The developmental consequences of early adverse care on infant macaques: A cross-fostering study

McCormack, Kai M.; Howell, Brittany R.; Higgins, Melinda; Bramlett, Sara N; Guzman, Dora; Morin, Elyse; Villongco, C.; Liu, Y.; Meyer, Jerrold S.; Sanchez, Maria

doi:10.1016/j.psyneuen.2022.105947

Cited by 10 publications

(28 citation statements)

References 48 publications

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“…McCormack et al, 2006K. McCormack et al, , 2009K. M. McCormack et al, 2022;Morin et al, 2019Morin et al, , 2020Morin et al, , 2022Wakeford et al, 2018) and profiled total RNA in circulating plasma EVs obtained from adolescent macaques that had received nurturing care (CONT) or maltreatment (MALT) from their mothers as infants.…”

Section: Discussionmentioning

confidence: 99%

“…Part of a larger longitudinal study of the effects of ELA, the animals in our study were well-characterized throughout infancy and the pre-pubertal period (Drury et al, 2017; Howell et al, 2013, 2017; K. M. McCormack et al, 2022; Morin et al, 2020). Six of the subjects (3 males and 3 females) experienced maternal maltreatment (MALT), and the other seven (4 males and 3 females) received nurturing maternal care (CONT).…”

Section: Methodsmentioning

confidence: 99%

“…Part of a larger longitudinal study of the effects of ELA, the animals in our study were wellcharacterized throughout infancy and the pre-pubertal period (Drury et al, 2017;Howell et al, 2013Howell et al, , 2017K. M. McCormack et al, 2022;Morin et al, 2020).…”

Section: Subjectsmentioning

confidence: 99%

“…Six of the subjects (3 males and 3 females) experienced maternal maltreatment (MALT), and the other seven (4 males and 3 females) received nurturing maternal care (CONT). Infant maltreatment is defined by co-morbid experience of maternal physical abuse, rejection and neglect of the infant during the first three months of life, resulting in pain, emotional distress, and elevations in stress hormones (Drury et al, 2017;Howell et al, 2013Howell et al, , 2017Maestripieri et al, 2000;Maestripieri & Carroll, 1998;McCormack et al, 2006McCormack et al, , 2009McCormack et al, , 2015McCormack et al, , 2022. Animals in the CONT group were the recipients of positive caregiving behaviors like cradling and grooming and none of the physical abuse or rejection experienced by MALT animals.…”

Section: Subjectsmentioning

confidence: 99%

“…Additionally, an unfortunate but ideal experimental framework within which to ask these questions would be one in which childhood maltreatment is the form of ELA that infants experience, and in which the maltreatment encapsulates both, neglect and physical abuse, without other confounding factors like prenatal exposure to drugs, lack of access to proper nutrition and medical care. To satisfy these criteria and gain better insights into the etiology and biomarkers of maltreatment-exacerbated disruptions to physiology and behavior, we used a highly translational and naturally occurring model of infant maltreatment in which rhesus macaques are recipients of both, physical abuse and neglect (in the form of infant rejection), from mothers during infancy (Drury et al, 2017; K. M. McCormack et al, 2022). Next, during adolescence we profiled RNA found in extracellular vesicles (EVs) circulating in the plasma of animals that had experienced infant maltreatment and compared this profile to RNA in EVs extracted from animals reared with nurturing maternal care.…”

Section: Introductionmentioning

confidence: 99%

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RNA in extracellular vesicles during adolescence reveal immune, energetic and microbial imprints of early life adversity

Korobkova

Morin

Aoued³

et al. 2023

Preprint

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Exposure to early life adversity (ELA), including childhood maltreatment, is one of the most significant risk factors for the emergence of neuropsychiatric disorders in adolescence and adulthood. Despite this relationship being well established, the underlying mechanisms remain unclear. One way to achieve this understanding is to identify molecular pathways and processes that are perturbed as a consequence of childhood maltreatment. Ideally, these perturbations would be evident as changes in DNA, RNA or protein profiles in easily accessible biological samples collected in the shadow of childhood maltreatment. In this study, we isolated circulating extracellular vesicles (EVs) from plasma collected from adolescent rhesus macaques that had either experienced nurturing maternal care (CONT) or maternal maltreatment (MALT) in infancy. RNA sequencing of RNA in plasma EVs and gene enrichment analysis revealed that genes related to translation, ATP synthesis, mitochondrial function and immune response were downregulated in MALT samples, while genes involved in ion transport, metabolism and cell differentiation were upregulated. Interestingly, we found that a significant proportion of EV RNA aligned to the microbiome and that MALT altered the diversity of microbiome-associated RNA signatures found in EVs. Part of this altered diversity suggested differences in prevalence of bacterial species in CONT and MALT animals noted in the RNA signatures of the circulating EVs. Our findings provide evidence that immune function, cellular energetics and the microbiome may be important conduits via which infant maltreatment exerts effects on physiology and behavior in adolescence and adulthood. As a corollary, perturbations of RNA profiles related to immune function, cellular energetics and the microbiome may serve as biomarkers of responsiveness to ELA. Our results demonstrate that RNA profiles in EVs can serve as a powerful proxy to identify biological processes that might be perturbed by ELA and that may contribute to the etiology of neuropsychiatric disorders in the aftermath of ELA.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Subjectsmentioning

confidence: 99%

Section: Subjectsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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RNA in extracellular vesicles during adolescence reveal immune, energetic and microbial imprints of early life adversity

Korobkova

Morin

Aoued³

et al. 2023

Preprint

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Hair and plasma cortisol throughout the first 3 years of development in infant rhesus macaques, Macaca mulatta

Pritchard,

Capitanio,

Del Rosso

et al. 2023

Developmental Psychobiology

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Cortisol expression has been demonstrated to have variation across development in rhesus macaques (Macaca mulatta). There exists contradictory evidence for the nature of this change, and age at which it occurs, across biological sample types. Consequently, we lack a cohesive understanding for cortisol concentrations across the development of a major human health translational model. We examined hair cortisol concentrations over the first 3 years of life for 49 mother‐reared infant macaques from mixed‐sex outdoor units at the California National Primate Research Center. For 48 of these subjects at infancy, 1 year, and 2 years, we obtained plasma cortisol samples for response to a stressor, adjustment to prolonged stress, and response to dexamethasone injection. Hair cortisol concentrations decreased dramatically between 3 and 10 months, followed by relative stability up to the final sampling event at around 34 months of age. Plasma cortisol showed within‐year consistency, and consistency between infancy and year 1. We document variability in the infant plasma cortisol samples, especially in percent change between samples 1 and 2. Our plasma cortisol results indicate that infants possess the physiological capacity to effectively inhibit the release of cortisol when stimulated, as effectively as later responses in juveniles. Age‐related changes in hair cortisol parallel findings indicating a large decline in the weeks following postparturation.

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Early life adversities and lifelong health outcomes: A review of the literature on large, social, long-lived nonhuman mammals

Dettmer

Chusyd²

2023

Neuroscience & Biobehavioral Reviews

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The developmental consequences of early adverse care on infant macaques: A cross-fostering study

Cited by 10 publications

References 48 publications

RNA in extracellular vesicles during adolescence reveal immune, energetic and microbial imprints of early life adversity

RNA in extracellular vesicles during adolescence reveal immune, energetic and microbial imprints of early life adversity

Hair and plasma cortisol throughout the first 3 years of development in infant rhesus macaques, Macaca mulatta

Early life adversities and lifelong health outcomes: A review of the literature on large, social, long-lived nonhuman mammals

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