Gray matter deficits and altered resting-state connectivity in the superior temporal gyrus among individuals with problematic hypersexual behavior (2018)

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COMMENTS: This brain scan study is added to our list of 38 neurological studies on sex addicts and porn users. This fMRI study compared carefully screened sex addicts ("problematic hypersexual behavior") to healthy control subjects. Sex addicts had reduced gray matter in the temporal lobes - regions the authors say are associated with inhibition of sexual impulses:

In the VBM results, reduced temporal gyrus volume was found in the individuals with PHB compared to healthy controls. In particular, the gray matter volume in the left STG was negatively correlated with the severity of PHB. Removal of the temporal lobes has been shown to lead to indiscriminate sexual advances (Baird et al., 2002). Task-based imaging studies on sexual arousal also have documented an association between deactivated temporal regions and the development of sexual arousal (Redouté et al. (2000); Stoleru et al., 1999). These studies suggest that the temporal regions are related to tonic inhibition of the development of sexual arousal and that alleviation of this inhibition resulting from damage or dysfunction of the temporal lobes could lead to dramatic hypersexuality (Baird et al., 2002; Redouté et al. (2000); Stoleru et al., 1999). We speculated that the reduced gray matter volume in the temporal gyrus may contribute to the increased sexuality in an individual with PHB

Study also reported poorer functional connectivity between the left superior temporal gyrus (STG) and the right caudate. Kuhn & Gallnat, 2014 reported a similar finding: "Functional connectivity of the right caudate to the left dorsolateral prefrontal cortex was negatively associated with hours of pornography consumption". This study's finding:

Compared to healthy subjects, individuals with PHB had significantly decreased functional connectivity between the STG and the caudate nucleus. A negative correlation was also observed between the severity of PHB and functional connectivity between these areas. Anatomically, the STG has direct connections with the caudate nucleus (Yeterian and Pandya, 1998). The caudate nucleus is the main subregion of the striatum, and is important for reward-based behavioral learning, intricately associated with pleasure and motivation, and related to the maintenance of addictive

Sex addicts also exhibited reduced precuneus to temporal cortex functional connectivity. The paper explains:

Several studies have reported that the left precuneus is involved in the integration of information from different sensory modalities, and plays a pivotal role in attention shifting and sustained attention (Cavanna and Trimble, 2006; Simon et al., 2002). In addition, studies on addiction have reported that participants with addiction have problems with attention shifting, and that this behavioral characteristic is related to altered activation of the precuneus (Dong et al., 2014; Courtney et al., 2014). Given the role of the precuneus, our results provide evidence for the possible role of the precuneus in PHB, as it may be related to functional abnormalities in attention shifting

The authors explain the significance of the two instances of altered functional connectivity:

The lower connectivity between the right caudate nucleus and the STG found in the present study may have implications for functional deficits such as reward delivery and anticipation in PHB (Seok and Sohn, 2015; Voon et al., 2014). These findings suggest that the structural deficits in the temporal gyrus and the altered functional connectivity between the temporal gyrus and specific areas (i.e., the precuneus and caudate) might contribute to the disturbances in tonic inhibition of sexual arousal in individuals with PHB. Thus, these results suggest that changes in structure and functional connectivity in the temporal gyrus might be PHBspecific features and may be biomarker candidates for the diagnosis of PHB

Put simply, several earlier studies on sex/porn addicts found poorer connectivity between the cortex and the reward system. Since one job of the cortex is to put the brakes of impulses arising from our deeper reward structures - this may indicate a deficit in "top-down" control. This functional and structural deficit is a hallmark of all types of addiction. The study summary:

In summary, the present VBM and functional connectivity study showed gray matter deficits and altered functional connectivity in the temporal gyrus among individuals with PHB. More importantly, the diminished structure and functional connectivity were negatively correlated with the severity of PHB. These findings provide new insights into the underlying neural mechanisms of PHB.

The study also reported an increase in gray matter associated with sexual activity:

Gray matter enlargement in the right cerebellar tonsil and increased connectivity of the left cerebellar tonsil with the left STG were also observed. Interestingly, the connectivity between these regions was not maintained after controlling for the effect of sexual activity among individuals with PHB.

The authors wondered if high levels of sexual activity altered the connections between the cortex and the cerebellum:

This may reflect that this connection is more likely associated with sexual activity rather than sexual addiction or hypersexuality....Therefore, it is possible that the increased gray matter volume and functional connectivity in the cerebellum is associated with compulsive behavior in individuals with PHB


Brain Res. 2018 Feb 5. pii: S0006-8993(18)30055-6. doi: 10.1016/j.brainres.2018.01.035.

LINK TO ABSTRACT

Seok JW1, Sohn JH2.

Abstract

Neuroimaging studies on the characteristics of hypersexual disorder have been accumulating, yet alternations in brain structures and functional connectivity in individuals with problematic hypersexual behavior (PHB) has only recently been studied. This study aimed to investigate gray matter deficits and resting-state abnormalities in individuals with PHB using voxel-based morphometry and resting-state connectivity analysis. Seventeen individuals with PHB and 19 age-matched healthy controls participated in this study. Gray matter volume of the brain and resting-state connectivity were measured using 3T magnetic resonance imaging. Compared to healthy subjects, individuals with PHB had significant reductions in gray matter volume in the left superior temporal gyrus (STG) and right middle temporal gyrus. Individuals with PHB also exhibited a decrease in resting-state functional connectivity between the left STG and left precuneus and between the left STG and right caudate. The gray matter volume of the left STG and its resting-state functional connectivity with the right caudate both showed significant negative correlations with the severity of PHB. The findings suggest that structural deficits and resting-state functional impairments in the left STG might be linked to PHB and provide new insights into the underlying neural mechanisms of PHB.

KEYWORDS: Caudate nucleus; Functional connectivity; Problematic hypersexual behavior; Superior temporal gyrus; Voxel-based morphometry

PMID: 29421186

DOI: 10.1016/j.brainres.2018.01.035

DISCUSSION SECTION

In the VBM results, reduced temporal gyrus volume was found in the individuals with PHB compared to healthy controls. In particular, the gray matter volume in the left STG was negatively correlated with the severity of PHB. Removal of the temporal lobes has been shown to lead to indiscriminate sexual advances (Baird et al., 2002). Task-based imaging studies on sexual arousal also have documented an association between deactivated temporal regions and the development of sexual arousal (Redouté et al. (2000); Stoleru et al., 1999). These studies suggest that the temporal regions are related to tonic inhibition of the development of sexual arousal and that alleviation of this inhibition resulting from damage or dysfunction of the temporal lobes could lead to dramatic hypersexuality (Baird et al., 2002; Redouté et al. (2000); Stoleru et al., 1999). We speculated that the reduced gray matter volume in the temporal gyrus may contribute to the increased sexuality in an individual with PHB, and this finding might suggest that the left STG is part of a relevant functional circuit associated with PHB. To identify the effects of reduced volume of the left STG on this functional circuit further, resting-state functional connectivity analysis was performed.

Our results demonstrate that individuals with PHB have reduced left precuneus-left STG and right caudate-left STG connectivity The precuneus has reciprocal cortical connections with the superior temporal sulcus. These regions, along with the occipital visual area, comprise the temporo-parieto-occipital cortex(Leichnetz, 2001; Cavanna and Trimble, 2006). Several studies have reported that the left precuneus is involved in the integration of information from different sensory modalities, and plays a pivotal role in attention shifting and sustained attention (Cavanna and Trimble, 2006; Simon et al., 2002). In addition, studies on addiction have reported that participants with addiction have problems with attention shifting, and that this behavioral characteristic is related to altered activation of the precuneus (Dong et al., 2014; Courtney et al., 2014). Given the role of the precuneus, our results provide evidence for the possible role of the precuneus in PHB, as it may be related to functional abnormalities in attention shifting

Compared to healthy subjects, individuals with PHB had significantly decreased functional connectivity between the STG and the caudate nucleus. A negative correlation was also observed between the severity of PHB and functional connectivity between these areas. Anatomically, the STG has direct connections with the caudate nucleus (Yeterian and Pandya, 1998). The caudate nucleus is the main subregion of the striatum, and is important for rewardbased behavioral learning, intricately associated with pleasure and motivation, and related to the maintenance of addictive

behaviors (Ma et al., 2012; Vanderschuren and Everitt, 2005). Neuronal activities in the striatum in monkeys have been shown to respond to reward delivery and anticipation (Apicella et al., 1991, 1992). Striatal neurons influence the representation of goals before and during the execution of actions by coding incentive salience, reward magnitude, and reward preference (Hassani et al., 2001). Neuroimaging studies of behaviorally addicted populations have reported the consistent finding of striatal alterations, such as decreased functional and structural connectivities and a reduction of task-based blood oxygenation level-dependent (BOLD) activity (Hong et al., 2013a,b; Jacobsen et al., 2001; Lin et al., 2012; Seok and Sohn, 2015). More recently, a study on sexually explicit material consumption suggested that alterations in the striatum could reflect changes in neural plasticity as a consequence of an intense stimulation of the reward system (Kühn and Gallinat, 2014). The lower connectivity between the right caudate nucleus and the STG found in the present study may have implications for functional deficits such as reward delivery and anticipation in PHB (Seok and Sohn, 2015; Voon et al., 2014). These findings suggest that the structural deficits in the temporal gyrus and the altered functional connectivity between the temporal gyrus and specific areas (i.e., the precuneus and caudate) might contribute to the disturbances in tonic inhibition of sexual arousal in individuals with PHB. Thus, these results suggest that changes in structure and functional connectivity in the temporal gyrus might be PHBspecific features and may be biomarker candidates for the diagnosis of PHB.

Gray matter enlargement in the right cerebellar tonsil and increased connectivity of the left cerebellar tonsil with the left STG were also observed. Interestingly, the connectivity between these regions was not maintained after controlling for the effect of sexual activity among individuals with PHB. This may reflect that this connection is more likely associated with sexual activity rather than sexual addiction or hypersexuality. The cerebellar tonsil is highly involved in obsessive-compulsive disorders, especially in its integration with corticostriatal neuronal processes (Middleton and Strick, 2000; Brooks et al., 2016). Previous studies on individuals with obsessive-compulsive disorders showed larger cerebellar volumes compared with healthy controls (Peng et al., 2012; Rotge et al., 2010). Some individuals with PHB present with clinical features that resemble obsessive-compulsive disorder, such as sexual obsessions and compulsions to act out sexually (Fong, 2006). Therefore, it is possible that the increased gray matter volume and functional connectivity in the cerebellum is associated with compulsive behavior in individuals with PHB.

These findings suggest that the structural deficits in the temporal gyrus and the altered functional connectivity between the temporal gyrus and specific areas (i.e., the precuneus and caudate) might contribute to the disturbances in tonic inhibition of sexual arousal in individuals with PHB. Thus, these results suggest that changes in structure and functional connectivity in the temporal gyrus might be PHB specific features and may be biomarker candidates for the diagnosis of PHB.

Gray matter enlargement in the right cerebellar tonsil and increased connectivity of the left cerebellar tonsil with the left STG were also observed. Interestingly, the connectivity between these regions was not maintained after controlling for the effect of sexual activity among individuals with PHB. This may reflect that this connection is more likely associated with sexual activity rather than sexual addiction or hypersexuality. The cerebellar tonsil is highly involved in obsessive-compulsive disorders, especially in its integration with corticostriatal neuronal processes (Middleton and Strick, 2000; Brooks et al., 2016). Previous studies on individuals with obsessive-compulsive disorders showed larger cerebellar volumes compared with healthy controls (Peng et al., 2012; Rotge et al., 2010). Some individuals with PHB present with clinical features that resemble obsessive-compulsive disorder, such as sexual obsessions and compulsions to act out sexually (Fong, 2006). Therefore, it is possible that the increased gray matter volume and functional connectivity in the cerebellum is associated with compulsive behavior in individuals with PHB.

There have been few studies on brain changes among individuals with PHB utilizing a combination of VBM and rs-fMRI. Previous reports have found that enhanced sexual activity could change brain structure and function, and these findings have elucidated the underlying neurobiology of compulsive sexual behavior (Schmidt et al., 2017). However, that study did not exclude the influence of behavioral characteristics on the relationship between PHB and brain alteration. Therefore, we replicated the previous study to identify brain alteration in individuals with PHB (Schmidt et al., 2017), and conducted further analysis controlling for sexual activity to further clarify the influence of the hypersexuality and sex addiction factors.

In summary, the present VBM and functional connectivity study showed gray matter deficits and altered functional connectivity in the temporal gyrus among individuals with PHB. More importantly, the diminished structure and functional connectivity were negatively correlated with the severity of PHB. These findings provide new insights into the underlying neural mechanisms of PHB.

PHB was defined by two qualified clinicians based on clinical interview using PHB diagnostic criteria set in previous studies (Carnes et al., 2010; Kafka, 2010) (Table S1). Nineteen age-, education-, gender-matched controls who did not meet the PHB diagnostic criteria were enrolled in the study. We used the following exclusion criteria for PHB and control participants: age over 35 or under 18; other addictions such as alcoholism or gambling addiction, previous or current psychiatric, neurological, and medical disorders, homosexuality, currently using medication, a history of serious head injury, and general MRI contraindications (i.e., having a metal in the body, severe astigmatism, or claustrophobia).