Testosterone biases automatic memory processes in women towards potential mates

Female mate choice involves the comparative evaluation of potential mates. Females use a pooled comparison of sampled males to maximize the perceived reproductive fitness of their partner, implying the memorization of sampled males. However, hormonal and reproductive states influence female choosiness, and women's preference and memory for masculinity. Here, we investigated whether testosterone biases memory processes in women towards male faces using functional MRI. A single nasal testosterone dose was administered to healthy women in their early follicular phase, in a double-blind, placebo-controlled, crossover design. Testosterone increased the difference in reaction times to categorize male and female faces during encoding, without influencing subsequent recognition accuracy or response bias. The imaging results showed that testosterone shifted memory formation in the hippocampus and inferior temporal gyri from the encoding of female faces towards the encoding of male faces. In contrast, testosterone shifted memory formation in the left inferior frontal gyrus from the encoding of male faces towards the encoding of female faces. Furthermore, the hippocampal contribution to memory retrieval also shifted from female towards male faces. These results indicate that testosterone biases memory processes towards the relatively automatic encoding and retrieval of males in temporal brain regions and elaborate encoding of females in frontal brain regions, suggesting that testosterone may support female mate sampling and comparison by biasing automatic memory processes towards the encoding and retrieval of potential mates.

[1]  A. Little,et al.  Raised salivary testosterone in women is associated with increased attraction to masculine faces , 2007, Hormones and Behavior.

[2]  D. Perrett,et al.  Menstrual cycle alters face preference , 1999, Nature.

[3]  D. Perrett,et al.  Female preference for male faces changes cyclically: Further evidence , 2000 .

[4]  Dennis J. L. G. Schutter,et al.  Testosterone Reduces Unconscious Fear but Not Consciously Experienced Anxiety: Implications for the Disorders of Fear and Anxiety , 2005, Biological Psychiatry.

[5]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[6]  S. Corkin,et al.  Two routes to emotional memory: distinct neural processes for valence and arousal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Yasushi Miyashita,et al.  Cognitive Memory: Cellular and Network Machineries and Their Top-Down Control , 2004, Science.

[8]  Melissa Bateson,et al.  Comparative evaluation and its implications for mate choice. , 2005, Trends in ecology & evolution.

[9]  E. Ketterson,et al.  Elevated testosterone reduces choosiness in female dark–eyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection? , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  W J Bremner,et al.  Reproductive aging: accelerated ovarian follicular development associated with a monotropic follicle-stimulating hormone rise in normal older women. , 1996, The Journal of clinical endocrinology and metabolism.

[11]  Michael J. Ryan,et al.  Hormonal state influences aspects of female mate choice in the Túngara Frog (Physalaemus pustulosus) , 2006, Hormones and Behavior.

[12]  S. Yen,et al.  Serum Androstenedione and Testosterone Levels During the Menstrual Cycle , 1973 .

[13]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Theory , 2002, NeuroImage.

[14]  S. Pruett-Jones,et al.  SEXUAL SELECTION THROUGH FEMALE CHOICE IN LAWES' PAROTIA, A LEK‐MATING BIRD OF PARADISE , 1990, Evolution; international journal of organic evolution.

[15]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[16]  Guillén Fernández,et al.  How Progesterone Impairs Memory for Biologically Salient Stimuli in Healthy Young Women , 2007, The Journal of Neuroscience.

[17]  A. Aleman,et al.  A single administration of testosterone improves visuospatial ability in young women , 2004, Psychoneuroendocrinology.

[18]  W. Rosner,et al.  Twenty-four-hour mean plasma testosterone concentration declines with age in normal premenopausal women. , 1995, The Journal of clinical endocrinology and metabolism.

[19]  S. Yen,et al.  Serum androstenedione and testosterone levels during the menstrual cycle. , 1973, The Journal of clinical endocrinology and metabolism.

[20]  Eldridge S. Adams,et al.  Active mate choice at cock-of-the-rock leks: tactics of sampling and comparison , 1989, Behavioral Ecology and Sociobiology.

[21]  A. Karter,et al.  Parasites, Bright Males, and the Immunocompetence Handicap , 1992, The American Naturalist.

[22]  Jennifer Small,et al.  Sexual Selection and Condition-Dependent Mate Preferences , 2006, Current Biology.

[23]  B. Sherwin,et al.  Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women , 1988, Psychoneuroendocrinology.

[24]  Jack van Honk,et al.  Testosterone administration reduces empathetic behavior: A facial mimicry study , 2006, Psychoneuroendocrinology.

[25]  Astrid M. Schloerscheidt,et al.  Person Perception Across the Menstrual Cycle: Hormonal Influences on Social-Cognitive Functioning , 2002, Psychological science.

[26]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[27]  M. Petrie,et al.  VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES , 1997, Biological reviews of the Cambridge Philosophical Society.

[28]  G. Patricelli,et al.  Complex Mate Searching in the Satin Bowerbird Ptilonorhynchus violaceus , 2001, The American Naturalist.

[29]  G. Beall,et al.  The use of a sensitive equilibrium dialysis method for the measurement of free testosterone levels in healthy, cycling women and in human immunodeficiency virus-infected women. , 1998, The Journal of clinical endocrinology and metabolism.

[30]  B. Sherwin,et al.  Androgen enhances sexual motivation in females: a prospective, crossover study of sex steroid administration in the surgical menopause. , 1985, Psychosomatic medicine.

[31]  Erno J. Hermans,et al.  A Single Administration of Testosterone Reduces Fear-Potentiated Startle in Humans , 2006, Biological Psychiatry.

[32]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  L. V. Doornen,et al.  A single administration of testosterone induces cardiac accelerative responses to angry faces in healthy young women. , 2001, Behavioral neuroscience.

[34]  E. Zohary,et al.  Inter-trial neuronal activity in inferior temporal cortex: a putative vehicle to generate long-term visual associations , 1998, Nature Neuroscience.

[35]  S. Davis,et al.  Androgen levels in adult females: changes with age, menopause, and oophorectomy. , 2005, The Journal of clinical endocrinology and metabolism.

[36]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[37]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[39]  Randy Thornhill,et al.  Adaptations to Ovulation , 2005 .

[40]  Michael J. Ryan,et al.  Plasticity in female mate choice associated with changing reproductive states , 2005, Animal Behaviour.

[41]  D. Schutter,et al.  Testosterone shifts the balance between sensitivity for punishment and reward in healthy young women , 2004, Psychoneuroendocrinology.

[42]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[43]  K. Grammer,et al.  Male facial attractiveness: evidence for hormone-mediated adaptive design , 2001 .

[44]  Widemo,et al.  Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. , 1999, Trends in ecology & evolution.

[45]  A. Zahavi Mate selection-a selection for a handicap. , 1975, Journal of theoretical biology.

[46]  L. Real Search Theory and Mate Choice. I. Models of Single-Sex Discrimination , 1990, The American Naturalist.

[47]  A. Bond,et al.  The use of analogue scales in rating subjective feelings , 1974 .

[48]  C. Bernaards,et al.  Time course of effects of testosterone administration on sexual arousal in women. , 2000, Archives of general psychiatry.

[49]  Barney Luttbeg,et al.  A Comparative Bayes tactic for mate assessment and choice , 1996 .

[50]  Orman,et al.  Transdermal testosterone treatment in women with impaired sexual function after oophorectomy. , 2000, The New England journal of medicine.

[51]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[52]  P. Ekman Pictures of Facial Affect , 1976 .

[53]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[54]  Martin Lepage,et al.  A face to remember: emotional expression modulates prefrontal activity during memory formation , 2005, NeuroImage.

[55]  A. Janetos Strategies of female mate choice: A theoretical analysis , 1980, Behavioral Ecology and Sociobiology.

[56]  M. Petrie,et al.  Peahens prefer peacocks with elaborate trains , 1991, Animal Behaviour.

[57]  Leslie A. Zebrowitz,et al.  Does sexual dimorphism in human faces signal health? , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  Albert Postma,et al.  Effects of testosterone administration on selective aspects of object-location memory in healthy young women , 2000, Psychoneuroendocrinology.

[59]  B. Sherwin,et al.  Sex steroids and affect in the surgical menopause: a double-blind, cross-over study , 1985, Psychoneuroendocrinology.

[60]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[61]  R. Morris,et al.  Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas , 2006, The European journal of neuroscience.