Tales of Passion and Disgust

Robert Mapplethorpe - St. Sebastian

The previous post (Pleasure or Pain?) described the visual stimuli and behavioral results (subjective emotional ratings) from an experiment examining brain activity in response to pictures from four categories: neutral, disgust-inducing, erotic, and sadomasochistic (Stark et al., 2005). The participants were 24 adults, 12 of whom identified as having sadomasochistic sexual preferences (SM) and 12 without (non-SM).

Some of the results were of no surprise to anyone. The emotion ratings for neutral and disgust-inducing stimuli did not differ between the two groups. As expected, however, ratings for the other two stimulus classes were divergent:

The erotic pictures revealed more positive affect, more arousal, and more sexual arousal for the nonSM group in comparison to the SM group. SM subjects indicated to have felt more positive, more dominant, less disgusted, and more sexually aroused during the presentation of the pictures with sadomasochistic content than the nonSM subjects.

Why conduct this study in the first place, you ask? One reason given by the authors is to examine the neural correlates of two motivational systems, the approach and withdrawal systems (Cacioppo & Gardner, 1999). The withdrawal (or avoidance) system is triggered by threats in the environment, including those inducing fear and disgust, while the approach (or appetitive) system promotes feeding, sexual activity, and social behavior. Everyone in Stark et al.'s experiment wanted to avoid rotting hamburgers, but only the non-SM participants wanted to avoid sadomasochistic images. Thus, the same exact stimulus class induced different approach and avoidance responses in two groups of people with divergent sexual preferences.

I would add that a broader societal function of such a study might be to educate and to reduce stigma. A greater understanding of people different from ourselves makes for a more accepting and tolerant populace.

What about the possibility of viewing similar images in different contexts? A painting of St. Sebastian in a cathedral vs. Mapplethorpe's Sebastian in a retrospective at the Whitney? A flogging scene from The Passion of the Christ vs. a flogging scene in a dungeon? Interestingly, some of the most fervent supporters of the former are the most rabid critics of the latter (Frank Rich provides examples in The Good News About Mel Gibson).

Disgust and Morality

This brings us back to the possible evolutionary basis of disgust. Since this emotion is a response to things that are physically distasteful or morally repugnant, disgust has been examined in a specific evolutionary framework: "from oral to moral" (Rozin et al., 2009) -- from the rejection of bitter tastes to being grossed out by bugs to being repelled by certain social groups or sexual acts (Haidt & Hersh, 2001). Are there identical brain systems underlying these emotional responses? To answer this question, the most important comparison is the one between sadomasochistic and disgust-inducing images in the non-SM group.

Several T-contrasts were calculated for each subject: the emotional conditions versus the neutral condition (Disgust <> Neutral, Erotic <> Neutral, Sm <> Neutral), and for the positive emotion versus negative emotion (Erotic <> Disgust, Sm <> Disgust, Sm <> Erotic).

For each of the six contrasts above, there were two within-group comparisons and one between-group comparison for 20 regions of interest (ROIs), which were selected from a meta-analysis on neuroimaging studies of emotion (Phan et al., 2002). Exploratory analyses were performed as well. That's an awful lot of comparisons! [requiring stringent correction, of course]. The power to detect differences was reduced further by small group sizes (n=12 for each), rather diverse subject groups, and the use of stimuli that weren't terribly potent at eliciting some of the desired effects. Compare the relatively tame images used here (no explicit presentation of the genitals) to the 3 minute porn films of Zhang et al. (see Erotic or Disgusting?).

With all these caveats in mind, what were the results? For the Disgust vs. Neutral comparison, there were no significant differences between the groups, which matches their behavioral ratings. For Erotic vs. Neutral, there was greater activation for non-SM participants in the ventral striatum (known as a reward-related area), the hypothalamus, (controls many metabolic and endocrine functions) and the thalamus (a sensory and motor "relay station"). Ratings for the erotic pictures were similar in the two groups for dominance and disgust but higher in valence, arousal, and sexual arousal for the non-SM group. For Sm vs. Neutral, the SM group showed extensive activations in a number of frontal, temporal, and subcortical regions, including (most bizarrely) the insula, which has been associated with disgust. The only significant between-group difference, however, was in the ventral striatum. And the non-SM group didn't seem to activate any "disgust-related" regions, perhaps because many of them weren't actually disgusted by those images -- rated only 4.25 on a 9-point scale (1=very low and 9=very high). The variability was large, though, which prevented a statistically significant difference between Sm and disgust-inducing pictures (the latter rated 6.67 on disgust).

I think this level of variability in disgust reactions to the Sm images compromises the all-important Sm <> Disgust contrast in the non-SM group. But for what it's worth, right anterior cingulate showed greater activation to disgust pictures, whereas left posterior cingulate showed greater activation to sadomasochistic pictures. In the SM participants, the same contrast revealed greater activity in frontal, temporal/occipital, and subcortical structures (ventral striatum, thalamus, and brainstem). The between-group comparison again demonstrated the obvious: Sm pictures were more rewarding for the SM participants than for their non-SM counterparts.

I'm not sure how to interpret the cingulate findings, so I'll let the authors speak for themselves... Oh, wait, they didn't say anything about that, either. Ultimately, this study needed more potent stimuli (films instead of stills) and larger subject groups to avoid any sex-related differences in disgust sensitivity.

References

Cacioppo JT, Gardner WL. (1999). Emotion. Annu Rev Psychol. 50:191-214.

Haidt J, Hersh MA (2001). Sexual morality: The cultures and emotions of conservatives and liberals. J Applied Social Psychol. 31:191–221.

Phan KL, Wager T, Taylor SF, Liberzon I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16:331-48.

Rozin P, Haidt J, Fincher K. (2009). Psychology. From oral to moral. Science 323:1179-80.

STARK, R., SCHIENLE, A., GIROD, C., WALTER, B., KIRSCH, P., BLECKER, C., OTT, U., SCHAFER, A., SAMMER, G., & ZIMMERMANN, M. (2005). Erotic and disgust-inducing pictures—Differences in the hemodynamic responses of the brain. Biological Psychology, 70 (1), 19-29 DOI: 10.1016/j.biopsycho.2004.11.014

Zhang, M., Hu, S., Xu, L., Wang, Q., Xu, X., Wei, E., Yan, L., Hu, J., Wei, N., & Zhou, W. (2010). Neural circuits of disgust induced by sexual stimuli in homosexual and heterosexual men: An fMRI study. Eur J Radiol. Jun 22. [Epub ahead of print].

With its laborious build-up to its orgasmic spurtings of blood and other bodily fluids, Mr. Gibson's film is constructed like nothing so much as a porn movie, replete with slo-mo climaxes and pounding music for the money shots. Of all the "Passion" critics, no one has nailed its artistic vision more precisely than Christopher Hitchens, who on "Hardball" called it a homoerotic "exercise in lurid sadomasochism" for those who "like seeing handsome young men stripped and flayed alive over a long period of time."

-Frank Rich, Mel Gibson Forgives Us For His Sins [March 7, 2004]