Facing changes and changing faces in adolescence: a new model for investigating adolescent-specific interactions between pubertal, brain and behavioral development

Abstract

Adolescence is a time of dramatic physical, cognitive, emotional, and social changes as well as a time for the development of many social-emotional problems. These characteristics raise compelling questions about accompanying neural changes that are unique to this period of development. Here, we propose that studying adolescent-specific changes in face processing and its underlying neural circuitry provides an ideal model for addressing these questions. We also use this model to formulate new hypotheses. Specifically, pubertal hormones are likely to increase motivation to master new peer-oriented developmental tasks, which will in turn, instigate the emergence of new social/affective components of face processing. We also predict that pubertal hormones have a fundamental impact on the re-organization of neural circuitry supporting face processing and propose, in particular, that, the functional connectivity, or temporal synchrony, between regions of the face-processing network will change with the emergence of these new components of face processing in adolescence. Finally, we show how this approach will help reveal why adolescence may be a period of vulnerability in brain development and suggest how it could lead to prevention and intervention strategies that facilitate more adaptive functional interactions between regions within the broader social information processing network.

Graphical abstract

Fig. 1

A schematic representation of the dynamic changes that are predicted to initiate the emergence of new social and affective components of face processing in adolescence (i.e., fine-tuned attractiveness ratings and an own-age bias in identity recognition). In Hypothesis 1 (purple lines), we predict that the pubertal hormones that initiate the development of secondary sex characteristics and sexual dimorphisms in the structure of the face and brain are also are likely to influence motivation to master new developmental tasks, such as developing confiding friendships and romantic relationships with peers. This is manifest in the brain as a modulation in the functioning of limbic circuitry (particularly the amygdala), which induces dynamic changes in the functional organization of many neural circuits that interact with the amygdala, including the face processing system. These developmental tasks will in turn, drive the emergence of new social/affective components of face processing (Hypothesis 2 – blue lines). In other words, puberty induces adolescents to be socially and affectively motivated to encode new social information from faces that is related to these developmental tasks, such as the attractiveness, trustworthiness, competence, and social status of a face, particularly for peer-aged faces. Finally, in Hypothesis 3 (red lines), we argue that the dynamical interactions between neural face processing regions are fundamentally altered as a result of the surge of gonadal hormones and the resulting new task demands for face processing. Specifically, the functional/effective connectivity, or temporal synchrony, between regions of the face-processing network will change with the emergence of these new components of face processing in adolescence. This re-organization allows for new socially relevant information to be encoded from faces, leading to new components of face processing behavior. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

Fig. 2

Schematic drawings of the social information processing network described by Nelson et al. (2005) and the distributed face-processing network summarized by Gobbini and Haxby (2007). Note the similarity in functional organization of the two models, particularly between the detection node of the SIPN and the core face processing system as well as the affective node of the SIPN and the emotion component of the extended face processing network.

Fig. 3

Two-stage model of social behavior development. Perinatal hormone secretions sexually differentiate behavioral neural circuits and pubertal hormone secretions refine and “finish” these processes during adolescence to allow for the display of sex-typical social behavioral in adulthood.

Fig. 4

Topography of face-, place-, and object-related regions in separate groups of children, adolescents, and adults projected onto a representative inflated brain. All three age groups exhibit indistinguishable topography for the place- and object-related regions. Only adults and adolescents exhibited consistent activation in the core face processing regions of the right hemisphere (FFA, OFA, STS). Only adults exhibited activation in these same core face processing regions in the left hemisphere. Neither children nor adolescents exhibited the same patterns of activation in the extended regions of the face processing network (anterior temporal lobes and prefrontal regions).

Fig. 5

Results from an fMRI-adaptation study in which children, adolescents, and adults observed images of different and identical faces and houses. Only adults exhibited bilateral adaptation for faces and not houses in the individually defined fusiform face selective regions. Adolescents only exhibited this adult-like pattern in the left fusiform and children failed to exhibit significant face-selective adaptation in either the right or the left fusiform gryus. These findings indicate that even though this core face processing region is exhibiting some degree of functional maturity in adolescence, the nature of the representations being computed in these regions is still developing into adulthood.