In the present investigation, patterns of brain activation were generally consistent with those of previous research in showing that heterosexual and homosexual men’s responses to male and female erotic stimuli are quite distinct4,53,54. Furthermore, our results are consistent with recent past studies of male bisexuality (e.g. Rosenthal et al.63,64) in showing that bisexual men’s responses to male and female stimuli tend to be less distinct compared with monosexual men’s responses63,64. Here, however, these response patterns were demonstrated using fMRI activations in the ventral striatum (VS), providing an objective measure of valence.

Category Specificity in Heterosexual and Homosexual Men

Heterosexual men showed greater VS responses to erotic stimuli featuring women, and homosexual men showed greater VS responses to erotic stimuli featuring men. Further, these responses were consistent with subjective assessments of the same stimuli.

Compared with videos, pictures produced somewhat stronger differential VS responses between male and female stimuli, as indicated by larger effect sizes in monosexual region of interest analyses (Table 1) and the robustness of whole-brain findings. One potential explanation for this difference may be that the reliability of the pictures paradigm benefited from the larger number of stimuli used. Alternatively, it may be the case that the VS is more sensitive to briefly presented stimuli, which is consistent with both reward-prediction error77,78,79,80 as well as incentive salience models43 of dopamine and VS functioning. Indeed, while the VS is frequently active during both reward anticipation and consumption, the association is particularly strong when consumed rewards occur unexpectedly or are uncertain30, as might be the case for randomly presented pictures. Additionally, for some participants it could have been the case that wanting or desire responses were strongest at the beginning of a video presentation, but then decreased—or fluctuated—over the subsequent 15 seconds.

Comparing Bisexual and Monosexual Men

Compared with monosexual men, bisexual men reported relatively bisexual subjective response patterns for all stimuli. With respect to VS activity, significantly bisexual patterns were observed for both picture and video stimuli, but in different tests. Compared with monosexual men, bisexual men showed significantly greater VS activity to their less activating sex for video stimuli, but not for pictures. Bisexual men also showed significantly less differential activation between male and female sexual stimuli for picture stimuli, but not for videos. Thus, although not all relevant fMRI test results were statistically significant, overall VS activation patterns support the idea that the bisexual men had a more bisexual reward responses compared with the monosexual men.

Whole brain activation patterns

This study focused on the VS as the primary region of interest, but whole brain activation patterns in each group revealed similar category-specific responses in monosexual men, as well as non-specific responses in bisexual men. These findings are described below along with tentative reverse inferences regarding potential functional significances.

Neural responses to erotic pictures

Heterosexual men had no areas where male pictures produced significantly greater activity than did female pictures. The reverse direction subtraction of female > male pictures, however, revealed extensive activations spanning multiple brain areas. Activity in the right VS likely indicated positive incentive value towards female stimuli (see introduction). This focal VS cluster in the nucleus accumbens exhibited the most robust differential activation compared with all other clusters in the brain, outside of occipital cortex, which likely indicated visual attention81,82. Right fusiform and adjacent extrastriate cortices may have indicated face and body perception83,84,85. Subgenual anterior cingulate and left orbitofrontal cortices may have indicated positive valence27,86,87,88. Additionally, motor strip (i.e. precentral gyrus) may have indicated preparation of motor sequences or perhaps motor imagery89,90,91,92.

Similarly to the heterosexual group, homosexual men had no areas where nonpreferred pictures (i.e., female erotic images) produced significantly greater activity than did male pictures. The reverse direction subtraction of male > female pictures, however revealed extensive activations spanning multiple brain areas. Similarly to the results for heterosexual men, some of the most robust activity was observed in the VS (again, focally in the nucleus accumbens), albeit more bilaterally, and particularly in the left hemisphere. Anterior cingulate and medial orbitofrontal cortices may have indicated positive valence27,86,87,88. Bilateral caudate body and cerebellum may have indicated imagination and preparation of motor sequences90,93,94,95,96.

In contrast to the activation patterns obtained for heterosexual men, the bisexual group had no brain areas with significantly different activation between male and female erotic pictures. While this sort of pattern could result from averaging over a mixture of heterosexual and homosexual response profiles, evidence for distinctly bisexuality responses is suggested by region of interest analyses in the VS.

Neural responses to erotic videos

Heterosexual men had no areas where male videos produced significantly greater activity than did female videos. The reverse direction subtraction of female > male videos, however, revealed activations in bilateral superior temporal cortices, which likely indicated an auditory confound from more extensive and substantial vocalizations being present in female erotic videos76.

Similarly to heterosexual men, homosexual men showed auditory activations in response to female compared with male stimuli. However, they also showed activity in the parietal lobe toward female compared with male stimuli, with clusters observed in both the right angular and right supramarginal gyri. The functional significance of these activations is unclear, but could be tentatively interpreted as indicating either mentalizing or mirroring-related-cognition97,98,99,100,101,102,103.

More extensive activations were observed in homosexual men for areas of the brain responding more to male than female erotic videos. A small focal cluster was observed in the medial orbitofrontal cortex, which may indicate positive valence86. Activity was observed bilaterally (albeit was somewhat right-lateralized) in a larger cluster spanning both early and higher order visual areas including fusiform and extrastriate cortices, and parietal areas indicative of spatial attention, mental imagery, bodily sensations, and possibly mirroring84,85,97,98,99,100,101,102,103. Bilateral (but primarily right-lateralized) pre-motor cortex potentially indicated imagination and preparation of motor sequences90. It is unclear why homosexual men showed more extensive category-specific responses than did heterosexual men in response to erotic videos.

In contrast to the patterns obtained for heterosexual and homosexual men viewing erotic videos, bisexual men showed extensive activation patterns for both the female > male and male > female subtractions. For the female > male subtraction, similar auditory-related activity was observed as in heterosexual and homosexual men. An additional parietal cluster was observed in the right angular gyrus, with possible interpretations including mentalizing97,98,99,100,101,102,103. For the male > female subtraction, activity in the superior occipital cortex may have indicated visual attention81,82. Activity in the postcentral sulcus may have indicated bodily sensations105,106. Additionally, superior parietal lobule and supramarginal gyrus—more anteriodorsomedial than observed in the female > male contrast for homosexual men—may have indicated perception or imagination related to depicted sexual activities107,108. For bisexual men, erotic videos did not produce clear category-specific brain activity in one direction or another. It is further notable that there were significant findings not present for either heterosexual or homosexual participants, suggesting that bisexuals represent a group with distinct response profiles.

Limitations

While our initial sample size was large by the standards of neuroimaging studies of human sexuality, a number of subjects were excluded in order to ensure data quality. Consequently, our study may have been somewhat underpowered for detecting small (but potentially meaningful) effects.

The establishment of an appropriate baseline for activation represents an ongoing challenge for studies of the neural bases of sexual responses. An ideal baseline should produce similar affective (and cognitive) responses between groups. While fixation cross presentations and nature scenes likely represented adequate control conditions for erotic pictures and videos (respectively), some participants could have had significant processing differences during these baseline measurements. For example, since we did not measure genital responses in the scanner, we cannot rule out the possibility that some participants (and perhaps in particular bisexual participants) experienced significant erectile activity that continued after the presentation of arousing stimuli. This could have had the effect of reducing the magnitude of evoked responses for our minimum arousal tests.

Future work may benefit from using other kinds of appetitive stimuli as controls (e.g. appealing food or monetary rewards). This could potentially provide an overall measure of reward sensitivity. Additionally, these appetitive stimuli could also be used to create individually customized functional regions of interest. Theoretically, by using a localizer task to determine the most strongly reward-sensitive voxels in each person’s brain, it may be possible to generate a particularly sensitive measure of erotic preferences.

Future Directions

Consistency among neural measures of incentive value, subjective and genital arousal, and sexual identity supports the idea that male sexual orientation (in heterosexual, bisexual, and homosexual men) is motivated by patterns of sexual arousal and attraction1. One question that remains to be examined is the stability of these neural responses over time, both in terms of early development109, as well as throughout life110. Although it may seem ethically problematic to conduct such research in younger participants, one advantage of fMRI over other measures of sexual interest is the ability to both objectively and non-invasively measure valenced responses to non-explicit stimuli109,111.

It may be the case that attraction patterns (and patterns of VS activation to male versus female stimuli) of bisexual individuals change based on a variety of contextual factors112. Conceivably, for example, a bisexual person may exhibit more gynephilic or androphilic preferences depending on whether they have recently been romantically or sexually involved with women or men. Research measuring individuals over multiple time-points is needed to examine this (admittedly speculative) possibility. Furthermore, it would be especially informative to include fMRI measures alongside measures of genital and subjective responses in a longitudinal study.

In the present study, we focused on the VS as a measure of positive incentive value. Exploring the role of sexual aversion may also be an informative avenue for future investigations113. For example, is bisexuality partially related to lower levels of sexual aversion? A major challenge for conducting these investigations would be finding a brain area in which activity is specific to aversion, rather than general arousal or overall salience. In the past, regions such as the anterior insula activity have been used as a metric of disgust114, when general visceral emotionality would likely be a more valid inference with respect to this region115. Additionally—and not limited in its applications to studying aversion—multi-voxel classifier techniques might be valuable for inferring valence from more sparsely distributed activation patterns116,117,118.

Future investigations should also explore the degree of specificity of reward-related (and possibly aversion-related) brain activity in women of different sexual orientations. Women’s subjective and genital responses to erotic stimuli suggest that relatively bisexual patterns may be observed in women compared to men53,69,119. Bisexual erotic responses in women are further suggested by preliminary fMRI evidence in which monosexual women—contrasted with monosexual men—exhibited greater activity toward non-preferred erotic pictures in posterolateral putamen, dorsal striatum, and thalamus70. Functional neuroimaging focusing on the VS may be a particularly valuable converging line of evidence for studying sexual responses in women, as physiological arousal patterns have been difficult to interpret in light of their low correlation with subjective report120. In addition, neuroimaging may have unique advantages for directly comparing men and women in their sexual response patterns, as the same type of objective measurement can be performed on the same brain structures in both men and women.

Conclusion

Here we replicated previous findings of category-specific neural responses in heterosexual and homosexual men, and further provided evidence that bisexual men exhibit distinctly bisexual neural responses. This sample exhibited bisexual arousal patterns in prior analyses of subjective and genital measures63,64, and has now been shown to exhibit relatively bisexual ventral striatum (VS) activation patterns. Although mixed results have been obtained in studies of genital arousal patterns in bisexual men, this investigation found bisexual patterns of VS activity in a sample in which participants had been specifically screened for bisexual romantic and sexual histories. However, it should be noted that these findings were variable across different tests, with some tests failing to find evidence for distinct patterns in bisexual participants. Nonetheless, convergence between multiple modalities suggests that for the men studied here, bisexual identities are consistent with bisexual patterns of arousal and desire, similarly to monosexual men.