Functional brain correlates of heterosexual paedophilia

Abstract

Although the neuronal mechanisms underlying normal sexual motivation and function have recently been examined, the alterations in brain function in deviant sexual behaviours such as paedophilia are largely unknown. The objective of this study was to identify paedophilia-specific functional networks implicated in sexual arousal. Therefore a consecutive sample of eight paedophile forensic inpatients, exclusively attracted to females, and 12 healthy age-matched heterosexual control participants from a comparable socioeconomic stratum participated in a visual sexual stimulation procedure during functional magnetic resonance imaging. The visual stimuli were sexually stimulating photographs and emotionally neutral photographs. Immediately after the imaging session subjective responses pertaining to sexual desire were recorded. Principally, the brain response of heterosexual paedophiles to heteropaedophilic stimuli was comparable to that of heterosexual males to heterosexual stimuli, including different limbic structures (amygdala, cingulate gyrus, and hippocampus), the substantia nigra, caudate nucleus, as well as the anterior cingulate cortex, different thalamic nuclei, and associative cortices. However, responses to visual sexual stimulation were found in the orbitofrontal cortex in healthy heterosexual males, but not in paedophiles, in whom abnormal activity in the dorsolateral prefrontal cortex was observed. Thus, in line with clinical observations and neuropsychological studies, it seems that central processing of sexual stimuli in heterosexual paedophiles may be altered by a disturbance in the prefrontal networks, which, as has already been hypothesized, may be associated with stimulus-controlled behaviours, such as sexual compulsive behaviours. Moreover, these findings may suggest a dysfunction (in the functional and effective connectivity) at the cognitive stage of sexual arousal processing.

Introduction

Paedophilia is a psychiatric disorder of high public concern characterized by intense sexually arousing urges and behaviours focused on sexual activity with a prepubescent child (American Psychiatric Association, 1994). Numerous studies have discussed the associations between behavioural disinhibition, frontal abnormalities, and impaired cognitive executive functioning. Although recent data from neuropsychological, sexual historical, plethysmographic, and neuroimaging investigations suggest that paedophilia is linked to early neurodevelopment perturbations (Cantor et al., 2004, Cohen et al., 2002), the neurobiological basis of the disorder is still unidentified.

Human sexual arousal is a multidimensional experience comprising physiological and psychological processes. Modern imaging techniques allow the in vivo observation of brain activation correlated with sensory or cognitive processing and emotional states (Krueger et al., 2005). Previous studies in healthy humans (Arnow et al., 2002, Beauregard et al., 2001, Bocher et al., 2001, Ferretti et al., 2005, Hamann et al., 2004, Holstege et al., 2003, Karama et al., 2002, Mouras et al., 2003, Park et al., 2001, Redoute et al., 2000, Stoleru et al., 1999, Paul et al., in press e-pub) 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 temporal cortex, the orbitofrontal cortex (OFC), the inferior and superior parietal lobules, the cingulate cortex, the anterior cingulate cortex (ACC), the insula, and the hypothalamus. These activation patterns are considered to represent the perceptual-cognitive, emotional, motivational, and physiological (autonomic and endocrinological) components of sexual arousal as proposed in a neurobehavioural and multifaceted model of neural mechanisms for sexual arousal (Redoute et al., 2000, Stoleru et al., 1999). Briefly, the cognitive component comprises a process of appraisal through which a stimulus is categorized as a sexual incentive and quantitatively evaluated as such. The emotional component includes the specific hedonic quality of sexual arousal, i.e., the pleasure associated with rising arousal and with the perception of specific bodily changes. The motivational component comprises the processes that direct behaviour to a sexual goal, including the perceived urge to express overt sexual behaviour. The autonomic and endocrinological components include various responses (e.g. cardiovascular, respiratory, and genital) leading the subject to a state of physiological readiness for sexual behaviour (Krueger et al., 2006). These four components are conceived to be closely interrelated and coordinated (Redoute et al., 2000).

Regarding deviant human sexual behaviour, several case reports on paedophilic patients and two group studies using voxel-based-morphometry described changes in the prefrontal cortex (PFC), the ventral striatum, the amygdala, and the medial temporal cortex (Mendez et al., 2000, Burns and Swerdlow, 2003, Schiffer et al., 2007, Schiltz et al., 2007). One group study using positron emission tomography (PET) also demonstrated a persistently decreased glucose metabolism in the right inferior temporal and superior ventral frontal gyrus (Cohen et al., 2002). Furthermore, two functional magnetic resonance imaging (fMRI) studies showed varying activations during different visual erotic stimulation paradigms (adult stimuli only and adult vs. child stimuli) in two groups of paedophilic forensic inpatient populations (heterosexual paedophiles and homosexual paedophiles). The results of one study comprised the hypothalamus, the periaqueductal gray, and the dorsolateral prefrontal cortex (Walter et al., 2007, for heterosexual paedophiles and adult stimuli), while those of the second study involved different parts of the PFC, the substantia nigra (SN), and the basal ganglia including caudate nucleus (CN), putamen, and pallidum (Schiffer et al., 2008, for homosexual paedophiles and adult vs. child stimuli).

The current study aimed to test for the first time the hypothesis that heterosexual paedophiles show altered neural activity in those brain regions implicated in sexual arousal, especially the OFC, the dorsolateral prefrontal cortex (DLPFC), the ACC, different limbic structures, including the cingulate gyrus, hypothalamus, and amygdala as well as the thalamus and parts of the basal ganglia. Therefore we used functional magnetic resonance imaging (fMRI) to compare neural activity patterns in a group of paedophile inpatients, who were exclusively attracted to female children, and heterosexually oriented control subjects, while viewing pictures of prepubescent girls and adult women in dressed/neutral vs. nude/sexually arousing mode.