Early adversity and the neotenous human brain - Tottenham - 2019 - Article

Neoteny is the delaying or slowing of the physiological development of an organism. Humans have a specifically neotenous brain development. The prolonged brain development has multiple sensitive periods, which are developmental moments when the environment has an especially potent and enduring impact on developing neurobiology. The brain develops in a hierarchical way. The structure and function of earlier-developing regions exert maturational consequences on the structure and function of later-developing regions, also called developmental cascades.

What is neoteny and why is it special in humans?

Neoteny is the delaying or slowing of the physiological development of an organism. Humans have a specifically neotenous brain development. The prolonged brain development has multiple sensitive periods, which are developmental moments when the environment has an especially potent and enduring impact on developing neurobiology. The brain develops in a hierarchical way. The structure and function of earlier-developing regions exert maturational consequences on the structure and function of later-developing regions, also called developmental cascades.

What is the advantage for human neotenous brain development?

Humans depend on learning from a very complex environment to produce many different behaviors. A delayed onset of adult phenotypes provides more opportunities for learning these behavioral repertoires and developing strategies appropriate to the given environment.

What are characteristics of the amygdala-medial prefrontal cortex (mPFC) circuitry?

In humans, the amygdala-mPFC circuitry is central to mature emotional behaviors, such as learning, modulation, attention, and prediction. Looking at the principles of neoteny and development in the context of early caregiving adversity, the following characteristics are of importance:

• Amygdala-mPFC circuitry constitutes the foundation for behaviors associated with emotion regulation in adulthood. These behaviors are often affected by early life stress.
• Amygdala-mPFC circuitry is highly sensitive to environmental influences during development.
• The amygdala is rich with stress hormone receptors, especially early in life. It exhibitis membrane potential characteristics early in development that make it highly reactive to stressors.

How does the amygdala-mPFC develop?

Human development shows strong amygdala activity and emotionality early in life. It is then followed by adult-like amygdala-mPFC connections and associated declines in emotionality at older ages. Frontotemporal tracts mature later than other tracts, paralleled by correlated activity between the amygdala and mPFC (functional connectivity). Amygdala-mPFC functional connectivity continues to change developmentally until early adulthood.

How do parents modulate early emotional learning?

Research shows that there appears to be a mechanism by which children learn to prefer and attach to parental cues. Early emotional learning systems are constructed to allow for modification by the parents. The presence of parents/caregivers provides a social scaffolding for the developing child, which may also be scaffolding the amygdala-mPFC circuitry. Parental stimuli can produce a momentary adult-like amygdala-mPFC connectivity pattern in children. Between childhood and adolescence, this circuitry changes and begins to show adult-like regulatory connectivity patterns. During adolescence, parental presence becomes less necessary in modulating this circuitry, which becomes more adult-like.

How does variation in parenting behavior influence the amygdala-mPFC circuitry?

Parental care (e.g. attachment styles, parental sensitivity) has been shown to correlate with the amygdala-mPFC circuitry structure and function. Caregiving adversities may have a profound impact on emotional development and psychopathology risk due to the sensitive periods that occur that let neurobiological systems be vulnerable to environmental pressures. Adverse caregiving appears to accelerate the development of the amygdala-mPFC circuitry, in order to help the person navigate stressors and threats independently without parental care. However, this may attenuate developmental plasticity and have adverse consequences on later functions that depend on learning and slow growth during early sensitive periods.

What is developmental multifinality?

Developmental multifinality refers to divergent developmental pathways for two individuals who begin with similar risk. The mental health outcomes associated with amygdala-mPFC development show significant heterogeneity and many youths exhibit psychological resilience despite exposure to adversity. It is not clear why these differences exist or how to predict them. It is possible that positive, strength-promoting experiences, such as interventions that target parental nurturance, sensitivity, and threatening behaviors, compete with adverse experiences and alleviate developmental outcomes after adverse experiences.