Rank acquisition in rhesus macaque yearlings following permanent maternal separation: The importance of the social and physical environment

Wooddell, Lauren J.; Kaburu, Stefano S. K.; Murphy, Ashley M.; Suomi, Stephen J.; Dettmer, Amanda M.

doi:10.1002/dev.21555

Cited by 14 publications

(40 citation statements)

References 75 publications

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“…Our results provide preliminary evidence that maternal rank inheritance persists for mother‐reared individuals initially reared together. This finding is similar to previous studies indicating that infants reared in large multigenerational groups obtained identical relative ranks as their mothers following separation (Wooddell et al., ), even following social instability, suggesting that their relative ranks were socially transmitted early in development (i.e., within the first 8 months of life) and persistent. Given that social status is a characteristic of relationships, it is possible that early relationships in infancy may be maintained through at least juvenility.…”

Section: Discussionsupporting

confidence: 91%

“…However, not all mother‐reared subjects were reared in the same harem groups in infancy ( N = 5 different groups), thus providing no social experience with the other mothers in the other rearing groups. This experience with the other mothers may be an important requisite for acquisition of relative status (Wooddell et al., ). When we examined mother‐reared dyads that were reared together in infancy, 8/10 (80%) of their dyadic statuses were predicted by their mothers’ dyadic statuses, which is greater than what could be expected by chance (one sample t test: t 9 = 2.25, p = 0.05, d = 0.71).…”

Section: Resultsmentioning

confidence: 99%

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Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

Wooddell¹,

Simpson

Murphy

et al. 2018

Developmental Science

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In humans, socioeconomic status (SES) has profound outcomes on socio-emotional development and health. However, while much is known about the consequences of SES, little research has examined the predictors of SES due to the longitudinal nature of such studies. We sought to explore whether interindividual differences in neonatal sociality, temperament, and early social experiences predicted juvenile social status in rhesus monkeys (Macaca mulatta), as a proxy for SES in humans. We performed neonatal imitation tests in infants' first week of life and emotional reactivity assessments at 2 and 4 weeks of age. We examined whether these traits, as well as the rearing environment in the first 8 months of life (with the mother or with same-aged peers only) and maternal social status predicted juvenile (2-3 years old) social status following the formation of peer social groups at 8 months. We found that infants who exhibited higher rates of neonatal imitation and newborn emotional reactivity achieved higher social status as juveniles, as did infants who were reared with their mothers, compared to infants reared with peers. Maternal social status was only associated with juvenile status for infant dyads reared in the same maternal group, indicating that relative social relationships were transferred through social experience. These results suggest that neonatal imitation and emotional reactivity may reflect ingrained predispositions toward sociality that predict later outcomes, and that nonnormative social experiences can alter socio-developmental trajectories. Our results indicate that neonatal characteristics and early social experiences predict later social outcomes in adolescence, including gradients of social stratification.

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Section: Discussionsupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

Wooddell¹,

Simpson

Murphy

et al. 2018

Developmental Science

Self Cite

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“…Because the ␣S T:M ratio is increasingly recognized as a relevant measure of ␣S pathology (Wooddell et al, 2017;Kim et al, 2018;Nuber et al, 2018;Fanning et al, 2019), we analyzed the potential hormone regulation on this ␣S homeostasis. Although we observed a statistically nonsignificant trend toward the ␣S60 tetramer level, female estrogen significantly increased 3K ␣S tetramerization toward the physiological T:M ratio of phenotypically normal WT mice while displaying lesser ␣S14 monomer signals at the Triton X-100-soluble membrane fraction.…”

Section: Discussionmentioning

confidence: 99%

Female Sex and Brain-Selective Estrogen Benefit α-Synuclein Tetramerization and the PD-like Motor Syndrome in 3K Transgenic Mice

et al. 2019

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Many studies report a higher risk for Parkinson's disease (PD) and younger age of onset in men. This, and the fact that the neuropathological process underlying PD symptoms may begin before menopause, suggests that estrogen-based hormone therapy could modify this higher risk in males. However, the effects of female sex or estrogen on ␣-synuclein (␣S) homeostasis and related PD neuropathology remain unknown. Here, we used an ␣S tetramer-abrogating mouse model of PD (3K) that amplifies the familial E46K PD mutation to investigate the effects of female sex and brain-selective estrogen treatment on ␣S tetramerization and solubility, formation of vesicle-rich ␣S ϩ aggregates, dopaminergic and cortical fiber integrity, and associated motor deficits. In male 3K mice, the motor phenotype became apparent at ϳ10 weeks and increased to age 6 months, paralleled by PD-like neuropathology, whereas 3K females showed a significant delay in onset. At 6 months, this beneficial phenotypic effect in 3K females was associated with a higher ␣S tetramer-to-monomer ratio and less decrease in dopaminergic and cortical fiber length and quantity. Brain-selective estrogen treatment in symptomatic 3K mice significantly increased the tetramer-to-monomer ratio, turnover by autophagy of aggregate-prone monomers, and neurite complexity of surviving DAergic and cortical neurons, in parallel with benefits in motor performance. Our findings support an upstream role for ␣S tetramer loss in PD phenotypes and a role for estrogen in mitigating PD-like neuropathology in vivo. Brain-selective estrogen therapy may be useful in delaying or reducing PD symptoms in men and postmenopausal women.

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“…Second, unlike mother‐reared infants, nursery‐reared monkeys showed no effects of maternal dominance rank on looking patterns. Even though dominance rank can affect monkeys’ behavioral tendencies and glucocorticoid regulation (Kohn, Snyder‐Mackler, Barreiro, Johnson, Tung, & Wilson, ), immune regulation (Snyder‐Mackler et al, ), learning (Bunnell, Kenshalo Jr, Allen, Manning & Sodetz, ), and even epigenetic changes during prenatal development (Massart, Suderman, Nemoda, Sutti, Ruggiero, Dettmer, Suomi, & Szyf, ), this lack of an effect for dominance rank in nursery‐reared monkeys in the current study suggests that: 1) postnatal rank inheritance is more of a social rather than a biological construct (Wooddell, Kaburu, Murphy, Suomi, & Dettmer, ) and 2) facial processing may be influenced by social rather than biological mechanisms, particularly via interactions with the mother or caregiver.…”

Section: Discussionmentioning

confidence: 99%

Sex and rank affect how infant rhesus macaques look at faces

Paukner

Slonecker

Murphy

et al. 2017

Developmental Psychobiology

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We investigated how differences in infant sex and mothers’ dominance status affect infant rhesus macaques’ (Macaca mulatta) interest in visually exploring emotional facial expressions. Thirty-eight infants were presented with animated avatars of macaque facial expressions during the first month of life. Sons of high-ranking mothers looked more at faces, especially the eye region, than sons of low-ranking mothers, but no difference in looking duration was found for daughters. Males looked significantly more at eyes than females, but this effect was reversed in infants who were reared without mothers in a primate nursery facility. In addition, in mother-infant interactions, mothers of sons were more likely to gaze at their infant’s face compared to mothers of daughters. Combined with previous research indicating that rhesus macaque mothers interact differently with infants based on their own rank and infant’s sex, these results support the view that social experiences shape early face preferences in rhesus macaques.

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Rank acquisition in rhesus macaque yearlings following permanent maternal separation: The importance of the social and physical environment

Cited by 14 publications

References 75 publications

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

Female Sex and Brain-Selective Estrogen Benefit α-Synuclein Tetramerization and the PD-like Motor Syndrome in 3K Transgenic Mice

Sex and rank affect how infant rhesus macaques look at faces

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