Men versus women on sexual brain function: Prominent differences during tactile genital stimulation, but not during orgasm

Biological differences in male and female sexuality are obvious in the behavioral domain, but the central mechanisms that might explain these behavioral gender differences remain unclear. In this study, we merged two earlier positron emission tomography data sets to enable systematic comparison of the brain responses in heterosexual men and women during sexual tactile genital (penile and clitoral) stimulation and during orgasm. Gender commonalities were most evident during orgasm, a phase which demonstrated activations in the anterior lobe of the cerebellar vermis and deep cerebellar nuclei, and deactivations in the left ventromedial and orbitofrontal cortex in both men and women. During tactile genital stimulation, deactivations in the right amygdala and left fusiform gyrus were found for both genders. Marked gender differences were seen during this phase: left fronto‐parietal areas (motor cortices, somatosensory area 2 and posterior parietal cortex) were activated more in women, whereas in men, the right claustrum and ventral occipitotemporal cortex showed larger activation. The only prominent gender difference during orgasm was male‐biased activation of the periaqueductal gray matter. From these results, we conclude that during the sexual act, differential brain responses across genders are principally related to the stimulatory (plateau) phase and not to the orgasmic phase itself. These results add to a better understanding of the neural underpinnings of human sexuality, which might benefit treatment of psychosexual disorders. Hum Brain Mapp 2009. © 2009 Wiley‐Liss, Inc.

[1]  B. Everitt,et al.  Increased expression of c-fos in the medial preoptic area after mating in male rats: Role of afferent inputs from the medial amygdala and midbrain central tegmental field , 1992, Neuroscience.

[2]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[3]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[4]  R. Woods,et al.  Gender effects on cortical thickness and the influence of scaling , 2006, Human brain mapping.

[5]  Hanna Damasio,et al.  Sexual dimorphism and asymmetries in the gray–white composition of the human cerebrum , 2003, NeuroImage.

[6]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[7]  L. Marson,et al.  Identification of neural circuits involved in female genital responses in the rat: a dual virus and anterograde tracing study. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[8]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[9]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

[11]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[12]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[13]  J. A. den Boer,et al.  Interscan Displacement-Induced Variance in PET Activation Data Is Excluded by a Scan-Specific Attenuation Correction , 2002, NeuroImage.

[14]  Alan C. Evans,et al.  Changes in brain activity related to eating chocolate: from pleasure to aversion. , 2001, Brain : a journal of neurology.

[15]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

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

[17]  E. Gizewski,et al.  Serial neurochemical measurement of cerebrospinal fluid during the human sexual response cycle , 2006, The European journal of neuroscience.

[18]  K. Zilles,et al.  Somatotopy and Attentional Modulation of the Human Parietal and Opercular Regions , 2004, The Journal of Neuroscience.

[19]  L. Coolen,et al.  Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison , 1996, Brain Research.

[20]  G. Ettlinger,et al.  The neural structures involved in cross-modal recognition and tactile discrimination performance: An investigation using 2-DG , 1989, Behavioural Brain Research.

[21]  N. Wagner,et al.  Written descriptions of orgasm: A study of sex differences , 1976, Archives of sexual behavior.

[22]  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.

[23]  M. Schedlowski,et al.  NEUROENDOCRINE AND CARDIOVASCULAR RESPONSE TO SEXUAL AROUSAL AND ORGASM IN MEN , 1998, Psychoneuroendocrinology.

[24]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

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

[26]  Alan C. Evans,et al.  Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space , 1999, NeuroImage.

[27]  G. Holstege,et al.  The emotional motor system. , 1996, Progress in brain research.

[28]  N. Alpert,et al.  Anger in healthy men: a PET study using script-driven imagery , 1999, Biological Psychiatry.

[29]  L. Cahill Why sex matters for neuroscience , 2006, Nature Reviews Neuroscience.

[30]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[31]  N. Costes,et al.  Brain processing of visual sexual stimuli in treated and untreated hypogonadal patients , 2005, Psychoneuroendocrinology.

[32]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[33]  Rebecca C. Knickmeyer,et al.  Sex Differences in the Brain: Implications for Explaining Autism , 2005, Science.

[34]  R. Aloni,et al.  A review of the effect of traumatic brain injury on the human sexual response. , 1999, Brain injury.

[35]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[36]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[37]  A. M. Graybiel,et al.  Sensory maps in the claustrum of the cat , 1980, Nature.

[38]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[39]  Gert Holstege,et al.  Human brain activation during sexual stimulation of the penis , 2005, The Journal of comparative neurology.

[40]  W. Dimpfel,et al.  Gender difference in electrical brain activity during presentation of various film excerpts with different emotional content. , 2003, European journal of medical research.

[41]  Karl J. Friston,et al.  Activation of reward circuitry in human opiate addicts , 1999, The European journal of neuroscience.

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

[43]  D. Pfaff,et al.  Facilitation of female reproductive behavior from mesensephalic central gray in the rat. , 1979, The American journal of physiology.

[44]  Y. Binik,et al.  The nature of human orgasm: a critical review of major trends. , 2001, Clinical psychology review.

[45]  A. Ishai,et al.  Distributed neural systems for the generation of visual images , 2000, NeuroImage.

[46]  E. Rolls,et al.  Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. , 2003, Cerebral cortex.

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

[48]  K. Mckenna,et al.  Central nervous system innervation of the penis as revealed by the transneuronal transport of pseudorabies virus , 1993, Neuroscience.

[49]  S. Newman The Medial Extended Amygdala in Male Reproductive Behavior A Node in the Mammalian Social Behavior Network , 1999, Annals of the New York Academy of Sciences.

[50]  T. P. S. Powell,et al.  The organization of the connections between the cortex and the claustrum in the monkey , 1982, Brain Research.

[51]  C. Keysers,et al.  Empathy and the Somatotopic Auditory Mirror System in Humans , 2006, Current Biology.

[52]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

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

[54]  M. Kringelbach The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[55]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[56]  P. Bladin,et al.  Hypersexuality after Temporal Lobe Resection , 2002, Epilepsy & Behavior.

[57]  S. Newman,et al.  Fos-Immunoreactivity within the Extended Amygdala Is Correlated with the Onset of Sexual Satiety , 1998, Hormones and Behavior.

[58]  D. Pfaff,et al.  Mesencephalic mechanisms for integration of female reproductive behavior in the rat. , 1979, The American journal of physiology.

[59]  Janniko R. Georgiadis,et al.  Brain activation during human male ejaculation revisited , 2006, Neuroreport.

[60]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[61]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[62]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[63]  Andreas Bartels,et al.  The neural correlates of maternal and romantic love , 2004, NeuroImage.

[64]  The claustrum/insula region integrates conceptually related sounds and pictures , 2007, Neuroscience Letters.

[65]  Gert Holstege,et al.  Regional cerebral blood flow changes associated with clitorally induced orgasm in healthy women , 2006, The European journal of neuroscience.

[66]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[67]  P E Roland,et al.  Cross-Modal Transfer of Information between the Tactile and the Visual Representations in the Human Brain: A Positron Emission Tomographic Study , 1998, The Journal of Neuroscience.

[68]  Gert Holstege,et al.  Chapter 1 The emotional motor system , 1996 .

[69]  L. Marson Central nervous system neurons identified after injection of pseudorabies virus into the rat clitoris , 1995, Neuroscience Letters.

[70]  L. Derogatis,et al.  Sexual functioning following traumatic brain injury. , 1996, Brain injury.

[71]  O. Narkiewicz,et al.  Degenerations in the claustrum after regional neocortical ablations in the cat , 1964, The Journal of comparative neurology.

[72]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[73]  S. Newman,et al.  Mating-induced expression of c-fos in the male Syrian hamster brain: role of experience, pheromones, and ejaculations. , 1997, Journal of neurobiology.

[74]  E. Laumann,et al.  Sexual dysfunction in the United States: prevalence and predictors. , 1999, JAMA.

[75]  S. Hite The Hite Report: A Nationwide Study of Female Sexuality , 1981 .

[76]  J. Tiihonen,et al.  Increase in cerebral blood flow of right prefrontal cortex in man during orgasm , 1994, Neuroscience Letters.

[77]  Michael Forsting,et al.  There are differences in cerebral activation between females in distinct menstrual phases during viewing of erotic stimuli: a fMRI study , 2006, Experimental Brain Research.

[78]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[79]  Y. Binik,et al.  Do all orgasms feel alike? Evaluating a two‐dimensional model of the orgasm experience across gender and sexual context , 2002, Journal of sex research.

[80]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[82]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[83]  V. Sadock The Social Organization of Sexuality: Sexual Practices in the United States , 1995 .

[84]  C. Koch,et al.  What is the function of the claustrum? , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[86]  M. Schedlowski,et al.  Cardiovascular and endocrine alterations after masturbation-induced orgasm in women. , 1999, Psychosomatic medicine.

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