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Abstract
Childhood maltreatment is a form of early life stress associated with severe behavioral, socioemotional, and cognitive developmental outcomes. The present study used a translational animal model to evaluate specific cognitive consequences of maternal maltreatment. Newborn rhesus monkeys (Macaca mulatta; n = 36, 16 male, 20 female) were cross-fostered with multiparous mothers who previously had been identified as either maltreating or competent based on established measures of abuse and neglect. At 18 months of age, subjects participated in a series of cognitive tasks that assessed some prefrontal cortex (PFC)-mediated cognitive functions, including behavioral flexibility and inhibitory control (Object Retrieval Detour task, ORD), and working memory (Delayed-Non-Matching-to-Sample Session Unique, DNMS-SU). Maternal behavior data, including frequency of abuse, rejection, restraint, and scores on a maternal rating scale designed to address maternal behavior dimensions (Sensitivity/Responsivity, Protectiveness, Attachment, and Irritability) were collected, as well as CSF concentrations of the monoamine metabolites 5-HIAA, HVA, and MHPG, and a primary stress neuropeptide, CRF. Although there was no effect of experimental group, sex differences, or interactions on cognitive task performance or CSF monoamine metabolite concentrations and CRF levels, we found significant correlations between dimensions of maternal care and performance on the ORD and DNMS-SU, as well as between CSF measures and cognitive task performance. On the ORD task, animals that experienced high rates of rejection were more likely to balk following an initial attempt on a trial, and monkeys who experienced more restraint and responsivity from their mothers exhibited increased Day 1 latencies. Furthermore, 5-HIAA, a serotonin metabolite, was correlated with barrier and perseverative reaches, indicating altered serotonergic ofPFC-mediated cognition in animals who perseverated. On the DNMS-SU task, animals that experienced more abuse and restraint committed more errors to criterion. Our results indicate that in addition to the continued investigation of neurochemical substrates of altered cognition in maltreated individuals, it is critical that we examine global dimensions of maternal maltreatment in order to better explore the qualities of maternal care that may have more impact on the behavioral, neurodevelopmental, and cognitive outcomes of maltreated monkeys than frequency rates of abuse and/or rejection alone.