Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?

Abstract

Postnatal brain development is studded with sensitive periods during which experience dependent plasticity is enhanced. This enables rapid learning from environmental inputs and reorganization of cortical circuits that matches behavior with environmental contingencies. Significant headway has been achieved in characterizing and understanding sensitive period biology in primary sensory cortices, but relatively little is known about sensitive period biology in associative neocortex. One possible mediator is the onset of puberty, which marks the transition to adolescence, when animals shift their behavior toward gaining independence and exploring their social world. Puberty onset correlates with reduced behavioral plasticity in some domains and enhanced plasticity in others, and therefore may drive the transition from juvenile to adolescent brain function. Pubertal onset is also occurring earlier in developed nations, particularly in unserved populations, and earlier puberty is associated with vulnerability for substance use, depression and anxiety. In the present article we review the evidence that supports a causal role for puberty in developmental changes in the function and neurobiology of the associative neocortex. We also propose a model for how pubertal hormones may regulate sensitive period plasticity in associative neocortex. We conclude that the evidence suggests puberty onset may play a causal role in some aspects of associative neocortical development, but that further research that manipulates puberty and measures gonadal hormones is required. We argue that further work of this kind is urgently needed to determine how earlier puberty may negatively impact human health and learning potential.

Changes in cognitive flexibility and hypothesis search across human life history from childhood to adolescence to adulthood

“…In particular, although adolescents have more accumulated experience than younger children, there is evidence, as noted above, that adolescence may also be a period of enhanced plasticity and learning (59,60), especially for social domains (32,61), in part through the privileging of social information processing and the salience of social rewards in decision making (62,63). Cultural innovations, such as new socially significant forms of language, dress, or music often first appear in adolescents.…”

Puberty and structural brain development in humans

“…Although the longitudinal studies have attempted to account for individual differences, more research is needed to truly understand how individual differences in pubertal onset and tempo may influence developmental outcomes. In fact, the influence of individual’s progression through puberty and its impact on brain development remains an understudied area (Piekarski, Johnson et al 2016). To study both onset and progression, studies would need to begin studying children as early as ages 6 or 7, before the onset of adrenarche and the re-activation of the HPG-axis.…”

“…Thus, there is great interest in understanding how sex hormones and puberty influence typical brain development as a point of reference in identifying differences in biomarkers of risk for, or resilience against, adolescent psychopathology in boys versus girls (Blakemore, Burnett et al 2010, Naninck, Lucassen et al 2011, Ladouceur 2012, Ladouceur, Peper et al 2012). Thus, pubertal-related timing of region specific brain changes may contribute to sex-specific differences in the rapid and disproportionate increases in rates of psychopathology seen between girls and boys (Berenbaum, Beltz et al 2015, Piekarski, Johnson et al 2016). As previously alluded to, timing and tempo of pubertal maturation has been linked with various psychological outcomes, including internalizing behaviors (Mendle, Leve et al 2014) and depression (Angold, Costello et al 1998, Angold, Costello et al 1999).…”

Ovarian Hormones Organize the Maturation of Inhibitory Neurotransmission in the Frontal Cortex at Puberty Onset in Female Mice

“…The onset of adolescence, initiated by the onset of puberty, is increasingly recognized as an inflection point for the development of associative regions of the neocortex [1]. Across mammals, adolescence is characterized by changes to cognitive and executive functions that coincide with large-scale reorganization of associative cortical regions, including the frontal cortex [2–4].…”

“…This period of development is also associated with declining plasticity in language-related circuits, declining capacity for recovery from cortical damage[5–11], and increased risk of psychiatric disease[3, 12]. While it remains unclear if these developmental changes are caused by the pubertal rise in gonadal hormones or are simply coincident [1], it is clear that early puberty onset exacerbates risk of psychiatric illnesses connected to frontal functions[13–15], suggesting a possible causal link. Gonadal steroid receptors are present across the neocortex [16–18], and a number of anatomical changes in human cortex correlate with changes in hormone levels during puberty [19–23].…”