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Science Perspectives on Psychological Perspectives on Psychological Science http://pps.sagepub.com/ What Do Sex, Twins, Spotted Hyenas, ADHD, and Sexual Orientation Have in Common? Dennis McFadden Perspectives on Psychological Science 2008 3: 309 DOI: 10.1111/j.1745-6924.2008.00082.x The online version of this article can be found at: http://pps.sagepub.com/content/3/4/309 Published by: http://www.sagepublications.com On behalf of: Association For Psychological Science Additional services and information for Perspectives on Psychological Science can be found at: Email Alerts: http://pps.sagepub.com/cgi/alerts Subscriptions: http://pps.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav Downloaded from pps.sagepub.com at University of Texas Libraries on November 5, 2014 PERSPECTIVES ON PSYCHOLOGICAL SCIENCE What Do Sex, Twins, Spotted Hyenas, ADHD, and Sexual Orientation Have in Common? Dennis McFadden Department of Psychology and Center for Perceptual Systems, University of Texas ABSTRACT—The otoacoustic emissions (OAEs) measured in measures may exist. They are unquestionably imperfect, but we a collection of special populations of humans and certain now have measures that seem to be sensitive to the degree of nonhuman species suggest that OAEs may provide a win- exposure to androgens a developing fetus receives. Some read- dow into some processes of human prenatal development ers surely will find it bizarre that those measures come from the and sexual differentiation. For reasons that are unclear, auditory system. Even more bizarre, some of the measures in- OAEs appear to be highly sensitive to events occurring volve sounds that come out of the ear. during prenatal development that seem to be related to the There are still plenty of dangling threads, but if you like degree of exposure to androgens a fetus receives. The mysteries involving stacks of compelling (if circumstantial) (largely circumstantial) evidence for a relationship be- evidence, pleas for parsimony, and collections of odd and cu- tween androgen exposure and OAE strength comes from a rious facts, you are going to love this story. The tale itself is based series of studies of twins, children with attention-deficit/ on a collection of physiological measures of the auditory system hyperactivity disorder, people of differing sexual orienta- obtained from several special populations. The mystery is tions, and spotted hyenas, among others. Some conclusions whether some or all of those outcomes are attributable to a are bolstered by parallel studies using auditory evoked common cause and, if so, what that cause might be. In the end, potentials (AEPs). OAEs and AEPs are simple, objective, you will find that the scientific jury is still out, but at least you noninvasive measures that appear to have potential as will know the essence of the case as it currently stands, and you tools of value to researchers working on a wide variety of will know something about these measures that may be revealing basic and applied topics beyond audition. about aspects of prenatal development. Plus, you will have an- other example for use in class of how following one’s nose in science can lead into totally unexpected realms. Human prenatal development involves an enormously complex Before examining the details of the mystery, it is necessary to series of processes that culminate in an individual having a body cover some background material, both on prenatal development and brain ready both to experience the rich array of stimuli that and on the auditory system. Then, evidence from such sources as constitute the everyday world and to benefit and mature physi- spotted hyenas, human twins, children with attention-deficit/ ologically and behaviorally in a sex-typical manner in response hyperactivity disorder (ADHD), and people of differing sexual to those stimuli. Much of what happens during human prenatal orientation will be presented for your consideration. The back- development is currently inaccessible to us, so most of what we ground is a bit long, but along the way you are likely to learn a know comes from indirect measures, accidents of nature, and few new facts to spice up those tired old lectures you’ve been observations of other species. Imagine how valuable it would be giving on development and perception. Junkies for more detail to scientists of various stripes to have some simple, noninvasive can read the footnotes. measures that are obtainable from adults and that provide in- formation about one of those otherwise invisible processes op- BACKGROUND ON PRENATAL DEVELOPMENT erating on the brain during early development. Well, such In humans, as in all mammals, the two sexes emerge as follows. All eggs carry one X chromosome, and they are fertilized by Address correspondence to Dennis McFadden, Department of Psy- chology and Center for Perceptual Systems, University of Texas, sperm cells that carry either an X or a Y chromosome. As the Austin, TX 78712-0187; e-mail: [email protected]. fertilized egg divides and becomes an embryo, all subsequent r Volume 3—Number 4 DownloadedCopyright from pps.sagepub.com2008 Association at University forPsychological of Texas Libraries Science on November 5, 2014 309 Sex, Twins, and Hyenas daughter cells are either XX or XY depending on which type of dimensional space, and what implications it carries for the lis- sperm cell fertilized the egg. If the developing embryo is XY,it tener’s behavior. To make this transformation, a delicate mem- carries a gene, called SRY,ontheY chromosome that is activated brane inside the cochlea (the basilar membrane) is displaced up early in the first trimester of prenatal development, and that gene and down in accord with the movements at the eardrum, and is responsible for the development of embryonic testes in that XY sensitive cells residing on the basilar membrane (the cochlear embryo. The testes begin to manufacture androgens, including hair cells) sense that movement and initiate neural activity when testosterone, which diffuse throughout the developing embryo and the movement is sufficiently great. begin the process of masculinization of body, brain, and behavior. Besides receiving, transducing, analyzing, and processing in- That is, the normally developing male fetus masculinizes itself via coming sounds, the human cochlea also can make sounds of its its own production of androgens. Embryos lacking the Y chro- own (Kemp, 1978, 1979; Probst, Lonsbury-Martin, & Martin, mosome, and thus the SRY gene, do not develop testes, and those 1991; Shera & Guinan, 1999). These sounds, known as otoacoustic XX embryos develop with female bodies, brains, and behavior. emissions (OAEs), are generated by the mechanisms that evolved Because the absence of the SRY gene leads to a sequence of to give the mammalian inner ear the extremely high sensitivity it events that culminates in a female individual, it is common to see has. (At 1,000 Hz—about two octaves above middle C—the the process summarized as ‘‘in all mammals, including humans, weakest sound that can just be heard by a normal ear displaces the female is the default condition.’’ eardrum about 0.5 nm, or about the diameter of a potassium atom; The production of androgens by the testes of the developing Mead C. Killion, personal communication, February 8, 2007.) human male fetus peaks between Weeks 10 and 22 after con- Because the mechanisms that provide such high sensitivity ac- ception (Smail, Reyes, Winter, & Faiman, 1981), after which the tually increase the magnitude of the displacement of the basilar fetal androgen levels gradually decline so that the hormone membrane for weak sounds, the term cochlear amplifiers is com- levels of male and female infants are essentially identical at monly used to denote those mechanisms. Because each successive birth. Then, beginning at birth and lasting for about 20 weeks, location along the length of the basilar membrane (each adjacent the testes of the male infant produce a ‘‘second surge’’ of an- frequency region) has its own amplification devices, the cochlea drogens (Smail et al., 1981), after which the hormone levels in can be viewed as having a sequence of frequency-specific cochlear male and female children again are essentially identical until amplifiers arrayed along its length. There are several types of puberty (when chaos ensues). Thus, any sex difference in body, OAEs, but I will focus primarily on two of them: spontaneous brain, or behavior present at birth or present between about 6 OAEs (SOAEs) and click-evoked OAEs (CEOAEs). months of age and puberty cannot be attributable to differences To measure SOAEs, all one need do is insert a sensitive mi- in the existing circulating levels of sex hormones. Rather, those crophone into the external ear canal of a subject seated com- sex differences are either aftereffects of the sex differences in fortably in a sound-deadened room, record the sounds present in exposure to androgens experienced during prenatal or early the canal, do some simple processing to exclude the most noisy postnatal development or the result of environmental or so- moments in the recording (breathing, swallowing, movements of cialization processes operating after birth. (After puberty, of the jaw, neck, or head, etc.), and then represent the result as a course, any sex difference may carry a contribution from cur- frequency spectrum (Pasanen & McFadden, 2000). Any SOAEs rently circulating levels of hormones. Eventually some sex emerge as sharp peaks
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