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A phenotype of early infancy predicts reactivity of the amygdala in male adults

Molecular Psychiatry volume 17, pages 1042–1050 (2012)Cite this article

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Abstract

One of the central questions that has occupied those disciplines concerned with human development is the nature of continuities and discontinuities from birth to maturity. The amygdala has a central role in the processing of novelty and emotion in the brain. Although there is considerable variability among individuals in the reactivity of the amygdala to novel and emotional stimuli, the origin of these individual differences is not well understood. Four-month old infants called high reactive (HR) demonstrate a distinctive pattern of vigorous motor activity and crying to specific unfamiliar visual, auditory and olfactory stimuli in the laboratory. Low-reactive infants show the complementary pattern. Here, we demonstrate that the HR infant phenotype predicts greater amygdalar reactivity to novel faces almost two decades later in adults. A prediction of individual differences in brain function at maturity can be made on the basis of a single behavioral assessment made in the laboratory at 4 months of age. This is the earliest known human behavioral phenotype that predicts individual differences in patterns of neural activity at maturity. These temperamental differences rooted in infancy may be relevant to understanding individual differences in vulnerability and resilience to clinical psychiatric disorder. Males who were HR infants showed particularly high levels of reactivity to novel faces in the amygdala that distinguished them as adults from all other sex/temperament subgroups, suggesting that their amygdala is particularly prone to engagement by unfamiliar faces. These findings underline the importance of taking gender into account when studying the developmental neurobiology of human temperament and anxiety disorders. The genetic study of behavioral and biologic intermediate phenotypes (or ‘endophenotypes’) indexing anxiety-proneness offers an important alternative to examining phenotypes based on clinically defined disorder. As the HR phenotype is characterized by specific patterns of reactivity to elemental visual, olfactory and auditory stimuli, well before complex social behaviors such as shyness or fearful interaction with strangers can be observed, it may be closer to underlying neurobiological mechanisms than behavioral profiles observed later in life. This possibility, together with the fact that environmental factors have less time to impact the 4-month phenotype, suggests that this temperamental profile may be a fruitful target for high-risk genetic studies.

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Acknowledgements

We thank the families and children who have stayed with the study over 18 years. This study was supported by the National Institutes of Mental Health R01MH071467 and R01MH074848 (CES). This research was carried out in part at the Athinoula A Martinos Center for Biomedical Imaging at the Massachusetts General Hospital, using resources provided by the Center for Functional Neuroimaging Technologies, P41RR14075, a P41 Regional Resource supported by the Biomedical Technology Program of the National Center for Research Resources (NCRR), National Institutes of Health.

Author contributions: CES designed the study, directed data collection and analyses, conducted analyses, and wrote the paper. PSK conducted analyses. DNG wrote analytic software and advised on its use. JK and NCS characterized the temperament of the subjects at 4 months of age. RBB served as a study coordinator and collected MRI data.

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Authors and Affiliations

  1. Department of Psychiatry, Developmental Neuroimaging and Psychopathology Laboratory, Massachusetts General Hospital, Boston, MA, USA

    C E Schwartz, P S Kunwar & R B Bloch

  2. Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, USA

    C E Schwartz, P S Kunwar & D N Greve

  3. Department of Psychiatry, Harvard Medical School, Boston, MA, USA

    C E Schwartz & D N Greve

  4. Department of Radiology, Massachusetts General Hospital, Boston, MA, USA

    D N Greve

  5. Department of Psychology, Harvard University, Cambridge, MA, USA

    J Kagan

  6. Child Development Unit, Children's Hospital, Boston, MA, USA

    N C Snidman

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Schwartz, C., Kunwar, P., Greve, D. et al. A phenotype of early infancy predicts reactivity of the amygdala in male adults. Mol Psychiatry 17, 1042–1050 (2012). https://doi.org/10.1038/mp.2011.96

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