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• W1982071551 abstract "Face perception is mediated by a distributed neural system in the human brain [1Haxby J.V. Hoffman E.A. Gobbini I.M. The distributed human neural system for face perception.Trends Cogn. Sci. 2000; 4: 223-233Abstract Full Text Full Text PDF PubMed Scopus (3264) Google Scholar, 2Ishai A. Schmidt C.F. Boesiger P. Face perception is mediated by a distributed cortical network.Brain Res. Bull. 2005; 67: 87-93Crossref PubMed Scopus (293) Google Scholar]. The response to faces is modulated by cognitive factors such as attention, visual imagery, and emotion [3Ishai A. Ungerleider L.G. Haxby J.V. Distributed neural systems for the generation of visual images.Neuron. 2000; 28: 979-990Abstract Full Text Full Text PDF PubMed Scopus (446) Google Scholar, 4Ishai A. Haxby J.V. Ungerleider L.G. Visual imagery of famous faces: Effects of memory and attention revealed by fMRI.Neuroimage. 2002; 17: 1729-1741Crossref PubMed Scopus (242) Google Scholar, 5Vuilleumier P. Armony J.L. Driver J. Dolan R.J. Effects of attention and emotion on face processing in the human brain: An event-related fMRI study.Neuron. 2001; 30: 829-841Abstract Full Text Full Text PDF PubMed Scopus (1287) Google Scholar, 6Ishai A. Pessoa L. Bikle P.C. Ungerleider L.G. Repetition suppression of faces is modulated by emotion.Proc. Natl. Acad. Sci. USA. 2004; 101: 9827-9832Crossref PubMed Scopus (219) Google Scholar]; however, the effects of gender and sexual orientation are currently unknown. We used fMRI to test whether subjects would respond more to their sexually preferred faces and predicted such modulation in the reward circuitry. Forty heterosexual and homosexual men and women viewed photographs of male and female faces and assessed facial attractiveness. Regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Within multiple, bilateral face-selective regions in the visual cortex, limbic system, and prefrontal cortex, similar patterns of activation were found in all subjects in response to both male and female faces. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in the thalamus and medial orbitofrontal cortex, where heterosexual men and homosexual women responded more to female faces and heterosexual women and homosexual men responded more to male faces. Our findings suggest that sexual preference modulates face-evoked activation in the reward circuitry. Face perception is mediated by a distributed neural system in the human brain [1Haxby J.V. Hoffman E.A. Gobbini I.M. The distributed human neural system for face perception.Trends Cogn. Sci. 2000; 4: 223-233Abstract Full Text Full Text PDF PubMed Scopus (3264) Google Scholar, 2Ishai A. Schmidt C.F. Boesiger P. Face perception is mediated by a distributed cortical network.Brain Res. Bull. 2005; 67: 87-93Crossref PubMed Scopus (293) Google Scholar]. The response to faces is modulated by cognitive factors such as attention, visual imagery, and emotion [3Ishai A. Ungerleider L.G. Haxby J.V. Distributed neural systems for the generation of visual images.Neuron. 2000; 28: 979-990Abstract Full Text Full Text PDF PubMed Scopus (446) Google Scholar, 4Ishai A. Haxby J.V. Ungerleider L.G. Visual imagery of famous faces: Effects of memory and attention revealed by fMRI.Neuroimage. 2002; 17: 1729-1741Crossref PubMed Scopus (242) Google Scholar, 5Vuilleumier P. Armony J.L. Driver J. Dolan R.J. Effects of attention and emotion on face processing in the human brain: An event-related fMRI study.Neuron. 2001; 30: 829-841Abstract Full Text Full Text PDF PubMed Scopus (1287) Google Scholar, 6Ishai A. Pessoa L. Bikle P.C. Ungerleider L.G. Repetition suppression of faces is modulated by emotion.Proc. Natl. Acad. Sci. USA. 2004; 101: 9827-9832Crossref PubMed Scopus (219) Google Scholar]; however, the effects of gender and sexual orientation are currently unknown. We used fMRI to test whether subjects would respond more to their sexually preferred faces and predicted such modulation in the reward circuitry. Forty heterosexual and homosexual men and women viewed photographs of male and female faces and assessed facial attractiveness. Regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Within multiple, bilateral face-selective regions in the visual cortex, limbic system, and prefrontal cortex, similar patterns of activation were found in all subjects in response to both male and female faces. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in the thalamus and medial orbitofrontal cortex, where heterosexual men and homosexual women responded more to female faces and heterosexual women and homosexual men responded more to male faces. Our findings suggest that sexual preference modulates face-evoked activation in the reward circuitry. Regardless of their gender or sexual orientation, all subjects assessed the attractiveness of both male and female faces in a similar way, as reflected by their response latencies (Figure 1). Longer reaction times were associated with attractive rather than unattractive faces (p < 0.0001 for both male and female faces, in all groups of subjects). On average, all subjects rated 45% of the female faces as neutral, 28% as attractive, and 27% as unattractive. Similarly, all subjects rated 45% of the male faces as neutral, 20% as attractive, and 35% as unattractive (Table 1). The interaction between the sexual preference of the subject and the attractiveness rating was not statistically significant (F3,36 = 0.308, p = 0.82).Table 1Assessment of Facial AttractivenessFemale FacesMale FacesUNAUNAHeW25 (5)47 (3)28 (4)34 (7)45 (5)21 (4)HoW18 (5)47 (4)35 (6)42 (9)43 (6)15 (4)HeM30 (5)42 (2)28 (5)33 (6)50 (5)17 (4)HoM36 (4)45 (3)19 (3)33 (4)42 (2)25 (2)Mean percentage of button presses, averaged across ten subjects in each group, is shown for unattractive (U), neutral (N) and attractive (A) faces. Standard deviations are indicated in parenthesis. Open table in a new tab Mean percentage of button presses, averaged across ten subjects in each group, is shown for unattractive (U), neutral (N) and attractive (A) faces. Standard deviations are indicated in parenthesis. Face perception evoked activation in a distributed network that included regions in the visual cortex, limbic system, prefrontal cortex, and reward circuitry (Table 2). We found significant activation in multiple, bilateral face-responsive regions in all subjects and analyzed the effects of stimulus gender and attractiveness scores within these regions; Figure 2 shows the patterns of activation during the attractiveness rating in the lateral fusiform gyrus and the amygdala. In both regions, assessing the attractiveness of female and male faces evoked similar activation. Moreover, in both regions, attractive female faces evoked stronger activation than unattractive female faces (p < 0.001, in HeW [heterosexual women], HoW [homosexual women], and HeM [heterosexual men] groups). Similar findings were found in other face-selective regions (e.g., inferior occipital gyrus, superior temporal sulcus, insula, and inferior frontal gyrus), where the effects of stimulus gender (male or female face) and sexual preference (heterosexual or homosexual) were not statistically significant.Table 2A Network of Face-Responsive RegionsRegionNVolume, cm3 (Mean, SEM)x (Mean, SEM)y (Mean, SEM)z (Mean, SEM)L IOG4012.3 (0.3)−36.0 (0.8)−75.2 (1.0)−12.9 (0.8)R IOG4013.1 (0.1)36.7 (0.8)−74.7 (0.9)−12.3 (0.7)L FG4012.0 (0.3)−36.8 (0.5)−46.0 (0.7)−18.5 (0.6)R FG4012.9 (0.1)37.3 (0.6)−47.7 (0.9)−17.9 (0.5)L STS244.7 (0.6)−49.0 (0.9)−44.9 (1.7)7.6 (1.3)R STS365.4 (0.5)46.2 (0.7)−41.1 (1.4)6.8 (0.9)L AMG389.2 (0.5)−15.8 (0.4)−7.8 (0.6)−8.1 (0.7)R AMG399.6 (0.5)16.6 (0.6)−7.3 (0.4)−9.1 (0.3)L IPS368.5 (0.7)−31.4 (1.1)−49.3 (1.5)42.2 (0.9)R IPS368.7 (0.6)31.3 (0.9)−51.1 (1.5)40.9 (0.9)mdT337.3 (0.7)1.0 (0.2)−11.5 (0.8)12.8 (0.5)L caudate275.5 (0.6)−11.9 (0.5)−1.1 (1.0)16.6 (0.8)R caudate324.8 (0.6)12.7 (0.5)−1.5 (1.0)17.4 (0.7)L IFG407.9 (0.6)−38.7 (0.7)2.7 (1.2)32.4 (0.9)R IFG3910.6 (0.4)40.5 (0.8)1.4 (0.8)32.0 (0.9)L putamen216.1 (0.7)−20.4 (0.7)4.8 (1.0)3.3 (0.6)R putamen206.1 (0.8)21.3 (0.7)4.3 (0.8)4.1 (0.9)ACC3711.4 (0.3)0.5 (0.4)13.7 (1.2)46.3 (1.0)L insula397.3 (0.5)−33.2 (0.7)19.1 (1.4)6.7 (0.7)R insula408.9 (0.5)35.3 (0.7)17.9 (0.9)7.0 (0.6)OFC358.9 (0.7)1.1 (0.3)58.5 (0.7)1.2 (0.9)Clusters were localized based on the main effect of faces (p < 0.01, uncorrected). N indicates the number of subjects who showed significant activation in each region. Volumes were calculated before spatial normalization. Coordinates are in the normalized space of the Talairach brain atlas 26Talairach J. Tournoux P. Co-Planar Stereotaxis Atlas of the Human Brain. Thieme Medical, New York1988Google Scholar. The standard error of the mean is indicated in parentheses. L = left, R = right. Open table in a new tab Clusters were localized based on the main effect of faces (p < 0.01, uncorrected). N indicates the number of subjects who showed significant activation in each region. Volumes were calculated before spatial normalization. Coordinates are in the normalized space of the Talairach brain atlas 26Talairach J. Tournoux P. Co-Planar Stereotaxis Atlas of the Human Brain. Thieme Medical, New York1988Google Scholar. The standard error of the mean is indicated in parentheses. L = left, R = right. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in two regions, namely the mediodorsal nucleus of the thalamus (mdT) and the medial orbitofrontal cortex (OFC). Within the OFC, attractive faces evoked significantly stronger activation (the mean response ± SEM, averaged across all subjects, was 0.97 ± 0.08) than neutral (0.84 ± 0.08, p < 0.01) and unattractive (0.86 ± 0.09, p < 0.01) faces. Because most faces presented during the attractiveness task were rated “neutral,” our interaction analysis included the mean responses evoked by all male and all female faces. Figure 3 shows the patterns of activation in mdT (A) and the OFC (B). In both regions, although male faces evoked stronger responses than female faces in HeW and HoM, HoW and HeM responded more to female than to male faces. The mean amplitude of the fMRI signal in response to male and female faces, averaged across all subjects in a group whose members showed activation in each region, is shown in Figure 3C. In both regions, the difference between activation evoked by male faces and activation evoked by female faces was significant in HoW (p < 0.04), HeM (p < 0.001), and HoM (p < 0.01), but not in HeW. The interaction between stimulus gender (male or female face) and the sexual preference (hetero- or homosexual) of the subject was highly significant in mdT (p < 0.01) and in the OFC (p < 0.001). To illustrate the effects of sexual preference in each group, we subtracted the mean amplitude of the fMRI response evoked by male faces from the mean amplitude of the fMRI response evoked by female faces (Figure 3D). Contrasting the response to male faces with the response to female faces did not reveal any significant cluster of activation in the brain, even when the threshold was lowered to p < 0.05 at both the subject and the group level. Furthermore, the interaction between the gender of the subject (male versus female), regardless of their sexual preference, and the gender of the stimulus (male vs. female faces) was not statistically significant. The patterns of activation in the mdT and the OFC therefore suggest that the response to faces within these regions was modulated by the sexual preference of the subject. Consistent with previous functional neuroimaging studies, our data indicate that face perception evokes activation in a distributed cortical network [1Haxby J.V. Hoffman E.A. Gobbini I.M. The distributed human neural system for face perception.Trends Cogn. Sci. 2000; 4: 223-233Abstract Full Text Full Text PDF PubMed Scopus (3264) Google Scholar, 2Ishai A. Schmidt C.F. Boesiger P. Face perception is mediated by a distributed cortical network.Brain Res. Bull. 2005; 67: 87-93Crossref PubMed Scopus (293) Google Scholar] that includes regions in the visual cortex, limbic system, and prefrontal cortex, where invariant (facial identity) and variant (gaze direction and facial expression) features are processed [7Grill-Spector K. Knouf N. Kanwisher N. The fusiform face area subserves face perception, not generic within-category identification.Nat. Neurosci. 2004; 7: 555-562Crossref PubMed Scopus (696) Google Scholar, 8Hoffman E.A. Haxby J.V. Distinct representation of eye gaze and identity in the distributed human neural system for face perception.Nat. Neurosci. 2000; 3: 80-84Crossref PubMed Scopus (943) Google Scholar, 9Phillips M.L. Young A.W. Senior C. Brammer M. Andrew C. Calder A.J. Bullmore E.T. Perrett D.I. Rowland D. Williams S.C.R. et al.A specific neural substrate for perceiving facial expressions of disgust.Nature. 1997; 389: 495-498Crossref PubMed Scopus (1211) Google Scholar], and regions in prefrontal cortex and the reward circuitry, where the assessment of facial beauty is processed [10Nakamura K. Kawashima R. Nagumo S. Ito K. Sugiura M. Kato T. Nakamura A. Hatano K. Kubota K. Fukuda H. et al.Neuroanatomical correlates of the assessment of facial attractiveness.Neuroreport. 1998; 9: 753-757Crossref PubMed Scopus (69) Google Scholar, 11Aharon I. Etcoff N. Ariely D. Chabris C.F. O'Connor E. Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence.Neuron. 2001; 32: 537-551Abstract Full Text Full Text PDF PubMed Scopus (774) Google Scholar, 12Kampe K.K. Frith C.D. Dolan R.J. Frith U. Reward value of attractiveness and gaze.Nature. 2001; 413: 589Crossref PubMed Scopus (333) Google Scholar, 13O'Doherty J. Winston J. Critchley H.D. Perrett D. Burt D.M. Dolan R.J. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness.Neuropsychologia. 2003; 41: 147-155Crossref PubMed Scopus (630) Google Scholar]. Given the benefits of facial beauty in mating [14Perrett D.I. Lee K.J. Penton-Voak I. Rowland D. Yoshikawa S. Burt D.M. Henzi S.P. Castles D.L. Akamatsu S. Effects of sexual dimorphism on facial attractiveness.Nature. 1998; 394: 884-887Crossref PubMed Scopus (902) Google Scholar, 15Senior C. Beauty in the brain of the beholder.Neuron. 2003; 38: 525-528Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar], we postulated differential patterns of activation in the heterosexual and homosexual brain in response to faces of the same or opposite sex. Interestingly, all subjects, regardless of their gender or sexual preference, showed virtually identical patterns of neural activation within multiple, bilateral face-selective regions, where male and female faces elicited responses of similar magnitude. It therefore seems that the gender of face stimuli is processed similarly in the cortical network that mediates face perception. Facial beauty is considered a marker for reproductive fitness [16Thornhill R. Gangestad S.W. Facial attractiveness.Trends Cogn. Sci. 1999; 3: 452-460Abstract Full Text Full Text PDF PubMed Scopus (683) Google Scholar]. Attributes such as symmetry [17Langlois J.H. Roggman L.A. Attractive faces are only average.Psychol. Sci. 1990; 1: 115-121Crossref Scopus (854) Google Scholar] and sexually dimorphic features [14Perrett D.I. Lee K.J. Penton-Voak I. Rowland D. Yoshikawa S. Burt D.M. Henzi S.P. Castles D.L. Akamatsu S. Effects of sexual dimorphism on facial attractiveness.Nature. 1998; 394: 884-887Crossref PubMed Scopus (902) Google Scholar] contribute to the assessment of facial attractiveness. Not surprisingly, recent studies have reported that facial beauty evokes activation in the reward circuitry [11Aharon I. Etcoff N. Ariely D. Chabris C.F. O'Connor E. Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence.Neuron. 2001; 32: 537-551Abstract Full Text Full Text PDF PubMed Scopus (774) Google Scholar, 13O'Doherty J. Winston J. Critchley H.D. Perrett D. Burt D.M. Dolan R.J. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness.Neuropsychologia. 2003; 41: 147-155Crossref PubMed Scopus (630) Google Scholar]. It has been suggested that the rewarding, adaptive value of an attractive face can be dissociated from its aesthetic value. An attractive opposite-sex face may signal that a potential sexual partner has a healthy genotype, whereas an attractive, same-sex face cannot have such reproductive benefits [15Senior C. Beauty in the brain of the beholder.Neuron. 2003; 38: 525-528Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar]. Our subjects, regardless of their gender or sexual orientation, similarly assessed the attractiveness of both male and female faces, suggesting that men and women equally notice and respond to beauty of the same and opposite sex. Similar behavioral findings were found in a group of heterosexual men [11Aharon I. Etcoff N. Ariely D. Chabris C.F. O'Connor E. Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence.Neuron. 2001; 32: 537-551Abstract Full Text Full Text PDF PubMed Scopus (774) Google Scholar] and a group of male and female subjects [13O'Doherty J. Winston J. Critchley H.D. Perrett D. Burt D.M. Dolan R.J. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness.Neuropsychologia. 2003; 41: 147-155Crossref PubMed Scopus (630) Google Scholar]. The virtually identical attractiveness rating of both male and female faces was reflected not only by the response latencies but, importantly, by the amplitude of the fMRI signal. Within a network of face-selective regions that included the lateral fusiform gyrus and the amygdala, unattractive, neutral, and attractive male and female faces elicited very similar activation. In contrast with previous studies that assumed automatic processing of facial beauty and instructed subjects to judge the gender of face stimuli (e.g., [13O'Doherty J. Winston J. Critchley H.D. Perrett D. Burt D.M. Dolan R.J. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness.Neuropsychologia. 2003; 41: 147-155Crossref PubMed Scopus (630) Google Scholar]), we chose a different approach, namely explicit assessment of facial attractiveness, so that the gender of the face stimulus was irrelevant to the task. We postulated that if face processing is indeed modulated by the gender or sexual preference of the subject, an interaction with the gender of the stimulus would be observed in regions such as the amygdala and the OFC. To our surprise, we did not observe differences between the neural responses evoked by male faces and those evoked by female faces in the amygdala. We did, however, observe a significant interaction between stimulus gender and sexual preference in the mdT and in the OFC. The OFC receives projections from the mdT, with which it is reciprocally connected [18Fuster J.M. The Prefrontal Cortex. Raven Press, New York1997Google Scholar], and thus the similar patterns of activation observed in these regions can be explained in terms of their anatomical connections. The OFC is involved in representing the reward value of various sensory stimuli [19Rolls E.T. The functions of the orbitofrontal cortex.Brain Cogn. 2004; 55: 11-29Crossref PubMed Scopus (834) Google Scholar], including beautiful faces [13O'Doherty J. Winston J. Critchley H.D. Perrett D. Burt D.M. Dolan R.J. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness.Neuropsychologia. 2003; 41: 147-155Crossref PubMed Scopus (630) Google Scholar], and abstract positive and negative reinforcers [20O'Doherty J. Kringelbach M.L. Rolls E.T. Hornak J. Andrews C. Abstract reward and punishment representations in the human orbitofrontal cortex.Nat. Neurosci. 2001; 4: 95-102Crossref PubMed Scopus (1515) Google Scholar]. A recent fMRI study has shown that passive viewing of various face stimuli is sufficient to evoke significant activation in the OFC [2Ishai A. Schmidt C.F. Boesiger P. Face perception is mediated by a distributed cortical network.Brain Res. Bull. 2005; 67: 87-93Crossref PubMed Scopus (293) Google Scholar]. The existence of face-selective neurons in the OFC [21Thorpe S.J. Rolls E.T. Maddison S. Neuronal activity in the orbitofrontal cortex of the behaving monkey.Exp. Brain Res. 1983; 49: 93-115Crossref PubMed Scopus (651) Google Scholar] and the inability of patients with OFC lesions to identify emotional facial expressions [22Hornak J. Rolls E.T. Wade D. Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage.Neuropsychologia. 1996; 34: 247-261Crossref PubMed Scopus (587) Google Scholar] further suggest that this region has an important role in the processing of facial cues required for social communication. Modulation by sexual preference of the response to faces within the OFC extends its role in social behavior. It could be argued that the OFC is mediating the adaptive value of attractive, opposite-sex faces, and thus provides putative neural correlates for the assessment of potential mates for reproductive purposes. We, however, did not find neural evidence in support of such dissociation between attractive opposite-sex faces that reflect evolutionary benefits and attractive same-sex faces that reflect aesthetic appraisal of beauty [15Senior C. Beauty in the brain of the beholder.Neuron. 2003; 38: 525-528Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar]. Rather, our findings demonstrate that the OFC has a more general role in representing the reward value of faces of potential sexual partners, including same-sex mates, irrespective of reproduction. Our data indicate that although in heterosexual and homosexual men and women faces are similarly processed within a distributed cortical network, stronger activation in response to sexually preferred faces is found in the reward circuitry, where HeW and HoM respond more to male faces and HoW and HeM respond more to female faces. Although HeW exhibited the smallest difference between activation evoked by male faces and activation evoked by female faces, the differential neural responses in HeW were significantly different from the patterns of response in the HoW and were more similar to the activation patterns observed in HoM. Consistent with our findings, a recent study has shown that heterosexual women and homosexual men exhibited similar patterns of responses to putative pheromones [23Savic I. Berglund H. Lindstrom P. Brain response to putative pheromones in homosexual men.Proc. Natl. Acad. Sci. USA. 2005; 102: 7356-7361Crossref PubMed Scopus (247) Google Scholar]. Taken together, these results provide converging evidence that sexual preference, and not reproductive fitness, modulates neural responses to relevant stimuli in the adult human brain. Male and female face stimuli evoke similar neural activation within a distributed cortical network that includes visual, limbic, and prefrontal regions. Sexually relevant faces elicit stronger neural responses in the reward circuitry, where the value of stimuli is represented." @default.
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• W1982071551 title "Face Perception Is Modulated by Sexual Preference" @default.
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