Brain Networks during Free Viewing of Complex Erotic Movie: New Insights on Psychogenic Erectile Dysfunction

Psychogenic erectile dysfunction (ED) is defined as a male sexual dysfunction characterized by a persistent or recurrent inability to attain adequate penile erection due predominantly or exclusively to psychological or interpersonal factors. Previous fMRI studies were based on the common occurrence in the male sexual behaviour represented by the sexual arousal and penile erection related to viewing of erotic movies. However, there is no experimental evidence of altered brain networks in psychogenic ED patients (EDp). Some studies showed that fMRI activity collected during non sexual movie viewing can be analyzed in a reliable manner with independent component analysis (ICA) and that the resulting brain networks are consistent with previous resting state neuroimaging studies. In the present study, we investigated the modification of the brain networks in EDp compared to healthy controls (HC), using whole-brain fMRI during free viewing of an erotic video clip. Sixteen EDp and nineteen HC were recruited after RigiScan evaluation, psychiatric, and general medical evaluations. The performed ICA showed that visual network (VN), default-mode network (DMN), fronto-parietal network (FPN) and salience network (SN) were spatially consistent across EDp and HC. However, between-group differences in functional connectivity were observed in the DMN and in the SN. In the DMN, EDp showed decreased connectivity values in the inferior parietal lobes, posterior cingulate cortex and medial prefrontal cortex, whereas in the SN decreased and increased connectivity was observed in the right insula and in the anterior cingulate cortex respectively. The decreased levels of intrinsic functional connectivity principally involved the subsystem of DMN relevant for the self relevant mental simulation that concerns remembering of past experiences, thinking to the future and conceiving the viewpoint of the other’s actions. Moreover, the between group differences in the SN nodes suggested a decreased recognition of autonomical and sexual arousal changes in EDp.

[1]  J. Desmond,et al.  Brain activation and sexual arousal in healthy, heterosexual males. , 2002, Brain : a journal of neurology.

[2]  D. Perani,et al.  Apomorphine-induced brain modulation during sexual stimulation: a new look at central phenomena related to erectile dysfunction , 2003, International Journal of Impotence Research.

[3]  G. Jeong,et al.  Assessment of brain metabolites change during visual sexual stimulation in healthy women using functional MR spectroscopy. , 2013, The journal of sexual medicine.

[4]  S. Hamann,et al.  Men and women differ in amygdala response to visual sexual stimuli , 2004, Nature Neuroscience.

[5]  Wei Zhang,et al.  Selective aberrant functional connectivity of resting state networks in social anxiety disorder , 2010, NeuroImage.

[6]  Maurizio Corbetta,et al.  Large-scale brain networks account for sustained and transient activity during target detection , 2009, NeuroImage.

[7]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[8]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[9]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Hajnal,et al.  Artifacts due to stimulus correlated motion in functional imaging of the brain , 1994, Magnetic resonance in medicine.

[11]  福田 博一 State-Trait Anxiety Inventoryによるペインクリニック外来患者の不安の評価 , 1994 .

[12]  C. Thinus-Blanc,et al.  Pointing to body parts: a double dissociation study , 2003, Neuropsychologia.

[13]  A. Merla,et al.  The role of left superior parietal lobe in male sexual behavior: dynamics of distinct components revealed by FMRI. , 2012, The journal of sexual medicine.

[14]  Sven Joubert,et al.  Areas of brain activation in males and females during viewing of erotic film excerpts , 2002, Human brain mapping.

[15]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[16]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[17]  G. Dunbar,et al.  The Mini International Neuropsychiatric Interview (MINI). A short diagnostic structured interview: reliability and validity according to the CIDI , 1997, European Psychiatry.

[18]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[19]  H. Critchley,et al.  Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans , 2000, The Journal of physiology.

[20]  Hans-Jochen Heinze,et al.  Distinguishing specific sexual and general emotional effects in fMRI—Subcortical and cortical arousal during erotic picture viewing , 2008, NeuroImage.

[21]  F. Montorsi,et al.  Guidelines on erectile dysfunction. , 2002, European urology.

[22]  Harold Mouras,et al.  Brain processing of visual sexual stimuli in healthy men: a functional magnetic resonance imaging study , 2003, NeuroImage.

[23]  B. Abler,et al.  Neural Correlates of Antidepressant-Related Sexual Dysfunction: A Placebo-Controlled fMRI Study on Healthy Males Under Subchronic Paroxetine and Bupropion , 2011, Neuropsychopharmacology.

[24]  N. Costes,et al.  Brain processing of visual sexual stimuli in human males , 2000, Human brain mapping.

[25]  J. Decety,et al.  Neuroanatomical Correlates of Visually Evoked Sexual Arousal in Human Males , 1999, Archives of sexual behavior.

[26]  M Corbetta,et al.  Searching for activations that generalize over tasks , 1997, Human brain mapping.

[27]  O. Bonne,et al.  Cerebral Activation Associated with Sexual Arousal in Response to a Pornographic Clip: A 15O–H2O PET Study in Heterosexual Men , 2001, NeuroImage.

[28]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

[29]  Cheryl L. Grady,et al.  Distributed self in episodic memory: neural correlates of successful retrieval of self-encoded positive and negative personality traits , 2004, NeuroImage.

[30]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[31]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[32]  Peter Fransson,et al.  The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis , 2008, NeuroImage.

[33]  R. Over,et al.  Male Sexual Arousal Elicited by Film and Fantasy Matched in Content , 1997 .

[34]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[35]  G. Romani,et al.  Macrostructural Alterations of Subcortical Grey Matter in Psychogenic Erectile Dysfunction , 2012, PloS one.

[36]  R. Rosen PSYCHOGENIC ERECTILE DYSFUNCTION: Classification and Management , 2001 .

[37]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[38]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[39]  G. Holstege,et al.  Brain Activation during Human Male Ejaculation , 2003, The Journal of Neuroscience.

[40]  T. Hergueta,et al.  The mini international neuropsychiatric interview , 1998, European Psychiatry.

[41]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[42]  Ruud Boessen,et al.  Dynamic subcortical blood flow during male sexual activity with ecological validity: A perfusion fMRI study , 2010, NeuroImage.

[43]  E. Pataraia,et al.  Genital automatisms in complex partial seizures , 1999, Neurology.

[44]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[45]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[46]  J. Decety Do imagined and executed actions share the same neural substrate? , 1996, Brain research. Cognitive brain research.

[47]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[48]  Harold Mouras,et al.  Neuroanatomical correlates of penile erection evoked by photographic stimuli in human males , 2006, NeuroImage.

[49]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[50]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[51]  A. Schnitzler,et al.  Functional Neuroimaging of Visceral Sensation , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[52]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  J. Wincze,et al.  An inventory for the measurement of female sexual arousability: The SAI , 1976, Archives of Sexual Behavior.

[54]  I. Osterloh,et al.  The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction. , 1997, Urology.

[55]  Emiliano Macaluso,et al.  Sensory processing during viewing of cinematographic material: Computational modeling and functional neuroimaging , 2013, NeuroImage.

[56]  A. L. A S T A I,et al.  Erectile dysfunction. , 2006, Harvard men's health watch.

[57]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[58]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[59]  M Liotti,et al.  Brain responses associated with consciousness of breathlessness (air hunger). , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[60]  J. Georgiadis,et al.  Subcortical BOLD responses during visual sexual stimulation vary as a function of implicit porn associations in women. , 2014, Social cognitive and affective neuroscience.

[61]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[62]  J. Decety,et al.  What you believe versus what you think they believe: a neuroimaging study of conceptual perspective‐taking , 2003, The European journal of neuroscience.

[63]  Pia Tikka,et al.  Functional Subdivision of Group-ICA Results of fMRI Data Collected during Cinema Viewing , 2012, PloS one.

[64]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[65]  Paolo Maria Rossini,et al.  Dynamics of male sexual arousal: distinct components of brain activation revealed by fMRI , 2005, NeuroImage.

[66]  Monique Ernst,et al.  Effect of Cigarette Smoking on Prefrontal Cortical Function in Nondeprived Smokers Performing the Stroop Task , 2007, Neuropsychopharmacology.

[67]  Aapo Hyvärinen,et al.  Independent component analysis of fMRI group studies by self-organizing clustering , 2005, NeuroImage.