Understanding heterosexual women’s erotic flexibility: the role of attention in sexual evaluations and neural responses to sexual stimuli. Janna A Dickenson, Lisa Diamond, Jace B King, Kay Jenson, Jeffrey S Anderson. Social Cognitive and Affective Neuroscience, Volume 15, Issue 4, April 2020, Pages 447–465, https://doi.org/10.1093/scan/nsaa058
Abstract: Many women experience desires, arousal and behavior that run counter to their sexual orientation (orientation inconsistent, ‘OI’). Are such OI sexual experiences cognitively and neurobiologically distinct from those that are consistent with one’s sexual orientation (orientation consistent, ‘OC’)? To address this question, we employed a mindful attention intervention—aimed at reducing judgment and enhancing somatosensory attention—to examine the underlying attentional and neurobiological processes of OC and OI sexual stimuli among predominantly heterosexual women. Women exhibited greater neural activity in response to OC, compared to OI, sexual stimuli in regions associated with implicit visual processing, volitional appraisal and attention. In contrast, women exhibited greater neural activity to OI, relative to OC, sexual stimuli in regions associated with complex visual processing and attentional shifting. Mindfully attending to OC sexual stimuli reduced distraction, amplified women’s evaluations of OC stimuli as sexually arousing and deactivated the superior cerebellum. In contrast, mindfully attending to OI sexual stimuli amplified distraction, decreased women’s evaluations of OI stimuli as sexually arousing and augmented parietal and temporo-occipital activity. Results of the current study constrain hypotheses of female erotic flexibility, suggesting that sexual orientation may be maintained by differences in attentional processing that cannot be voluntarily altered.
Keywords: sexual arousal, sexual orientation, fMRI, women, mindfulness, attention
Discussion
We found that OC, relative to OI, sexual stimuli elicited greater activity in brain regions involved in automatic visual processing, executive attention and appraisal whereas OI, relative to OC, sexual stimuli elicited greater activity in brain regions involved in complex visual processing and shifting attention. In contrast to our hypothesis that mindful attention would enhance the sexual processing of OI stimuli, results suggest that mindful attention augments women’s natural-occurring responses—increasing sexual evaluations of OC sexual stimuli but decreasing sexual evaluation of OI sexual stimuli.
Consistent with prior neuroimaging research on men’s processing of sexual stimuli (see Table 1), women’s neural responses to sexual, relative to neutral, stimuli activated regions associated with autonomic processing (midbrain, periaqueductal gray, posterior insula), attention (frontoparietal network, thalamus, anterior cingulate cortex, middle prefrontal cortex and lateral prefrontal cortex), appraisal (OFC, hippocampus), somatosensory awareness (anterior insula), motor imagery (cerebellum, premotor cortex) and deactivated areas involved in inhibition and devaluation (lateral temporal cortex, amygdala). These findings provide neurobiological support for the information processing model of the sexual response (e.g. see also Janssen et al., 2000; Chivers, 2017) and corroborate existing neurobiological models of sexual arousal (see Stoléru et al., 2012).
Differences across women’s OC and OI sexual processing
Importantly, women showed greater neural activity in the primary and secondary visual cortices and the thalamus. Primary and secondary visual areas are the first areas to receive visual input and the thalamus serves as a relay station to transmit relevant motor and sensory information to the cortex necessary for conscious awareness. These areas have been implicated in preconscious attention, precipitate male erectile responses, and are related to perceptions of arousal (see Table 1). Together, these findings suggest that women process OC stimuli on a more implicit level, marked by basic visual processing and implicit attention.
According to the IPM, preconscious visual attention serves to draw one’s attention to the sexual properties of the stimuli and trigger autonomic arousal and implicit appraisal. Although women showed greater neural activity associated with autonomic arousal in response to sexual, compared to neutral stimuli, these regions responded similarly to OC and OI sexual stimuli. On a neural level, women hold similar representations of autonomic or visceral responses across OC and OI sexual stimuli. This pattern of results indicates that women’s sexual orientation is more likely constrained by early implicit attention than by autonomic arousal or visceral sensations.
Predominantly heterosexual women showed greater processing in the explicit pathway. Women evaluated OC stimuli as more sexual and less distracting and women’s self-report mirrored the pattern of neural activity. When women viewed OC sexual stimuli, their brain showed greater activity in regions associated with volitional attention (e.g. dorsolateral and dorsomedial prefrontal cortex) and explicit appraisal (orbitofrontal areas, which evaluates and encodes reward value of punishers and integrates reward with emotional arousal), but not somatosensory awareness. Situating these findings in the context of the IPM suggests that women explicitly appraise OC stimuli as more sexual and more rewarding and better sustain volitional attention to OC, compared to OI, sexual stimuli, but are not any less aware of their sexual sensations toward OI sexual stimuli than they are for OC sexual stimuli. Hence, women may be just as aware of their somatosensory response to OI stimuli as they are to OC stimuli, suggesting that women’s erotic flexibility is not related to differences in or a lack of somatosensory awareness. Rather, differences between OC and OI sexual stimuli appear to be driven by attentional processing.
Additionally, OC stimuli elicited heightened activity in regions associated with sexual imagery and, unexpectedly, speech production and language processing. One possibility is that OC stimuli elicited self-referential mentalizing in the default mode network and Broca’s and Wernicke’s areas represent associated ‘self-talk’ (Raichle et al., 2001). Alternatively, the angular gyrus, premotor cortex, Broca’s area, somatosensory cortex and inferior temporal areas comprise the extended mirror neuron system (Caspers et al., 2010). The greater self-relevance of OC stimuli may facilitate the linkage between women’s observations of male masturbation and their own experience in response to this behavior. Future research should investigate how mentalizing, sexual imagery and self-referential processes contribute to OC sexual responses.
OI sexuality is not related to inhibition or judgment
In contrast to the hypothesis that women would be more likely to judge and negatively evaluate OI sexual stimuli, neural responses to OI, relative to OC, sexual stimuli showed no neural differences associated with judgment or negative evaluation. Rather, women responded to OI sexual stimuli with greater activity in higher order visual association areas, such as the fusiform gyri, involved in body and face perception, modulation of volitional attention and responses to genitalia and attractive faces, regardless of sexual orientation (see Table 1). As well, women showed greater activity in the superior parietal lobe (which acts in orienting attention, responding to distractors, and rearranging information to modify perspectives; Van Assche et al., 2014) and the posterior angular gyrus (involved in decoding symbolism and serves as a linking hub to transform visual input into associations; Caspers et al., 2012). Whereas predominantly heterosexual women visually process OC stimuli implicitly and automatically, OI visual processing is more elaborative, emphasizing face and bodily perception and modulating shifts in attention, meaning and perspective. Hence, OI stimuli might require more active symbolic interpretation that prompts predominantly heterosexual women to shift their perspective. This attentional and perspective shifting corroborates the very nature of OI stimuli—an inconsistency with women’s orientation.
The relative impact of mindful attention
Mindfully attending to OC stimuli enhanced women’s evaluations of OC stimuli as more sexually arousing and suppressed neural activity. Specifically, deactivation in superior cerebellum/lingual gyrus (involved in the visual processing of faces and complex visual processing) suggests that mindful attention operates by suppressing complex visual or facial processing. This is consistent with prior research demonstrating that mindfulness may operate by acting as an enhanced recovery phase that suppresses, rather than activates, neurobiological activity associated with general arousal (Dickenson et al., 2019).
Mindfully attending to OI sexual stimuli reduced women’s evaluations of OI stimuli as sexually arousing, but heightened activation in regions associated with complex visual processing and attention. The angular gyrus and superior parietal lobule work together to detect novel stimuli, distractions and to shift attention (Corbetta et al., 2008). These results extend findings concerning the role of distraction in inhibiting sexual responses (e.g. De Jong, 2009). Specifically, neural responses to OI stimuli are marked by attentional shifting, which is further enhanced by mindful attention, and ultimately weakens subjective sexual attention and evaluation. Importantly, these results indicate that the direction of one’s subjective sexual processing cannot be changed by volitionally altering attention or appraisal. Hence, the underlying mechanism that guides sexual orientation and deviations in sexual responses is distinct from explicit attentional and appraisal processes.
Within the specific direction of one’s sexual processing, mindful attention can impact the magnitude of evaluating sexual stimuli as arousing. That is, mindful attention facilitates sexual evaluations of genders that women typically find arousing (OC) and impedes sexual evaluations of genders that women find less arousing (OI). Women felt less distracted when viewing OI in a sexual, relative to a neutral, context and mindful attention improved women’s attentional focus toward OI neutral stimuli. However, mindful attention exacerbated women’s distraction toward OI sexual stimuli. This pattern of results suggests that women were not feeling distracted by OI stimuli until they were asked to attend their bodies in a sexual context. Such pattern of findings also suggests that women were similarly subjectively responsive to the sexual content in the absence of mindful attention to their bodily sensations. Perhaps results were due to the specific attentional processes altered, such that greater explicit monitoring (e.g. monitoring non-judgment and bodily sensations) may have overridden women’s implicit enjoyment of OI sexual stimuli. An important avenue for future research is to investigate the pathways by which specific forms of attention may impede or enhance compassion and sexual pleasure.
Specifically, mindful attention can shift attention either by heightening a detached, observational stance, attending to a stimulus as a third-party observer, or by heighten one’s ability to fully immerse oneself within an activity. Previous research has found that immersive attention increases subjective arousal, whereas more observational forms of attention reduce women’s subjective arousal (Both et al., 2011). Women are more likely to employ immersive attention to OC stimuli and employ detached, observation to OI stimuli (Bossio et al., 2013). Moreover, immersive participation has been associated with a lack of frontal lobe activation (Dietrich, 2003). Hence, mindful attention may have reduced effortful attention, through suppressing complex visual processing in OC stimuli. In contrast, mindful attention may increase detached observation to OI stimuli, which should then increase effortful attentional shifts, thereby decreasing arousal. Although we did not measure immersive or observatory attention, results suggest that sexual processing may be enhanced or attenuated based on the specific form of attention mindfulness augments. Investigating the pathways by which specific forms of attention account for the ways in which mindful attending to OC and OI stimuli impact sexual responses could explain the diversity of effects across mindfulness-based therapies for sexual desire and arousal concerns (Brotto et al., 2012). Our findings suggest that sexual orientation, rather than erotic flexibility, guides women’s sexual processing and attempting to change attentional processing only magnifies the effect of sexual orientation on women’s sexual processing.
Limitations and future directions
Inferring function from brain activation cannot serve as a proof of function. Nonetheless, identifying relevant brain regions helps to narrow the range of processes potentially involved. Additionally, our single-item measure of sexual response was limited to evaluating the stimulus as sexually arousing and does not reflect a specific aspect of sexual response. These limitations are also strengths, in that we were able to test our specific hypotheses because we engaged in careful inference of brain function and because our measure of sexual evaluation was not limited to a specific aspect of sexual response.
Although prior research indicates that one training session is sufficient to induce emotional regulation benefits (Arch and Craske, 2006), we know little about how many instances of mindful attention training are required to elicit changes in the processing of sexual stimuli. Although we were unable to determine how effectively participants were able to toggle between mindful attention and control tasks within the short epochs or assess for demand characteristics related to OC and OI stimuli, women’s self-reported level of distraction did, in fact, decrease as a result of the mindful attention task for OC and OI neutral stimuli. Future research should explore how these factors influence the degree to which participants are able to direct their attention to present-moment sensations to OC and OI desires, attractions, and arousal with compassion and non-judgment.
The current sample included predominantly heterosexual cisgender women who were willing to undergo brain scans while watching erotic films. Moreover, the sample mirrored the racial demographics of the state in which this study was conducted (mostly white). Among these women, we found that attempting to change attentional processing only magnified the effect of sexual orientation on women’s sexual processing. A critical direction for future research is to investigate subjective and neurobiological differences between OC and OI desires among women of various orientations, genders (including transgender and gender non-binary individuals) and ethnicities/races. A particularly intriguing direction is to examine differences between the same and other gender(s) desires of bisexual women (who rarely report that their desires for all genders are absolutely equivalent in frequency and intensity) and pansexual women (who report attraction toward a person, rather than a specific sex/gender).
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