The time course of pupil dilation evoked by visual sexual stimuli: Exploring the underlying ANS mechanisms
Corresponding Author
Johannes B. Finke
Department of Clinical Psychophysiology, Institute of Psychobiology, University of Trier, Trier, Germany
Correspondence Johannes B. Finke, University of Trier, Institute of Psychobiology, Johanniterufer 15, 54290 Trier, Germany. Email: [email protected]Search for more papers by this authorChristian E. Deuter
Department of Psychiatry and Psychotherapy, Charité University Medical Center, Berlin, Germany
Search for more papers by this authorXenia Hengesch
Department of Clinical Psychophysiology, Institute of Psychobiology, University of Trier, Trier, Germany
Search for more papers by this authorHartmut Schächinger
Department of Clinical Psychophysiology, Institute of Psychobiology, University of Trier, Trier, Germany
Search for more papers by this authorCorresponding Author
Johannes B. Finke
Department of Clinical Psychophysiology, Institute of Psychobiology, University of Trier, Trier, Germany
Correspondence Johannes B. Finke, University of Trier, Institute of Psychobiology, Johanniterufer 15, 54290 Trier, Germany. Email: [email protected]Search for more papers by this authorChristian E. Deuter
Department of Psychiatry and Psychotherapy, Charité University Medical Center, Berlin, Germany
Search for more papers by this authorXenia Hengesch
Department of Clinical Psychophysiology, Institute of Psychobiology, University of Trier, Trier, Germany
Search for more papers by this authorHartmut Schächinger
Department of Clinical Psychophysiology, Institute of Psychobiology, University of Trier, Trier, Germany
Search for more papers by this authorAbstract
The early processing of visual sexual stimuli shows signs of automaticity. Moreover, there is evidence for sex-specific patterns in cognitive and physiological responding to erotica. However, little is known about the time course of rapid pupillary responses to sexual stimuli and their correspondence with other measures of autonomic activity in women and men. To study pupil dilation as an implicit measure of sexual arousal at various stages of picture processing, we presented 35 heterosexual participants with pictures showing either erotic couples or single (male/female) erotic nudes, contrasted with people involved in everyday situations. Brightness-adjusted grayscale pictures were shown for a duration of 2,500 ms within the central visual field, alternating with perceptually matched patches. Left pupil diameter was recorded at 500 Hz using a video-based eye tracker. Skin conductance and heart rate were coregistered and correlated with latent components of pupil dilation (dissociated by temporal PCA). Whereas stimulus-evoked changes in pupil size indicated virtually no initial constriction, a rapid effect of appetence emerged (dilation to erotica within 500 ms). Responses at early stages of processing were remarkably consistent across both sexes. In contrast, later phases of pupil dilation, subjective ratings, and skin conductance responses showed a sex-specific pattern. Moreover, evidence for an association of early-onset pupil dilation and heart rate acceleration was found, suggestive of parasympathetic inhibition, whereas the late component was mainly related to sympathetically mediated skin conductance. Taken together, our results indicate that different temporal components of pupil responses to erotic stimuli may reflect divergent underlying neural mechanisms.
REFERENCES
- Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403–450. doi:10.1146/annurev.neuro.28.061604.135709
- Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48. doi:10.18637/jss.v067.i01
- Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91(2), 276–292. doi:10.1037/0033-2909.91.2.276
- Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1991). Autonomic determinism: The modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychological Review, 98(4), 459–487. doi:10.1037/0033-295X.98.4.459
- Bitsios, P., Szabadi, E., & Bradshaw, C. M. (2004). The fear-inhibited light reflex: Importance of the anticipation of an aversive event. International Journal of Psychophysiology, 52(1), 87–95. doi:10.1016/j.ijpsycho.2003.12.006
- Bradley, M. M., & Lang, P. J. (2015). Memory, emotion, and pupil diameter: Repetition of natural scenes. Psychophysiology, 52(9), 1186–1193. doi:10.1111/psyp.12442
- Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45(4), 602–607. doi:10.1111/j.1469-8986.2008.00654.x
- Brody, S. (2007). Intercourse orgasm consistency, concordance of women's genital and subjective sexual arousal, and erotic stimulus presentation sequence. Journal of Sex & Marital Therapy, 33(1), 31–39. doi:10.1080/00926230600998458
- Brody, S., Laan, E., & van Lunsen, R. H. W. (2003). Concordance between women's physiological and subjective sexual arousal is associated with consistency of orgasm during intercourse but not other sexual behavior. Journal of Sex & Marital Therapy, 29(1), 15–23. doi:10.1080/713847101
- Brody, S., Veit, R., & Rau, H. (2000). A preliminary report relating frequency of vaginal intercourse to heart rate variability, Valsalva ratio, blood pressure, and cohabitation status. Biological Psychology, 52(3), 251–257. doi:10.1016/S0301-0511(99)00048-4
- Chivers, M. L., & Bailey, J. M. (2005). A sex difference in features that elicit genital response. Biological Psychology, 70(2), 115–120. doi:10.1016/j.biopsycho.2004.12.002
- Chivers, M. L., Rieger, G., Latty, E., & Bailey, J. M. (2004). A sex difference in the specificity of sexual arousal. Psychological Science, 15(11), 736–744. doi:10.1111/j.0956-7976.2004.00750.x
- Chivers, M. L., Seto, M. C., Lalumiere, M. L., Laan, E., & Grimbos, T. (2010). Agreement of self-reported and genital measures of sexual arousal in men and women: A meta-analysis. Archives of Sexual Behavior, 39(1), 5–56. doi:10.1007/s10508-009-9556-9
- Costa, R. M., & Brody, S. (2012). Greater resting heart rate variability is associated with orgasms through penile–vaginal intercourse, but not with orgasms from other sources. Journal of Sexual Medicine, 9(1), 188–197. doi:10.1111/j.1743-6109.2011.02541.x
- Czeluscinska-Peczkowska, A., Vögele, C., & Blechert, J. (2016). Perception and evaluation of sexually explicit visual stimuli. Journal of Sexual Medicine, 13(5), S170–S171. doi:10.1016/j.jsxm.2016.03.351
- Dawson, M. E., Schell, A. M., & Filion, D. L. (2007). The electrodermal system. Handbook of Psychophysiology, 2, 200–223.
- Ferrari, V., Cesarei, A. de, Mastria, S., Lugli, L., Baroni, G., Nicoletti, R., & Codispoti, M. (2016). Novelty and emotion: Pupillary and cortical responses during viewing of natural scenes. Biological Psychology, 113, 75–82. doi:10.1016/j.biopsycho.2015.11.008
- Gillath, O., & Collins, T. (2016). Unconscious desire: The affective and motivational aspects of subliminal sexual priming. Archives of Sexual Behavior, 45(1), 5–20. doi:10.1007/s10508-015-0609-y
- Graham, F. K. (1978). Constraints on measuring heart rate and period sequentially through real and cardiac time. Psychophysiology, 15(5), 492–495. doi:10.1111/j.1469-8986.1978.tb01422.x
- Hagan, J. J., Leslie, R. A., Patel, S., Evans, M. L., Wattam, T. A., Holmes, S., … Upton, N. (1999). Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proceedings of the National Academy of Sciences, 96(19), 10911–10916. doi:10.1073/pnas.96.19.10911
- Hedges, L. V., & Vevea, J. L. (1998). Fixed- and random-effects models in meta-analysis. Psychological Methods, 3(4), 486–504. doi:10.1037/1082-989X.3.4.486
- Henderson, R. R., Bradley, M. M., & Lang, P. J. (2014). Modulation of the initial light reflex during affective picture viewing. Psychophysiology, 51(9), 815–818. doi:10.1111/psyp.12236
- Hess, E. H., Seltzer, A. L., & Shlien, J. M. (1965). Pupil response of hetero- and homosexual males to pictures of men and women: A pilot study. Journal of Abnormal Psychology, 70(3), 165–168. doi:10.1037/h0021978
- Hewig, J., Trippe, R. H., Hecht, H., Straube, T., & Miltner, W. H. R. (2008). Gender differences for specific body regions when looking at men and women. Journal of Nonverbal Behavior, 32(2), 67–78. doi:10.1007/s10919-007-0043-5
- Hinojosa-Laborde, C., Chapa, I., Lange, D., & Haywood, J. R. (1999). Gender differences in sympathetic nervous system regulation. Clinical and Experimental Pharmacology and Physiology, 26(2), 122–126. doi:10.1046/j.1440-1681.1999.02995.x
- Janssen, E., Everaerd, W., Spiering, M., & Janssen, J. (2000). Automatic processes and the appraisal of sexual stimuli: Toward an information processing model of sexual arousal. Journal of Sex Research, 37(1), 8–23. doi:10.1080/00224490009552016
- Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89(1), 221–234. doi:10.1016/j.neuron.2015.11.028
- Kagerer, S., Wehrum, S., Klucken, T., Walter, B., Vaitl, D., & Stark, R. (2014). Sex attracts: Investigating individual differences in attentional bias to sexual stimuli. PLOS ONE, 9(9), e107795.
- Korn, C. W., & Bach, D. R. (2016). A solid frame for the window on cognition: Modeling event-related pupil responses. Journal of Vision, 16(3), 28. doi:10.1167/16.3.28
- Kuo, T. B. J., Lin, T., Yang, C. C. H., Li, C.-L., Chen, C.-F., & Chou, P. (1999). Effect of aging on gender differences in neural control of heart rate. American Journal of Physiology–Heart and Circulatory Physiology, 277(6), H2233–H2239.
- Laeng, B., Sirois, S., & Gredebäck, G. (2012). Pupillometry a window to the preconscious? Perspectives on Psychological Science, 7(1), 18–27. doi:10.1177/1745691611427305
- Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International Affective Picture System (IAPS): Affective ratings of pictures and instruction manual. Technical report A-8. Gainesville, FL: University of Florida.
- Liu, C. C., Kuo, T. B. J., & Yang, C. C. H. (2003). Effects of estrogen on gender-related autonomic differences in humans. American Journal of Physiology–Heart and Circulatory Physiology, 285(5), H2188–H2193. doi:10.1152/ajpheart.00256.2003
- Loewenfeld, I. E. (1993). The pupil: Anatomy, physiology, and clinical applications . Ames, IA: Iowa State University Press.
- Lykins, A. D., Meana, M., & Strauss, G. P. (2008). Sex differences in visual attention to erotic and non-erotic stimuli. Archives of Sexual Behavior, 37(2), 219–228. doi:10.1007/s10508-007-9208-x
- Macefield, V. G., & Wallin, B. G. (1996). The discharge behaviour of single sympathetic neurones supplying human sweat glands. Journal of the Autonomic Nervous System, 61(3), 277–286. doi:10.1016/S0165-1838(96)00095-1
- Meston, C. M. (2000). Sympathetic nervous system activity and female sexual arousal. American Journal of Cardiology, 86(2), 30–34. doi:10.1016/S0002-9149(00)00889-4
- Nieuwenhuis, S., de Geus, E. J., & Aston-Jones, G. (2011). The anatomical and functional relationship between the P3 and autonomic components of the orienting response. Psychophysiology, 48(2), 162–175. doi:10.1111/j.1469-8986.2010.01057.x
- Nummenmaa, L., Hietanen, J. K., Santtila, P., & Hyönä, J. (2012). Gender and visibility of sexual cues influence eye movements while viewing faces and bodies. Archives of Sexual Behavior, 41(6), 1439–1451. doi:10.1007/s10508-012-9911-0
- Peterson, Z. D., & Janssen, E. (2007). Ambivalent affect and sexual response: The impact of co-occurring positive and negative emotions on subjective and physiological sexual responses to erotic stimuli. Archives of Sexual Behavior, 36(6), 793–807. doi:10.1007/s10508-006-9145-0
- Rieger, G., Cash, B. M., Merrill, S. M., Jones-Rounds, J., Dharmavaram, S. M., & Savin-Williams, R. C. (2015). Sexual arousal: The correspondence of eyes and genitals. Biological Psychology, 104, 56–64. doi:10.1016/j.biopsycho.2014.11.009
- Rupp, H. A., & Wallen, K. (2008). Sex differences in response to visual sexual stimuli: A review. Archives of Sexual Behavior, 37(2), 206–218.
- Sanchis-Gimeno, J. A., Sanchez-Zuriaga, D., & Martinez-Soriano, F. (2012). White-to-white corneal diameter, pupil diameter, central corneal thickness and thinnest corneal thickness values of emmetropic subjects. Surgical and Radiologic Anatomy, 34(2), 167–170. doi:10.1007/s00276-011-0889-4
- Sarlo, M., & Buodo, G. (2017). To each its own? Gender differences in affective, autonomic, and behavioral responses to same-sex and opposite-sex visual sexual stimuli. Physiology & Behavior, 171, 249–255. doi:10.1016/j.physbeh.2017.01.017
- Silver, N. C., & Dunlap, W. P. (1987). Averaging correlation coefficients: Should Fisher's z transformation be used? Journal of Applied Psychology, 72(1), 146–148. doi:10.1037/0021-9010.72.1.146
- Spiering, M., Everaerd, W., & Laan, E. (2004). Conscious processing of sexual information: Mechanisms of appraisal. Archives of Sexual Behavior, 33(4), 369–380. doi:10.1023/B:ASEB.0000028890.08687.94
- Steiner, G. Z., & Barry, R. J. (2011). Pupillary responses and event-related potentials as indices of the orienting reflex. Psychophysiology, 48(12), 1648–1655. doi:10.1111/j.1469-8986.2011.01271.x
- Steinhauer, S. R., & Hakerem, G. (1992). The pupillary response in cognitive psychophysiology and schizophrenia. Annals of the New York Academy of Sciences, 658(1), 182–204. doi:10.1111/j.1749-6632.1992.tb22845.x
- Steinhauer, S. R., Siegle, G. J., Condray, R., & Pless, M. (2004). Sympathetic and parasympathetic innervation of pupillary dilation during sustained processing. International Journal of Psychophysiology, 52(1), 77–86. doi:10.1016/j.ijpsycho.2003.12.005
- van Bockstaele, E. J., Colago, E. E., & Valentino, R. J. (1998). Amygdaloid corticotropin-releasing factor targets locus coeruleus dendrites: Substrate for the co-ordination of emotional and cognitive limbs of the stress response. Journal of Neuroendocrinology, 10(10), 743–758. doi:10.1046/j.1365-2826.1998.00254.x
- Wessa, M., Kanske, P., Neumeister, P., Bode, K., Heissler, J., & Schönfelder, S. (2010). EmoPicS: Subjective and psychophysiological evaluation of new imagery for clinical biopsychological research [Supplement]. Z. Klin. Psychol. Psychother, 1, 11–77.
- Wetzel, N., Buttelmann, D., Schieler, A., & Widmann, A. (2015). Infant and adult pupil dilation in response to unexpected sounds. Developmental Psychobiology, 58(3), 382–392. doi:10.1002/dev.21377
- Willenbockel, V., Sadr, J., Fiset, D., Horne, G. O., Gosselin, F., & Tanaka, J. W. (2010). Controlling low-level image properties: The SHINE toolbox. Behavior Research Methods, 42(3), 671–684. doi:10.3758/BRM.42.3.671
- Zuckerman, M. (1971). Physiological measures of sexual arousal in the human. Psychological Bulletin, 75(5), 297–329. doi:10.1037/h0030923