erection rather than to simple sexual arousal and that in the former condition the relative timing of the activated areas should reflect the progression from a general sexual arousal to a sustained sexual response.