Early life exposure to unpredictable parental sensory signals shapes cognitive development: Evidence from 3 species

• In Event: Unpredictable Environmental Input and Socioemotional and Cognitive Development

Abstract

Mental and cognitive health and vulnerability to neuropsychiatric disorders involve an interplay of genes and environment, especially during sensitive developmental periods. Both genetic and environmental factors contribute to the development and maturation of neurons, synapses and the resulting brain circuits. Whereas the environmental signals for the sculpting of visual and auditory circuits (visual patterns, auditory tone patterns), are known, the nature of the signals and signal patterns that influence normal or aberrant maturation of emotional and cognitive brain circuits is less well understood. Early in life, essential environmental signals arise from the parent/caregiver. Indeed, across species, the enduring impact of quality of parental care is well established. However, whether patterns of parental signals contribute to neural circuit development and consequent behavioral phenotypes is unclear. We employ prospective longitudinal studies concurrently in experimental animals (rodents), as well as monkeys and humans to determine the role of patterns of maternal behaviors, focusing on their unpredictability in the maturation of cognitive outcomes. Methods: Briefly, parent-child interactions are observed during infancy (2 to 7 days in rats, 3 months in monkeys, and 6 and 12 months in humans) and species relevant sensory signals from the parent to the infant/pup are recorded. To quantify unpredictability across species, we computed entropy rates. These define the degree to which one behavior predictably leads to another, thus providing an index of the predictability of sensory signals that the mother provides to her infant/pup, that is aligned across species. Memory outcomes were assessed in the juvenile period for all 3 species (rats: novel object recognition; monkeys: delayed non match to sample; humans: continuous recognition memory). Results: We find that unpredictable parental signals influence memory function across species. Specifically, higher entropy rate, indicating more unpredictable signals, was associated with significantly poorer performance on memory tasks. Importantly for the human finding, the impact of unpredictability remains significant after covarying established contributions of early-life adversities including socioeconomic status and parental mental health. Discussion: In summary, these cross-species studies highlight that unpredictable patterns of parental signals during the sensitive period of infancy may contribute to subsequent memory function and suggest that the developmental importance of unpredictable signals is conserved across species. The mechanisms for these robust effects will be discussed and involve aberrant synaptic growth and pruning, apparent in animal studies, and, across species, aberrant neural circuit maturation assessed with diffusion tensor imaging (DTI).

Authors

• Elysia Poggi Davis, University of Denver
  Presenting Author

• Kai McCormack, Spelman College & Emory University

• Hina Arora, University of California-Irvine

• Desiree Sharpe, University of Georgia

• Annabel K Short, University of California-Irvine

• Laura Glynn, Chapman University

• Curt Sandman, University of California, Irvine

• Hal Stern, University of California-Irvine

• Mar M. Sanchez, Emory University

• Tallie Z Baram, University of California-Irvine