How early-life patterns of parental signals enduringly sculpt the developing brain

• In Event: 1-206 - Early life exposure to unpredictable maternal signals influences child development: A cross species approach.

Integrative Statement

Mental illnesses originate early in life, governed by combined environmental and genetic factors. Indeed, 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 are known (light, sound), the nature of the signals that influence normal or aberrant maturation of emotional and cognitive brain circuits has not been fully resolved.

During prenatal- as well as early in postnatal life, the major source of crucial environmental signals is the mother and /or principal care-taker. Indeed, parental signals--–starting with maternal signals in utero--are major contributors to children’s mental health. Not surprisingly, a robust body of work has focused on parental signals in both humans and experimental models. However, which maternal signals are salient to optimal brain development, how these signals reach specific populations of neurons and how they influence neuronal and behavioral phenotype enduringly is remained unresolved.

Whereas the vast majority of existing work has centered on the quantity, quality and valence (maternal depression, sensitivity) of maternal-derived signals, we identify here a novel dimension of maternal signals: their patterns. Specifically we discuss novel findings suggesting that patterns of maternal behaviors, and specifically fragmented and unpredictable patterns, are a critical factor that influences neuronal circuit maturation and behavioral phenotype.

In both rat and mouse experimental models, when fragmented/unpredictable maternal care patterns are induced while the quantity and qualitative aspects of maternal care remain unchanged, the disrupted patterns of maternal care directly induce aberrant synaptic connectivity and disturbed maturation of cognitive and emotional brain circuits. As shown in the illustration (Figure 1), the altered maturation of brain circuits can be visualized using diverse MR imaging modalities, enabling assessments of these findings across species.

Notably, the neurobiological disturbances are associated with altered cognitive and emotional behavioral problems including spatial memory deficits and anhedonia. Together, our findings across species demonstrate that patterns of maternal signals influence brain circuit maturation, promoting resilience or vulnerability to mental illness.

Authors

• Jessica L. Bolton, Departments of Pediatrics and Anatomy/Neurobiology, University of California-Irvine, Irvine, CA
  Presenting Author

• Short Annabel, Departments of Pediatrics and anatomy/Neurobiology; University of California-Irvine, Irvine, CA,
  Non-Presenting Author

• Jenny Molet, Departments of Pediatrics and anatomy/Neurobiology, University of California-Irvine, Irvine, CA
  Non-Presenting Author

• Tallie Baram, University of California-Irvine
  Non-Presenting Author