Prenatal androgen blockade accelerates pubertal development in male rhesus monkeys

Herman, Rebecca A.; Zehr, Julia L.; Wallen, Kim

doi:10.1016/j.psyneuen.2005.06.004

Cited by 38 publications

(50 citation statements)

References 42 publications

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“…The monkey prefrontal cortex continues to undergo anatomical maturation during adolescence and early adulthood, similar to the human pattern of development (26,33,34). From a developmental standpoint, the male rhesus monkey enters puberty (the typical transition point between the juvenile and adolescent state) at ∼3.5 y of age, equivalent to 11 y in humans (19,35). Some developmental studies suggest, however, that the human adolescent prefrontal cortex is more similar to that of the juvenile, 2-to 3-y old macaque (26,36).…”

Section: Discussionmentioning

confidence: 99%

Age-dependent changes in prefrontal intrinsic connectivity

Zhou

Zhu

Katsuki

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The prefrontal cortex continues to mature after puberty and into early adulthood, mirroring the time course of maturation of cognitive abilities. However, the way in which prefrontal activity changes during peri-and postpubertal cortical maturation is largely unknown. To address this question, we evaluated the developmental stage of peripubertal rhesus monkeys with a series of morphometric, hormonal, and radiographic measures, and conducted behavioral and neurophysiological tests as the monkeys performed working memory tasks. We compared firing rate and the strength of intrinsic functional connectivity between neurons in peripubertal vs. adult monkeys. Notably, analyses of spike train cross-correlations demonstrated that the average magnitude of functional connections measured between neurons was lower overall in the prefrontal cortex of peripubertal monkeys compared with adults. The difference resulted because negative functional connections (indicative of inhibitory interactions) were stronger and more prevalent in peripubertal compared with adult monkeys, whereas the positive connections showed similar distributions in the two groups. Our results identify changes in the intrinsic connectivity of prefrontal neurons, particularly that mediated by inhibition, as a possible substrate for peri-and postpubertal advances in cognitive capacity. neurophysiology | cognitive development T he prefrontal cortex, the brain area associated with the highestlevel cognitive operations, is known to undergo a protracted period of development (1-3). A virtually linear increase in performance with age has been observed in tasks that assess visuospatial working memory, executive control, and resistance to distraction, a process that continues well after puberty and into early adulthood (4, 5). The accrual of cognitive capacities during this period parallels structural changes of the prefrontal cortex in humans and nonhuman primates (6-10). Imaging studies in humans suggest that patterns of brain activation associated with working memory tasks undergo distinct changes between childhood and adulthood, supporting the idea of prolonged prefrontal maturation (11)(12)(13)(14). However, how the patterns of prefrontal activation change during cortical maturation remains unclear. A possible mechanism that could account for variations in prefrontal responsesand which could have a significant functional impact (15)-is an overall change in the distribution of intrinsic functional connections, i.e., those between neurons within the prefrontal cortex. The intrinsic connectivity of a network is directly related to the correlation structure of neuronal responses, and this determines in a fundamental way the information-coding properties of the network and its ability to sustain activity on its own (16)(17)(18). In this study, we sought to determine if the strengths of functional connections inferred from multisite neurophysiological recordings differ between peripubertal and adult monkeys. ResultsWe obtained neurophysiological recordings from eigh...

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Section: Discussionmentioning

confidence: 99%

Age-dependent changes in prefrontal intrinsic connectivity

Zhou

Zhu

Katsuki

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…More insight into the developmental differences in the role of androgens comes from the use of flutamide, an androgen receptor blocker. Prenatal flutamide treatment during early gestation accelerates pubertal timing in male monkeys (Herman et al, 2006). Indirect evidence that this could involve hypothalamic effects arises from the stimulation of LH levels and pulse frequency after flutamide treatment for 3 days in adult men (Urban et al, 1988).…”

Section: Critical Windows For the Effects Of Sex Steroids On Pubertymentioning

confidence: 99%

Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: Revision of human observations and mechanistic insight from rodents

Parent

Franssen

Fudvoye

et al. 2015

Frontiers in Neuroendocrinology

161

140

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Puberty presents remarkable individual differences in timing reaching over 5 years in humans. We put emphasis on the two edges of the age distribution of pubertal signs in humans and point to an extended distribution towards earliness for initial pubertal stages and towards lateness for final pubertal stages. Such distortion of distribution is a recent phenomenon. This suggests changing environmental influences including the possible role of nutrition, stress and endocrine disruptors. Our ability to assess neuroendocrine effects and mechanisms is very limited in humans. Using the rodent as a model, we examine the impact of environmental factors on the individual variations in pubertal timing and the possible underlying mechanisms. The capacity of environmental factors to shape functioning of the neuroendocrine system is thought to be maximal during fetal and early postnatal life and possibly less important when approaching the time of onset of puberty.

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“…All subjects have been studied throughout infancy, the juvenile period, and puberty, and subtle but significant effects of the treatments have been seen in their morphology and endocrinology (Herman et al, 2000), developmental timing (Herman et al, 2006), vocal communication (Tomaszycki et al, 2001, and social behavior (Herman et al, 2003;Wallen, 2005).…”

Section: Subjectsmentioning

confidence: 99%

“…Treatments produced six experimental and two control groups of subjects as shown in Table 1. Androgen-treated male offspring were not included in this study as a result of subject loss over the 8 years of this extended study.All subjects have been studied throughout infancy, the juvenile period, and puberty, and subtle but significant effects of the treatments have been seen in their morphology and endocrinology (Herman et al, 2000), developmental timing (Herman et al, 2006), vocal communication (Tomaszycki et al, 2001, and social behavior (Herman et al, 2003;Wallen, 2005).For all habituation, training, and testing, subjects were temporarily removed from their social groups using procedures to which all subjects were already fully accustomed. All females tested in the first three months of testing performed trials with their infant offspring present on their ventrum.…”

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confidence: 99%

Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure

Herman

Wallen

2007

Hormones and Behavior

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Men and women differ on performance and strategy on several spatial tasks. Rodents display similar sex differences, and manipulations of early hormone exposure alter the direction of these differences. However, most cognitive testing of nonhuman primates has utilized sample sizes too small to investigate sexually-differentiated behaviors. This study presents an investigation of sex differences and the effects of prenatal androgen on spatial memory and strategy use in rhesus monkeys. Monkeys prenatally exposed to vehicle, testosterone, or the androgen receptor blocker flutamide performed a search task in which 5 of 12 goal boxes contained food rewards. Spatial consistency and the presence of local landmarks were varied. Performance when both spatial and marker cues were available did not differ by sex or prenatal treatment. Contrary to predictions, females easily solved the task when local markers were removed, and their performance outscored males. Although eliminating spatial consistency and requiring subjects to use local markers impaired performance by all monkeys, females continued to locate correct goal boxes at higher than chance levels and scored better than males. Blocking prenatal androgen exposure in males improved use of local markers. These findings suggest that the tendency to attend to landmarks and to use them in solving spatial problems is typical of females across many species, including rodents, humans, and rhesus monkeys. In rhesus monkeys and rodents, developmental androgen eliminates this specialization. However, these results are the only known example of better performance of females than males when salient markers are removed.Keywords rhesus monkey; spatial cognition; sex differences; testosterone; flutamide; prenatal; landmarks On a variety of spatially-demanding tasks, men outperform women. Tests of mental rotation, the ability to imagine the rotation of a two-or three-dimensional object rapidly, provide the largest and most reliable sex differences (Linn and Petersen, 1985), but performance differences exist in other spatial abilities also, including the ability to quickly and accurately learn a described route (Galea and Kimura, 1993;Ward et al., 1986). Not only do differences exist in overall performance, but men and women tend to use different strategies in maplearning and navigation. Men use cardinal directions and mileage estimates more, whereas women rely upon landmarks more (Galea and Kimura, 1993;Lawton, 1994Lawton, , 1996Saucier et al., 2002;Ward et al., 1986). Choice of strategy may be the important difference as route 1 To whom correspondence should be addressed: Department of Psychology Emory University 532 N. Kilgo Circle Atlanta, Georgia 30322 E-mail: rebecca.herman@gmail.com Phone: 678-637-1357 Fax: 404-727-0372 Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and ...

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Prenatal androgen blockade accelerates pubertal development in male rhesus monkeys

Cited by 38 publications

References 42 publications

Age-dependent changes in prefrontal intrinsic connectivity

Age-dependent changes in prefrontal intrinsic connectivity

Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: Revision of human observations and mechanistic insight from rodents

Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure

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