Skip to main content

Advertisement

Log in

Females and attention to eye gaze: effects of the menstrual cycle

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

It is well known that an observer will attend to the location cued by another’s eye gaze and that in some circumstances, this effect is enhanced when the emotion expressed is threat-related. This study explored whether attention to the gaze of threat-related faces is potentiated in the luteal phase of the menstrual cycle when detection of threat is suggested to be enhanced, compared to the follicular phase. Female participants were tested on a gaze cueing task in their luteal (N = 13) or follicular phase (N = 15). Participants were presented with various emotional expressions with an averted eye gaze that was either spatially congruent or incongruent with a forthcoming target. Females in the luteal phase responded faster overall to targets on trials with a 200-ms stimulus onset asynchrony interval. The results suggest that during the luteal phase, females show a general and automatic hypersensitivity to respond to stimuli associated with socially and emotionally relevant cues. This may be a part of an adaptive biological mechanism to protect foetal development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. A within design, whereby females completed the task twice, in their luteal and in their follicular phase, was initially considered; however, it soon became clear from detailed pilot work that there would be large and confounding session-to-session practise effects. Practise effects in various cognitive abilities have also been observed when measured across the menstrual cycle (Hampson 1990). A between-subjects design was the simplest way to avoid this confound. Previous studies, such as that by Derntl et al. (2008), have also employed the between design to identify differences in performance between the luteal and follicular phase.

References

  • Alliende ME (2002) Mean versus individual hormonal profiles in the menstrual cycle. Fertil Steril 78:90–95

    Google Scholar 

  • Bayliss AP, di Pellegrino G, Tipper SP (2005) Sex differences in the symbolic cueing of attention. Q J Exp Psychol A 58:631–650

    PubMed  Google Scholar 

  • Calvo MG, Avero P, Lundqvist D (2006) Facilitated detection of angry faces: initial orienting and processing efficiency. Cogn Emot 20:785–811

    Article  Google Scholar 

  • Collignon O, Girard S, Gosselin F, Saint-Amour D, Lepore F, Lassonde M (2009) Women process multisensory emotion expressions more efficiently than men. Neuropsychologia 48:220–225

    Article  Google Scholar 

  • Conway CA, Jones BC, DeBruine LM, Welling LLM, Law Smith MJ, Perrett DI et al (2007) Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised. Horm Behav 51:202–206

    Article  PubMed  CAS  Google Scholar 

  • Deaner RO, Shepherd SV, Platt ML (2007) Familiarity accentuates gaze cueing in women but not men. Biol Lett 3:64–67

    Article  PubMed  Google Scholar 

  • DeBruine LM, Jones BC, Perrett DI (2005) Women’s attractiveness judgments of self-resembling faces changes across the menstrual cycle. Horm Behav 47:379–383

    Article  PubMed  Google Scholar 

  • Derntl B, Kryspin-Exner I, Fernbach E, Moser E, Habel U (2008) Emotion recognition accuracy in healthy young females is associated with cycle phase. Horm Behav 53:90–95

    Article  PubMed  Google Scholar 

  • Derntl B, Schöpf V, Kollndorfer K, Lanzenberger R (2012) Menstrual cycle phase and duration of oral contraception intake affect olfactory perception. Chem Senses 38:67–75

    Article  PubMed  Google Scholar 

  • Derntl B, Hack RL, Kryspin-Exner I, Habel U (2013) Association of menstrual cycle phase with the core components of empathy. Horm Behav 63:97–104

    Article  PubMed  CAS  Google Scholar 

  • Driver J, Davis G, Ricciardelli P, Kidd P, Maxwell E, Baron-Cohen S (1999) Gaze perception triggers reflexive visuospatial orienting. Vis Cogn 6:509–540

    Article  Google Scholar 

  • Durante KM, Li NP, Haselton MG (2008) Changes in women’s choice of dress across the menstrual cycle: naturalistic and laboratory task-based evidence. Pers Soc Psychol B 34:1451–1460

    Article  Google Scholar 

  • Egeth HE, Yantis S (1997) Visual attention: control, representation, and time course. Annu Rev Psychol 48:269–297

    Article  PubMed  CAS  Google Scholar 

  • Ekman P, Friesen WV (1976) Pictures of facial affect. Consulting Psychologists Press, Palo Alto

    Google Scholar 

  • Fessler DMT (2001) Luteal phase immunosuppression and meat eating. Biol Forum 94:407–430

    Google Scholar 

  • Fessler DMT, Navarrete CD (2003) Domain-specific variation in disgust sensitivity across the menstrual cycle. Evol Hum Behav 24:406–417

    Article  Google Scholar 

  • Fox E, Lester V, Russo R, Bowles RJ, Pichler A, Dutton K (2000) Facial expressions of emotion: are angry faces detected more efficiently? Cogn Emot 14:61–92

    Article  PubMed  Google Scholar 

  • Fox E, Russo R, Dutton K (2002) Attentional bias for threat: evidence for delayed disengagement from emotional faces. Cogn Emot 16:355–379

    Article  PubMed  Google Scholar 

  • Fox E, Mathews A, Calder AJ, Yiend J (2007) Anxiety and sensitivity to gaze direction in emotionally expressive faces. Emotion 7:478–486

    Article  PubMed  Google Scholar 

  • Friesen CK, Kingstone A (1998) The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychonomic B Rev 5:490–495

    Article  Google Scholar 

  • Friesen CK, Bayliss AP, Tipper SP (2007) Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychol Bull 133:694–724

    Article  Google Scholar 

  • Gangestad SW, Thornhill R (1998) Menstrual cycle variation in women’s preferences for the scent of symmetrical men. P Roy Soc B Biol Sci 265:927–933

    Article  CAS  Google Scholar 

  • Gilbert SF (2000) Developmental biology. Sinauer, USA

    Google Scholar 

  • Graham R, Friesen CK, Fichtenholtz HM, LaBar KS (2010) Modulation of reflexive orienting to gaze direction by facial expressions. Visual Cogn 18:331–368

    Article  Google Scholar 

  • Hall CW, Gaul L, Kent M (1999) College students’ perception of facial expressions. Percept Motor Skill 89:763–770

    Article  CAS  Google Scholar 

  • Hampson E (1990) Variations in sex-related cognitive abilites across the menstrual cycle. Brain Cogn 14:26–43

    Google Scholar 

  • Hampson E, van Anders S, Mullin L (2006) A female advantage in the recognition of emotional facial expressions: test of an evolutionary hypothesis. Evol Hum Behav 27:401–416

    Article  Google Scholar 

  • Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223–233

    Article  PubMed  Google Scholar 

  • Hietanen JK, Leppänen JM (2003) Does facial expression affect attention orienting by gaze direction cues? J Exp Psychol Human 29:1228–1243

    Article  Google Scholar 

  • Holmes A, Richards A, Green S (2006) Anxiety and sensitivity to eye gaze in emotional faces. Brain Cogn 60:282–294

    Article  PubMed  Google Scholar 

  • Hood BM, Willen JD, Driver J (1998) Adult’s eyes trigger shifts of visual attention in human infants. Psychol Sci 9:131–134

    Article  Google Scholar 

  • Johnston VS, Hagel R, Franklin M, Fink B, Gammer K (2001) Male facial attractiveness: evidence for a hormone-mediated adaptive design. Evol Hum Behav 22:251–267

    Article  Google Scholar 

  • Jones BC, Little AC, Boothroyd L, DeBruine LM, Feinberg DR, Law Smith MJ et al (2005a) Commitment to relationships and preferences for femininity and apparent health in faces are strongest on days of the menstrual cycle when progesterone level is high. Horm Behav 48:283–290

    Article  PubMed  CAS  Google Scholar 

  • Jones BC, Perrett DI, Little AC, Boothroyd L, Cornwell RE, Feinberg DR et al (2005b) Menstrual cycle, pregnancy and oral contraceptive use alter attraction to apparent health in faces. P Roy Soc B Biol Sci 272:347–354

    Article  CAS  Google Scholar 

  • Jones BC, DeBruine LM, Perrett DI, Little AC, Feinberg DR, Law Smith MJ (2008) Effects of menstrual cycle phase on face preferences. Arch Sex Behav 37:78–84

    Article  PubMed  Google Scholar 

  • Manber R, Bootzin RR (1997) Sleep and the menstrual cycle. Health Psychol 16:209–214

    Article  PubMed  CAS  Google Scholar 

  • Masataka N, Shibasaki M (2012) Premenstrual enhancement of snake detection in visual search in healthy women. Sci Rep 2:1–4

    Google Scholar 

  • Mathews A, Fox E, Yiend J, Calder A (2003) The face of fear: effects of eye gaze and emotion on visual attention. Vis Cogn 10:823–835

    Article  PubMed  Google Scholar 

  • Mogg K, Bradley BP (1999) Orienting of attention to threatening facial expressions presented under conditions of restricted awareness. Cogn Emot 13:713–740

    Article  Google Scholar 

  • Müller HJ, Rabbitt PMA (1989) Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J Exp Psychol Human 15:315–330

    Article  Google Scholar 

  • Penton-Voak IS, Perrett DI, Castles DL, Kobayashi T, Burt DM, Murray L, Minamisawa R (1999) Menstrual cycle alters face preference. Nature 399:741–742

    Article  PubMed  CAS  Google Scholar 

  • Puce A, Allison T, Bentin S, Gore JC, McCarthy G (1998) Temporal cortex activation in humans viewing eye and mouth movements. J Neurosci 18:2188–2199

    PubMed  CAS  Google Scholar 

  • Reiman EM, Armstrong SM, Matt KS, Mattox JH (1996) The application of positron emission tomography to the study of the normal menstrual cycle. Hum Reprod 11:2799–2805

    Article  PubMed  CAS  Google Scholar 

  • Spielberger CD, Diaz-Guerrero R (1983) Cross-cultural anxiety: an overview. Ser Clin C Stress Anxiety 2:3–11

    Google Scholar 

  • Sprengelmeyer R, Rausch M, Eysel UT, Przuntek H (1998) Neural structures associated with the recognition of facial expressions of basic emotions. P Roy Soc B Biol Sci 265:1927–1931

    Article  CAS  Google Scholar 

  • Tipples J (2006) Fear and fearfulness potentiate automatic orienting to eye gaze. Cogn Emot 20:309–320

    Article  Google Scholar 

  • van Wingen GA, van Broekhoven F, Verkes RJ, Petersson KM, Bäckström T, Buitelaar JK et al (2008) Progesterone selectively increases amygdala activity in women. Mol Psychiatr 13:325–333

    Article  Google Scholar 

  • Wolohan FDA, Crawford TJ (2012) The anti-orienting phenomenon re-visited: effects of gaze cues on antisaccade performance. Exp Brain Res 221:385–392

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to sincerely thank D. Litchfield for support and assistance in manuscript preparation and T. Donovan for comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Felicity D. A. Wolohan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wolohan, F.D.A., Bennett, S.J.V. & Crawford, T.J. Females and attention to eye gaze: effects of the menstrual cycle. Exp Brain Res 227, 379–386 (2013). https://doi.org/10.1007/s00221-013-3515-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3515-3

Keywords

Navigation