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The Human Sexual Response Cycle: Brain Imaging Evidence Linking Sex To Progress in Neurobiology 98 (2012) 49–81 Contents lists available at SciVerse ScienceDirect Progress in Neurobiology jo urnal homepage: www.elsevier.com/locate/pneurobio The human sexual response cycle: Brain imaging evidence linking sex to other pleasures a, b,c J.R. Georgiadis *, M.L. Kringelbach a Department of Neuroscience/Section Anatomy, University Medical Center Groningen (UMCG), University of Groningen, Groningen, The Netherlands b Department of Psychiatry, Warneford Hospital, University of Oxford, Oxford, UK c Centre for Functionally Integrative Neuroscience (CFIN), University of Arhus, Arhus, Denmark A R T I C L E I N F O A B S T R A C T Article history: Sexual behavior is critical to species survival, yet comparatively little is known about the neural Received 15 November 2011 mechanisms in the human brain. Here we systematically review the existing human brain imaging Received in revised form 21 April 2012 literature on sexual behavior and show that the functional neuroanatomy of sexual behavior is Accepted 8 May 2012 comparable to that involved in processing other rewarding stimuli. Sexual behavior clearly follows the Available online 15 May 2012 established principles and phases for wanting, liking and satiety involved in the pleasure cycle of other rewards. The studies have uncovered the brain networks involved in sexual wanting or motivation/ Keywords: anticipation, as well as sexual liking or arousal/consummation, while there is very little data on sexual Pleasure satiety or post-orgasmic refractory period. Human sexual behavior also interacts with other pleasures, Reward Emotion most notably social interaction and high arousal states. We discuss the changes in the underlying brain Sex networks supporting sexual behavior in the context of the pleasure cycle, the changes to this cycle over Object processing the individual’s life-time and the interactions between them. Overall, it is clear from the data that the Food functional neuroanatomy of sex is very similar to that of other pleasures and that it is unlikely that there Social interaction is anything special about the brain mechanisms and networks underlying sex. Orbitofrontal cortex ß 2012 Elsevier Ltd. All rights reserved. Brain networks Orgasm Arousal Interest Contents 1. Introduction . 50 1.1. The human sexual pleasure cycle and its relation to other pleasure cycles . 50 1.2. Human sexual behavior is a complex interaction between biology and culture . 54 1.3. Outline of review . 54 2. Wanting: Sensory gateways to sexual interest and arousal. 54 2.1. Auditory, olfactory, gustatory and somatosensory routes. 54 2.2. The visual route . 55 2.2.1. VSS in heterosexual men: Early object processing. 55 2.2.2. VSS in heterosexual men: Subcortical effects. 56 2.2.3. VSS in heterosexual men: Evaluative reward processing. 57 2.2.4. Summary of heterosexual male VSS effects . 58 2.2.5. VSS in heterosexual women: Menstrual cycle influences and gender differences . 59 Abbreviations: Amy, amygdala; pACC, anterior cingulate cortex, pregenual part; sACC, anterior cingulate cortex, subgenual part; ASL, arterial spin labelling; BOLD, blood oxygenation level dependent; Cb, cerebellum; Claus, claustrum; dlPFC, dorsolateral prefrontal cortex; dmPFC, dorsomedial prefrontal cortex; FO, frontal operculum; FBA/EBA, fusiform body area/extrastriate body area; HT, hypothalamus; IPC, intraparietal cortex; med-temp, medial temporal lobe; aMCC, middle cingulate cortex, anterior part; NAcc, nucleus accumbens; OFC, orbitofrontal cortex; PERT, post-ejaculatory (orgasmic) refractory period; MI, primary motor cortex; SI, primary somatosensory cortex; SPL, superior parietal lobule; vmPFC, ventral medial prefrontal cortex; VP, ventral pallidum; vPMC, ventral part of the premotor cortex; VS, ventral striatum; vlOT, ventrolateral occipitotemporal; VSS, visual sexual stimulation. * Corresponding author. E-mail address: [email protected] (J.R. Georgiadis). 0301-0082/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pneurobio.2012.05.004 50 J.R. Georgiadis, M.L. Kringelbach / Progress in Neurobiology 98 (2012) 49–81 3. Liking: Sexual arousal, consummation and climax. 60 3.1. Arousal: Sexual genital stimulation . 60 3.1.1. Sensory receptors in the human sexual organs . 60 3.1.2. Brain representation of genitals and pelvic floor motor control during sexual activity . 60 3.1.3. Penile erection: Critical contributions of the posterior insula–claustrum complex? . 61 3.1.4. Waves of sexual arousal and de-arousal with self-limited partnered penis stimulation . 61 3.1.5. Sexual clitoral and vaginal stimulation . 63 3.2. Orgasm . 63 3.2.1. A special note on orgasm in women . 63 3.2.2. Orgasm-specific activity in orbitofrontal and other prefrontal regions. 64 3.2.3. Pelvic muscular contractions and the cerebellum . 65 3.2.4. Sexual arousal linked to temporal and ventral prefrontal regions . 65 3.3. Summary of brain responses related to sexual consummation . 65 4. Satiety or post-orgasmic refractory period . 66 5. Variations of human sexual interest . 67 5.1. Homosexual preference . 67 5.2. Hyposexual desire. 68 5.3. Paedophilia . 68 6. Comparison of the human sexual response cycle to other reward cycles. 69 6.1. Comparison of sex and food cycles . 69 6.1.1. Identification of food and sex in the brain . 69 6.1.2. Sex and food anticipation . 70 6.1.3. Sex and food consummation. 70 6.1.4. Sex and food satiety . 70 6.2. Sex and social interaction. 71 6.3. Sex, drugs, and rock ‘n roll: pleasure, euphoria and arousal . 72 6.4. Life-time evolution of sex in relation to other pleasure cycles. 73 7. Conclusion . 74 References . 75 1. Introduction behavior.
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