Abstract Secondary sexual characteristics convey information about reproductive potential. In the same way that facial symmetry and masculinity, and shoulder-to-hip ratio convey information about reproductive/genetic quality in males, waist-to-hip-ratio (WHR) is a phenotypic cue to fertility, fecundity, neurodevelopmental resources in offspring, and overall health, and is indicative of “good genes” in women. Here, using fMRI, we found that males show activation in brain reward centers in response to naked female bodies when surgically altered to express an optimal (∼0.7) WHR with redistributed body fat, but relatively unaffected body mass index (BMI). Relative to presurgical bodies, brain activation to postsurgical bodies was observed in bilateral orbital frontal cortex. While changes in BMI only revealed activation in visual brain substrates, changes in WHR revealed activation in the anterior cingulate cortex, an area associated with reward processing and decision-making. When regressing ratings of attractiveness on brain activation, we observed activation in forebrain substrates, notably the nucleus accumbens, a forebrain nucleus highly involved in reward processes. These findings suggest that an hourglass figure (i.e., an optimal WHR) activates brain centers that drive appetitive sociality/attention toward females that represent the highest-quality reproductive partners. This is the first description of a neural correlate implicating WHR as a putative honest biological signal of female reproductive viability and its effects on men's neurological processing.

Citation: Platek SM, Singh D (2010) Optimal Waist-to-Hip Ratios in Women Activate Neural Reward Centers in Men. PLoS ONE 5(2): e9042. https://doi.org/10.1371/journal.pone.0009042 Editor: Henry Harpending, University of Utah, United States of America Received: December 9, 2009; Accepted: January 18, 2010; Published: February 5, 2010 Copyright: © 2010 Platek, Singh. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by a faculty induction award from the University of Liverpool and a grant from the Pioneer Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction Variations in men's facial (e.g., symmetry, masculinity) and body (e.g., shoulder-to-hip ratio) morphology are related to women's ratings of attractiveness. Specifically, women tend to rate more symmetrical and masculine faces, and higher SHR[1] as attractive during fertile phases of their menstrual cycle and for short-term mating partners[2], [3], [4], [5], [6], [7], [8]. Several recent findings[9], [10], [11], [12] demonstrate that faces that are rated as attractive activate neural reward substrates in females, and that this neural activation is partly modulated by hormonal status of women[11]. These findings support the hypothesis that men's facial and body morphology serves as an honest biosignal to genetic fitness. Women have a larger proportion of fat stores in comparison to non-human female primates and men[13]. Prior to puberty, a sexual dimorphism in fat distribution is not apparent, however, in post-menarche women estrogen inhibits storage of fat around abdominal areas and fat is stored in the gluteofemoral (thighs and buttock) region[14]. Women have a lower waist-to-hip ratio (WHR) than men and men's preference for lower WHR, or hour-glass figures, appears to be cross-cultural[15], [16]c.f.[17], [18] and adaptive because WHR is positively correlated with fecundity, levels of the reproductive hormones estradiol and progesterone[19], higher likelihood of conception[20], and availability of neurodevelopmental resources for offspring[21], but negatively correlated with lower likelihood of illnesses such as heart disease and various cancers[15], and lower incidence of depression[22]. Differences in WHR can also be used to index pregnancy and the capacity for unencumbered childbirth[1]. Consequently, it's been hypothesized that distribution of body fat represents a secondary sexual characteristic that, in the same way variation in men's facial and body morphology does, can influence ratings of attraction and fecundity (see also[23] for arguments regarding female BMI).

Methods Participants Here 14 men (M age = 25.21, S.D. = 6.30) were scanned using fMRI while making attractiveness ratings to randomly and individually presented pictures (one from the rear and one from an oblique rear position for each woman) of seven naked female bodies prior to and after recovery from an elective cosmetic surgical procedure to reconfigure and optimize WHR[14]. All participants provided written informed consent and the study was approved by the University of Liverpool School of Biological Sciences committee on research ethics. Stimuli Stimuli were a sample of seven images taken from those used in another study [14]. Images were presented in both the rear and oblique rear position (see [14]). Images were presented 15 times for 1 second with a variable interstimulus (2–15 s) interval to maximize jittering using Neurobehavioral Systems Presentation. Each participant saw each of the 14 different images in random order. Participants were asked to respond to the attractiveness of the images by using a 5 button fMRI-comaptible response pad (MR technologies). Order of button anchor (most attractive/least attractive) was randomized across subjects. fMRI Procedures Data were collected using a Siemens Trio 3T scanner using gradient-echo T2*-weighted echo-planar images (EPI) to measure blood-oxygen-level-dependent (BOLD) contrasts. For each participant approximately 225 volumes were collected with an interleaved acquisition, a slice thickness of 2 mm, at a TR of 2.75 s, TE of 30 ms, and a resolution of 3.5×3.5 mm for each participant. Slices were tilted to 30 degrees from horizontal to maximize image quality in areas near susceptibility field gradients[24]. All participants also underwent high-resolution structural scanning with a standard MP-RAGE sequence (176 1 mm voxel saggital slices, TR = 2040 ms, TE = 5.57 ms, FoV = 256, flip angle = 8°). While being scanned participants were asked to make explicit ratings of attractiveness to naked female body images [14] presented for 1 second (ISI randomization optimized for jitter 2–15 seconds). Ratings were made on a 5-point scale from very unattractive to very attractive (counterbalanced for which finger anchored each end of the attractiveness scale). fMRI data were analyzed using general linear modeling and mixed effects analysis implemented in FEAT-FSL[25]. We hypothesized that if WHR represents a cue to genetic quality then, similar to symmetry and masculinity in male faces, bodies that represent optimal WHR would activate neural reward substrates.

Discussion Our observed activation patterns in the brain suggest that female body configuration represents a salient stimulus to men and that optimal female body configurations activate areas of men's brains that are associated with reward processing and appetitive behaviors. This activation may represent the proximate neural mechanism of attraction to females that express curvaceous body types and also further account for cross-cultural findings showing that optimal WHR (∼.7) as being consistently rated as attractive. Lastly, this finding may extend our understanding of some men's proclivity to develop a preoccupation with stimuli depicting optimally designed women (e.g., pornography)[44], [45]. Interestingly, our findings did not demonstrate that BMI had a large effect on brain activation except in areas associated with simple visual evaluations of shape and size. This does not downplay the importance of BMI in evaluations of female attractiveness, but may suggest that BMI's role in these evaluations is less the product of evolved psychological mechanisms and more the part of culturally driven, or societal based norms and perceptions.

Acknowledgments The authors would like to thank Magdalena Babiszewska for her assistance with data collection. The authors would also like to thank Rebecca Burch, J. Mark Davis, Jennifer Davis, Andrew Gallup, Gordon Gallup, Aaron Goetz, Austen Krill, Katherine Reding, Todd Shackelford, Kyrre Wahtne and the staff at MARIARC for comments on an earlier draft and assistance with fMRI data acquisition.

Author Contributions Conceived and designed the experiments: SMP DS. Performed the experiments: SMP. Analyzed the data: SMP. Wrote the paper: SMP DS. Contributed stimuli for experiments: DS.