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International Journal of Impotence Research (2006) 18, 452–457 & 2006 Nature Publishing Group All rights reserved 0955-9930/06 $30.00 www.nature.com/ijir

ORIGINAL ARTICLE Brain activation by visual erotic stimuli in healthy middle aged males

SW Kim1, DW Sohn1, Y-H Cho1, WS Yang2, K-U Lee2, R Juh3, K-J Ahn4, Y-A Chung5, S-I Han2, KH Lee6, CU Lee2 and J-H Chae2

1Department of , The Catholic University of Korea, Seoul, Korea; 2Department of Psychiatry, The Catholic University of Korea, Seoul, Korea; 3Department of Biomedical Engineering, The Catholic University of Korea, Seoul, Korea; 4Department of Radiology, The Catholic University of Korea, Seoul, Korea; 5Department of Nuclear Medicine, The Catholic University of Korea, Seoul, Korea and 6School of Biological Sciences, Seoul National University, Seoul, Korea

The objective of the present study was to identify brain centers, whose activity changes are related to erotic visual stimuli in healthy, heterosexual, middle aged males. Ten heterosexual, right-handed males with normal sexual function were entered into the present study (mean age 52 years, range 46–55). All potential subjects were screened over 1 h interview, and were encouraged to fill out questionnaires including the Brief Male Sexual Function Inventory. All subjects with a history of sexual disorder or were excluded. We performed functional brain magnetic resonance imaging (fMRI) in male volunteers when an alternatively combined erotic and nonerotic film was played for 14 min and 9 s. The major areas of activation associated with sexual arousal to visual stimuli were occipitotemporal area, anterior cingulate gyrus, insula, orbitofrontal cortex, caudate nucleus. However, and thalamus were not activated. We suggest that the nonactivation of hypothalamus and thalamus in middle aged males may be responsible for the lesser physiological arousal in response to the erotic visual stimuli. International Journal of Impotence Research (2006) 18, 452–457. doi:10.1038/sj.ijir.3901449; published online 9 February 2006

Keywords: functional MRI; brain center; middle aged male; erotic stimuli

Introduction including an objective measure of and erotic visual stimuli, as well as neutral and visually With the development of the functional imaging stimulating control segments using fMRI technology techniques such as positron emission tomography to evaluate regional brain activation during sexual (PET) or functional magnetic resonance imaging arousal. The major areas of activation associated with (fMRI), the knowledge for brain substrate for the tumescence were right insula/subinsular region, sexual response is accumulating.1,2 Park et al.3 had including the claustrum, caudate nucleus, putamen, investigated relationships between brain activation cingulate gyrus, occipito-temporal area, and hypo- and sexual response in 12 young males (mean thalamus. A study compared gender differences in age ¼ 23 years) with normal sexual function. They sexual stimuli showed that only for the male subjects reported that the activated brain areas by erotic visual had a significant activation of hypothalamus.4 stimuli were inferior frontal lobe, cingulate gyrus, Although the understanding for the brain substrate insula, corpus callosum, caudate nucleus, globus for sexual arousal has been much increased like these pallidus, inferior temporal lobe, and thalamus. studies, subject of all studies were limited into young Arnow et al.2 developed an experimental paradigm adults. Since the is very prevalent in older male than younger ones, it should be elucidated the aging-related changes of brain activa- Correspondence: Dr J-H Chae, Department of Psychiatry, tion by sexual stimuli.5 To identify brain regions College of Medicine, The Catholic University of Korea, St. where functional perturbations disrupt the regulation Mary’s Hospital, 62, Yeouido-dong, Youngdeungpo-gu, Seoul 150-713, Korea. of sexual arousal in patients with sexual arousal E-mail: [email protected] disorders, a study that is exploring the brain activa- Received 21 September 2005; revised 22 November 2005; tion in the middle aged males would be needed. accepted 13 December 2005; published online 9 February The objective of the present study was to identify 2006 brain centers, whose activity changes are related to Brain activation by visual erotic stimuli SW Kim et al 453 erotic visual stimuli in healthy, heterosexual middle The absence of physical disorders and of any aged males. Comparing with the findings reported in pharmacological treatment was checked through a the functional neuroimaging studies in young males, medical examination. The study design was explained different brain activation profiles would be ex- in detail and the selected subjects read and signed pected.2–4 informed consent before entering the study. All subjects with a history of or erectile dysfunction were excluded. The study proto- Methods col was approved by the institutional review board at St. Mary’s Hospital, The Catholic University of Korea. Subjects Ten heterosexual, right handed males with normal sexual function were entered into the present study Activation stimuli and MRI image acquisition (mean age 52 years, range 46–55). All potential We presented to the subjects a film clip, which subjects were screened over 1-h interview, and were lasted for 14 min and 9 s. This clip consisted of encouraged to fill out questionnaires including the alternating segments of relaxing scenes (R), sports Brief Male Sexual Function Inventory (Table 1).6 highlights (S) or sexually arousing erotic scenes (E)

Table 1 Brief male sexual function inventory

Sexual drive Let us define sexual drive as a feeling that may include No days Only a few Some days Most days Almost wanting to have a sexual experience ( or days every day intercourse), thinking about having sex, or feeling frustrated due to lack of sex 1. During the part 30 days, how many days have you for 01234 sexual drive? 2. During the past 30 days, how would you rate your level None at all Low Medium Medium High of sexual drive? high 01234

Erections 3. Over the part 30 days, how often have you had partial or Not at all A few Fairly often Usually Always full sexual when you were sexually stimulated times in any way? 01234 4. Over the past 30 days, when you had erections, how often 01234 were they firm enough to have ? 5. How much difficulty did you have getting an Did not get A lot of Some Little No during the past 30 days? erection at all difficulty difficulty difficulty difficulty 01234

Ejaculation 6. In the past 30 days, how much difficulty have you had Have had no A lot of Some Little No ejaculating when you have been sexually stimulated? sexual difficulty difficulty difficulty difficulty stimulation in past month 01234 7. In the past 30 days, how much did you consider the Did not climax Big Medium Small No amount of you ejaculate to be a problem for you? problem problem problem problem 01234

Problem assessment 8. In the past 30 days, to what extent have you considered Big problem Medium Small Very small No a lack of sex drive to be a problem? problem problem problem problem 01234 9. In the past 30 days, to what extent have you considered 01234 your ability to get and keep erections to be a problem? 10. In the past 30 days, to what extent have you considered 01234 your to be a problem?

Overall satisfaction 11. Overall, during the past 30 days, how satisfied have you Very Mostly Neutral or Mostly Very been with your ? dissatisfied dissatisfied mixed (about satisfied satisfied equally satisfied and dissatisfied) 01234

International Journal of Impotence Research Brain activation by visual erotic stimuli SW Kim et al 454 in the following order: S, R, E, R, E, R, S, R, S, R and were then convolved in space with a 3D isotopic E. The respective times for these segments in Gaussian kernel (full-width at half-maximum, seconds were: 129, 60, 120, 30, 120, 30, 120, 30, FWHM, of 8 mm) to improve the signal-to-noise 60, 30 and 120 (s). A number of considerations ratio and to accommodate for residual variations informed the design and specific stimuli. Given data in functional neuroantomy that usually persist suggesting that subject disengagement from emo- between subjects after spatial normalization. Effects tionally stimulating visual material under fMRI at each and every voxel were estimated using the conditions takes approximately 15 s, the S and E general linear model. Voxel values for each contrast segments were not contiguous and were separated yielded a statistical parametric map of the t statistic by a minimum of 30 s of R.7 The content of the erotic (SPMt), subsequently transformed to the unit nor- segments involved four types of sexual activities: mal distribution, SPM{Z}. A ‘random-effects model’ rear-entry intercourse, intercourse with the female was implemented to produce the E () minus in the superior position, , and sexual inter- N (neutral) contrasts. This model is implemented course with the male in the superior position. Of within SPM99 using a multi-stage approach. eight different sexual activity-depicted films, these The hypothalamus, thalamus, anterior cingulate four activities were associated with the highest level gyrus, occipitotemporal cortex, anterior temporal of perceived sexual arousal and penile erection in cortex, parietal cortex, , hippocampal for- a sample of 40 healthy males. Finally, in order to mation, orbitofrontal cortex, ventral striatum, the control possible anticipation effect, subjects were claustrum, the nucleus accumbens, the parietal not informed of the ordering of segments. lobules have all been shown to respond to sexually During fMRI sessions, the film clips were pre- explicit films in male subjects.2–4,8 For each of the sented to the subjects through a mirror located at the brain areas mentioned above, a set of coordinates was top of the head coil that receives video-images from calculated by taking the average for each orthogonal outside of the magnetic room. Echoplanar images axis X, Y and Z of reported Talairach coordinates.9 (EPI) were acquired on 1.5 T MRI system (Magentom Predetermined regions of interest (ROI) were limited Vision Plus, Siemens, Erlangen, Germany). Thirty by spheres having a radius of 9 mm and for center, the slices (5 mm thick) were acquired every 3.106 s in calculated average reported coordinates. For these an inclined axial plane, aligned with the AC-PC priori ROIs, height threshold was set at Po0.001 axis. These T2-weighted functional images (z ¼ 3.09), uncorrected for multiple comparisons. For were acquired using an EPI pulse sequence other brain areas, height threshold was set at Po0.05, (TR ¼ 0.6 ms, TE ¼ 60 ms, Flip 90, FOV ¼ 240 mm, corrected for multiple comparison. Matrix ¼ 64 Â 64). After functional scanning, high- resolution data were acquired via a T1-weighted 3D volume acquisition obtained using a gradient echo Results pulse sequence (TR ¼ 9.7 ms, TE ¼ 4 ms, Flip ¼ 12, FOV ¼ 240 mm, Matrix ¼ 200 Â 256). When the blood oxygen level dependent (BOLD) Data were analyzed using Statistical Parametric activity associated with viewing the emotionally Mapping (SPM99, Wellcome Department of Cogni- neutral film segment (S) was subtracted from that tive Neurology, London, UK). Scans were realigned associated with viewing the erotic segment (E), and spatially normalized using the standard Mon- significant (Po0001, uncorrected) loci of activation treal Neurological Institute (MNI) template. Images are listed in Table 2 and illustrated in Figures 1

Table 2 Brain regions with a differential activity in response to sexually explicit and emotionally neutral visual stimuli in healthy middle aged male subjects (pooled group data, N ¼ 10)

z-score x, y, z (mm) Regions

6.07 10 À60 58 Right Parietal Lobe (BA 7) 4.42 À58 À42 36 Left Supramarginal Gyrus (BA 40) 5.39 10 À90 24 Right Occipital Lobe, Cuneus (BA 19) 4.95 28 À6 68 Right Superior Frontal Gyrus (BA 6) 4.04 60 24 14 Right Inferior Frontal Gyrus (BA 45) 3.77 38 57 À8 Right Orbitofrontal Gyrus (BA 10) 4.14 À34 50 À6 Left Orbitofrontal Gyrus (BA 10) 3.95 À3 À4 41 Left Cingulate Gyrus (BA 24) 3.84 À12 8 6 Left Caudate Nucleus 3.18 10 8 6 Right Caudate Nucleus 3.61 60 12 0 Right Superior Temporal Gyrus 3.42 4 24 6 Right Corpus Callosum 3.31 38 À10 8 Right Insula (BA 13)

BA, Brodmann’s area.

International Journal of Impotence Research Brain activation by visual erotic stimuli SW Kim et al 455 ever, hypothalamus and thalamus were not acti- vated. Activation of the occipitotemporal area accords with results of recent functional study, in which emotionally laden visual stimuli elicited increased activation in this cortical region.11,12 Reiman et al.13 provided some evidence that the anterior cingulate gyrus is involved in the conscious experience of emotion. In functional neuroimaging study, the activation of anterior cingulate gyrus was highly correlated with the levels of perceived sexual arousal, which were related to the perceived urge to perform sexual actions.8 These results have been replicated in following studies using fMRI.2–4 Orbitofrontal cortex has been shown to be impli- cated in the representation of rewards.14 Redoute et al.8 suggested that the orbitofrontal activation noted in their PET study might have been related to the representation of the pleasant bodily sensations induced by penile tumescence. In the present study, the thalamus and hypotha- lamus were not activated. The afferent stimuli are routed to the cortex via the thalamus that regulates the flow of sensory information. Interestingly, the thalamus represents a hub from which any area in the cortex can communicate with any other brain regions. This extensive thalamocortical inter-con- nectivity has been theorized to constitute a neural basis for conscious awareness.15 If this hypothesis were correct, the thalamus would be implicated in the cognitive dimension of sexual arousal. One of the major thalamocortical interconnections is corti- co-striato-thalamo-cortical curcuit. Projections from the orbitofrontal cortex via the caudate nucleus, both of which are considered as inhibitory systems, is thought to mediate context-related operations and response inhibition.16 In light of such a view, the non-activation of thalamus, and activation of orbito- Figure 1 Brain areas whose activation was related to erotic- visual stimuli in healthy middle aged male subjects (pooled group frontal cortex and caudate nucleus in this study data, N ¼ 10). might suggest that middle aged males be more inhibited by thalamocortical interconnection and then less aroused to the visual sexual stimuli than and 2. The major areas of activation associated with young ones. A large number of studies have linked sexual arousal to visual stimuli were occipitotem- the hypothalamus to sexual response. Neuroanato- poral area, anterior cingulate gyrus, insula, orbito- mically, lesions in the medial preoptic area of the frontal cortex, caudate nucleus. However, hypothalamus impair male copulatory behavior hypothalamus and thalamus were not activated. in all species tested,17 and electrical stimulation of the paraventricular nucleus of the hypothalamus is associated with erection in rats.18 In addition, Discussion neurochemically, direct injection of apomorphine, dopamine agonist, into the paraventricular nucleus It has been proposed that sexual arousal, stimulates erections in the rats.19 Redoute et al.8 which is usually triggered by external stimuli or demonstrated a correlation between activation in the endogenous factors, is a multidimensional experi- hypothalamus and measures of penile tumescence ence comprised of four closely interrelated and in the PET study. Arnow et al.2 also reported similar coordinate component: cognitive, emotional, moti- results in the fMRI study. Interestingly, Karama vational, and physiological.8,10 et al.4 reported that the hypothalamus was less In the present study, the major areas of activation activated in female than in male in response to associated with sexual arousal to visual stimuli were visual sexual stimuli, and suggested that female occipitotemporal area, anterior cingulate gyrus, subjects were physiologically less aroused than insula, orbitofrontal cortex, caudate nucleus. How- male subjects. Yang20 examined the brain activation

International Journal of Impotence Research Brain activation by visual erotic stimuli SW Kim et al 456

Figure 2 Axial view of activated brain areas by erotic visual stimuli in healthy middle aged male subjects (pooled group data, N ¼ 10).

to the visual sexual stimuli in depressed patients known as primitive center for sexual arousal could with sexual dysfunction, and reported that hypotha- be exaggerated inhibition of the inhibitory system. lamus and thalamus were less activated than normal Regarding the limitations of the study, it should control group. Based on the results mentioned firstly be noted that we had studied only middle above, hypothalamic nonactivation in this study aged males and young control group were not for the middle aged males suggests that these included. Since our study design, (e.g. the lasting subjects were physiologically less aroused in re- time of erotic and neutral film segments) was very sponse to the erotic visual stimuli. Although similar to the previous works for the young ones, evidences for such inhibitory mechanisms over it would be possible to compare each others hypothalamus has been largely indirect and has indirectly.2,4 However, to control the variability of received much less attention than excitatory me- functional imaging research, the comparison study chanisms, a recent attempt to locate the specifically for middle aged and young adults at the same time sexual inhibitory effects of serotonin does have an should be needed. Secondly, we could not demon- inhibitory role in the lateral hypothalamic area.21 strate directly the inter-connectivity of particular This is consistent with the well-established inhibi- brain regions involving excitatory and inhibitory tory effects of specific serotonin re-uptake inhibitors system. Thus, our interpretations should be con- (SSRIs) on sexual response.22 sidered as a hypothesis to be tested in the future Considering extensive inter-connectivity of the more direct study focused on these brain circuitry. brain, and ‘dual control’ model over sexual re- Another limitation concerns the lack of objective sponse, one of the mechanisms of the nonactivation measures of the sexual arousal such as penile in the thalamus and hypothalamus, which are tumescence.

International Journal of Impotence Research Brain activation by visual erotic stimuli SW Kim et al 457 Conclusions 8 Redoute J, Stoleru S, Gregoire MC, Costes N, Cinotti L, Lavenne F et al. Brain processing of visual sexual stimuli in human males. Hum Brain Mapping 2000; 11: 162–177. We have identified by using fMRI, for the first time, 9 Talairach J, Tournoux P. Co-planar Stereotaxic Atlas of The the functional neuroanatomy of the brain associated Human Brain. Stuttgart: Thieme, 1988. with sexual arousal in middle aged males. The result 10 Stoleru S, Gregoire MC, Gerard D, Decety J, Lafarge E, was the activation of occipitotemporal gyrus, ante- Cinotti L et al. Neuroanatomical correlates of visually evoked rior cingulate gyrus, orbitofrontal cortex, and non- sexual arousal in human males. Arch Sex Behav 1999; 28: 1–21. activation of hypothalamus and thalamus. We 11 Lane RD, Reiman EM, Ahern GL, Schwartz GE, Davidson RJ. suggest that the nonactivation of hypothalamus Neuroanatomical correlates of happiness, sadness, and dis- and thalamus in middle aged males may be gust. Am J Psychiatry 1997; 154: 926–933. responsible for the lesser physiological arousal in 12 Beauregard M. The functional neuroanatomy of amusement, disgust and sexual arousal. In: The 4th International Con- response to the erotic visual stimuli. ference on Functional Mapping of the Human Brain. Mon- treal, Canada, 1988, p 7. 13 Reiman EM, Lane RD, Ahern GL, Schwartz GE, Davidson RJ, Acknowledgments Friston KJ. Neuroanatomical correlates of externally and internally generated human emotion. Am J Psychiatry 1997; 154: 918–925. This work was supported by Grant No. R01-2003- 14 Francis S, Rolls ET, Bowtell R, McGlone F, O’Doherty J, 000-10432-0 from the Basic Research Program of the Browning A et al. The representation of pleasant touch in the Korea Science & Engineering Foundation. brain and its relationship with taste and olfactory areas. Neuroreport 1999; 10: 453–459. 15 Linas R, Ribary U, Contreras D, Pedroarena C. The neuronal basis for consciousness. Philos Trans R Soc London B Biol Sci References 1998; 353: 1841–1849. 16 Stein DJ, Hollander E. Textbook of Anxiety Disorders. 1 Moseley ME, Glover GH. Functional MR imaging: capabilities American Psychiatric Publishing, Inc.: Washington, DC, and limitations. Neuroimaging Clin N Am 1995; 5: 161–191. 2002, 194p. 2 Arnow BA, Desmond JE, Banner LL, Glover GH, Solomon A, 17 Meisel RL. Effects of postweaning rearing condition on Polan ML et al. Brain activation and sexual arousal in healthy, recovery of copulatory behavior from lesions of the medial heterosexual males. Brain 2002; 125: 1014–1023. preoptic area in rats. Dev Psychobiol 1982; 15: 331–338. 3 Park K, Seo JJ, Kang HK, Ryu SB, Kim HJ, Jeong GW. A new 18 Chen KK, Chan SH, Chang LS, Chan JY. Participation of potential of blood oxygenation level dependent (BOLD) paraventricular nucleus of hypothalamus in central regulation functional MRI for evaluating cerebral centers of penile of penile erection in the rat. J Urol 1997; 158: 238–244. erection. Int J Impot Res 2001; 13: 73–81. 19 Argiolas A, Melis MR. Central control of penile erection: role 4 Karama S, Lecours AR, Leroux JM, Bourgouin P, Beaudoin G, of the paraventricular nucleus of the hypothalamus. Prog Joubert S et al. Areas of brain activation in males and females Neurobiol 2005; 76: 1–21. during viewing of erotic film excerpts. Human Brain Mapping 20 Yang JC. Functional neuroanatomy in depressed patients with 2002; 16: 1–13. sexual dysfunction: Blood oxygenation level dependent 5 Braun M, Wassmer G, Klotz T, Reifenrath B, Mathers M, functional MR imaging. Korean J Radiol 2004; 5: 87–95. Engelmann U. Epidemiology of erectile dysfunction: results of 21 Lorrain DS, Matuszewich L, Friedman R, Hull EM. Extra- the ‘Cologne Male Survey’. Int J Impot Res 2000; 12: 305–311. cellular serotonin in the lateral hypothalamic area increases 6 O’Leary MP, Fowler FJ, Lenderking WR, Barber B, Sagnier PP, during postejaculatory interval and impairs in Guess HA et al. A brief male sexual function inventory for male rats. J Neurosci 1997; 17: 9361–9366. urology. Urology 1995; 46(5): 697–706. 22 Hull EM, Lorrain DS, Du J, Matuszewich L, Lumley LA, 7 Garrett AS, Maddock RJ. Time-course of the subjective Putnam SK, Moses J. - interactions emotional response to aversive pictures: relevance to fMRI in the control of sexual behavior. Behav Brain Res 1999; 105: studies. Psychiatry Res 2001; 108: 39–48. 105–116.

International Journal of Impotence Research