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Individual differences in sensitivity to the early environment as a function of amygdala and hippocampus volumes: An exploratory analysis in 12-year-old boys

Published online by Cambridge University Press:  21 December 2020

Michael Pluess*
Affiliation:
Department of Biological and Experimental Psychology, Queen Mary University of London, London, UK
Stephane A. De Brito
Affiliation:
School of Psychology, University of Birmingham, Edgbaston, UK
Alice Jones Bartoli
Affiliation:
Department of Psychology, Goldsmiths University of London, London, UK
Eamon McCrory
Affiliation:
Psychology and Language Sciences, University College London, London, UK
Essi Viding
Affiliation:
Psychology and Language Sciences, University College London, London, UK
*
Author for Correspondence: Michael Pluess, Department of Biological and Experimental Psychology, Queen Mary University of London, Mile End Road, LondonE1 4NS, UK; E-mail: [email protected]

Abstract

Children differ in their response to environmental exposures, with some being more sensitive to contextual factors than others. According to theory, such variability is the result of individual differences in neurobiological sensitivity to environmental features, with some individuals generally more affected by both negative and/or positive experiences. In this exploratory study we tested whether left and right amygdala and hippocampus volumes (corrected for total brain size) account for individual differences in response to environmental influences in a sample of 62 boys. Cumulative general environmental quality, ranging from low to high, was measured across the first 9 years and child behavior was reported by teachers when boys were 12–13 years old. According to analyses, only the left amygdala volume – not any of the other brain volumes – emerged as an important brain region for sensitivity to positive environmental aspects. Boys with a larger left amygdala benefited significantly more from higher environmental quality than boys with a smaller left amygdala whilst not being more vulnerable to lower quality. Besides providing preliminary evidence for differences in environmental sensitivity due to brain structure, the results also point to the left amygdala as having a specific role regarding the response to environmental influences.

Type
Regular Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Acevedo, B. P., Aron, E. N., Aron, A., Sangster, M. D., Collins, N., & Brown, L. L. (2014). The highly sensitive brain: An fMRI study of sensory processing sensitivity and response to others’ emotions. Brain and Behavior, 4, 580594.CrossRefGoogle ScholarPubMed
Aron, E. N., & Aron, A. (1997). Sensory-processing sensitivity and its relation to introversion and emotionality. Journal of Personality and Social Psychology, 73, 345368. doi:10.1037/0022-3514.73.2.345CrossRefGoogle ScholarPubMed
Aron, E. N., Aron, A., & Jagiellowicz, J. (2012). Sensory processing sensitivity: A review in the light of the evolution of biological responsivity. Personality and Social Psychology Review, 16, 262282. doi:10.1177/1088868311434213CrossRefGoogle ScholarPubMed
Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage, 38, 95113.CrossRefGoogle ScholarPubMed
Barros-Loscertales, A., Meseguer, V., Sanjuan, A., Belloch, V., Parcet, M., Torrubia, R., & Avila, C. (2006). Behavioral inhibition system activity is associated with increased amygdala and hippocampal gray matter volume: A voxel-based morphometry study. Neuroimage, 33, 10111015.CrossRefGoogle ScholarPubMed
Bateson, P., Barker, D., Clutton-Brock, T., Deb, D., D'Udine, B., Foley, R. A., … Sultan, S. E. (2004). Developmental plasticity and human health. Nature, 430, 419421.CrossRefGoogle ScholarPubMed
Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., & Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746754. doi:10.1038/mp.2009.44CrossRefGoogle ScholarPubMed
Belsky, J., & Pluess, M. (2009a). The nature (and nurture?) of plasticity in early human development. Perspectives on Psychological Science, 4, 345351.CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2009b). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908. doi:10.1037/a0017376CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2011). Beyond adversity, vulnerability and resilience: Individual differences in developmental plasticity. In Cicchetti, D. & Roisman, G. I. (Eds.), Minnesota symposium on child psychology, Vol. 36: The origins and organization of adaptation and maladaptation (pp. 379422). Hoboken, NJ: Wiley.Google Scholar
Belsky, J., & Pluess, M. (2013). Beyond risk, resilience, and dysregulation: Phenotypic plasticity and human development. Development and Psychopathology, 25, 12431261. doi:10.1017/S095457941300059XCrossRefGoogle ScholarPubMed
Belsky, J., & Pluess, M. (2016). Differential susceptibility to environmental influences. In Cicchetti, D. (Ed.), Developmental psychopathology (3rd ed., Vol. 3, pp. 59). New York, NY: Wiley.Google Scholar
Bickart, K. C., Wright, C. I., Dautoff, R. J., Dickerson, B. C., & Barrett, L. F. (2011). Amygdala volume and social network size in humans. Nature Neuroscience, 14, 163164. doi:10.1038/nn.2724CrossRefGoogle ScholarPubMed
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271301. doi:10.1017/s0954579405050145CrossRefGoogle ScholarPubMed
Brett, M., Anton, J. L., Valabregue, R., & Poline, J. B. (2002). Region of interest analysis using an SPM toolbox. In 8th international conference on functional mapping of the human brain (Vol. 16, pp. 497).Google Scholar
Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012). Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences of the United States of America, 109, E1312E1319.Google ScholarPubMed
Cunningham, W. A., Arbuckle, N. L., Jahn, A., Mowrer, S. M., & Abduljalil, A. M. (2010). Aspects of neuroticism and the amygdala: Chronic tuning from motivational styles. Neuropsychologia, 48, 33993404. doi:10.1016/j.neuropsychologia.2010.06.026CrossRefGoogle ScholarPubMed
Dunbar, R. I. (2012). The social brain meets neuroimaging. Trends in Cognitive Sciences, 16, 101102. doi:10.1016/j.tics.2011.11.013CrossRefGoogle ScholarPubMed
Elliott, M. L., Knodt, A. R., Ireland, D., Morris, M. L., Poulton, R., Ramrakha, S., … Hariri, A. R. (2020). What is the test-retest reliability of common task-functional MRI measures? New empirical evidence and a meta-analysis. Psychological Science, 31, 792806. doi:10.1177/0956797620916786CrossRefGoogle ScholarPubMed
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & Van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 728. doi:10.1017/S0954579410000611CrossRefGoogle Scholar
Evans, G. W., Swain, J. E., King, A. P., Wang, X., Javanbakht, A., Ho, S. S., … Liberzon, I. (2016). Childhood cumulative risk exposure and adult amygdala volume and function. Journal of Neuroscience Research, 94, 535543. doi:10.1002/jnr.23681CrossRefGoogle ScholarPubMed
Gard, A. M., Shaw, D. S., Forbes, E. E., & Hyde, L. W. (2018). Amygdala reactivity as a marker of differential susceptibility to socioeconomic resources during early adulthood. Developmental Psychology, 54, 23412355. doi:10.1037/dev0000600CrossRefGoogle ScholarPubMed
Goodman, R. (1997). The strengths and difficulties questionnaire: A research note. The Journal of Child Psychology and Psychiatry, 38, 581586.CrossRefGoogle ScholarPubMed
Hariri, A. R., Mattay, V. S., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., … Weinberger, D. R. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science, 297, 400403.CrossRefGoogle ScholarPubMed
Hartman, S., Freeman, S. M., Bales, K. L., & Belsky, J. (2018). Prenatal stress as a risk—and an opportunity—factor. Psychological Science, 29, 572580.CrossRefGoogle ScholarPubMed
Haworth, C. M., Davis, O. S., & Plomin, R. (2013). Twins Early Development Study (TEDS): A genetically sensitive investigation of cognitive and behavioral development from childhood to young adulthood. Twin Research and Human Genetics, 16, 117125.CrossRefGoogle ScholarPubMed
Hill, S. Y., Tessner, K., Wang, S., Carter, H., & McDermott, M. (2010). Temperament at 5 years of age predicts amygdala and orbitofrontal volume in the right hemisphere in adolescence. Psychiatry Research: Neuroimaging, 182, 1421.CrossRefGoogle ScholarPubMed
Holmes, A. J., Lee, P. H., Hollinshead, M. O., Bakst, L., Roffman, J. L., Smoller, J. W., & Buckner, R. L. (2012). Individual differences in amygdala-medial prefrontal anatomy link negative affect, impaired social functioning, and polygenic depression risk. Journal of Neuroscience, 32, 1808718100.CrossRefGoogle ScholarPubMed
Keers, R., Coleman, J. R., Lester, K. J., Roberts, S., Breen, G., Thastum, M., … Meiser-Stedman, R. (2016). A genome-wide test of the differential susceptibility hypothesis reveals a genetic predictor of differential response to psychological treatments for child anxiety disorders. Psychotherapy and Psychosomatics, 85, 146158.CrossRefGoogle ScholarPubMed
Kovas, Y., Haworth, C. M., Dale, P. S., Plomin, R., Weinberg, R. A., Thomson, J. M., … Fischer, K. W. (2007). The genetic and environmental origins of learning abilities and disabilities in the early school years. Monographs of the Society for Research in Child Development, 72, vii, 1144. doi:10.1111/j.1540-5834.2007.00439.xGoogle ScholarPubMed
Lionetti, F., Aron, A., Aron, E. N., Burns, G. L., Jagiellowicz, J., & Pluess, M. (2018). Dandelions, tulips and orchids: Evidence for the existence of low-sensitive, medium-sensitive and high-sensitive individuals. Translational Psychiatry, 8, 24. doi:10.1038/s41398-017-0090-6CrossRefGoogle ScholarPubMed
Meyer-Lindenberg, A., Buckholtz, J. W., Kolachana, B., Hariri, A. R., Pezawas, L., Blasi, G., … Weinberger, D. R. (2006). Neural mechanisms of genetic risk for impulsivity and violence in humans. Proceedings of the National Academy of Sciences of the United States of America, 103, 62696274.CrossRefGoogle ScholarPubMed
Moore, S. R., & Depue, R. A. (2016). Neurobehavioral foundation of environmental reactivity. Psychological Bulletin, 142, 107164. doi:10.1037/bul0000028CrossRefGoogle ScholarPubMed
Munafo, M. R., Brown, S. M., & Hariri, A. R. (2008). Serotonin transporter (5-HTTLPR) genotype and amygdala activation: A meta-analysis. Biological Psychiatry, 63, 852857.CrossRefGoogle ScholarPubMed
Pluess, M. (2015). Individual differences in environmental sensitivity. Child Development Perspectives, 9, 138143. doi:10.1111/cdep.12120CrossRefGoogle Scholar
Pluess, M., Assary, E., Lionetti, F., Lester, K. J., Krapohl, E., Aron, E. N., & Aron, A. (2018). Environmental sensitivity in children: Development of the Highly Sensitive Child Scale and identification of sensitivity groups. Developmental Psychology, 54, 5170. doi:10.1037/dev0000406CrossRefGoogle ScholarPubMed
Pluess, M., & Belsky, J. (2011). Prenatal programming of postnatal plasticity? Development and Psychopathology, 23, 2938. doi:10.1017/S0954579410000623CrossRefGoogle ScholarPubMed
Pluess, M., & Belsky, J. (2013). Vantage sensitivity: Individual differences in response to positive experiences. Psychological Bulletin, 139, 901916. doi:10.1037/a0030196CrossRefGoogle ScholarPubMed
Pluess, M., Stevens, S., & Belsky, J. (2013). Differential susceptibility: developmental and evolutionary mechanisms of gene-environment interactions. In Legerstee, M., Haley, D. W. & Bornstein, M. H. (Eds.), The infant mind: Origins of the social brain (pp. 7796). New York, NY: Guilford Press.Google Scholar
Preacher, K. J., Curran, P. J., & Bauer, D. J. (2006). Computational tools for probing interactions in multiple linear regressions, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31, 437448.CrossRefGoogle Scholar
Rasch, B., Spalek, K., Buholzer, S., Luechinger, R., Boesiger, P., de Quervain, D. J., & Papassotiropoulos, A. (2010). Aversive stimuli lead to differential amygdala activation and connectivity patterns depending on catechol-O-methyltransferase Val158Met genotype. Neuroimage, 52, 17121719. doi:10.1016/j.neuroimage.2010.05.054CrossRefGoogle ScholarPubMed
Rijsdijk, F. V., Viding, E., De Brito, S., Forgiarini, M., Mechelli, A., Jones, A. P., & McCrory, E. (2010). Heritable variations in gray matter concentration as a potential endophenotype for psychopathic traits. Archives of General Psychiatry, 67, 406413.CrossRefGoogle ScholarPubMed
Roisman, G. I., Newman, D. A., Fraley, R. C., Haltigan, J. D., Groh, A. M., & Haydon, K. C. (2012). Distinguishing differential susceptibility from diathesis-stress: Recommendations for evaluating interaction effects. Development and Psychopathology, 24, 389409. doi:10.1017/S0954579412000065CrossRefGoogle ScholarPubMed
Ruigrok, A. N., Salimi-Khorshidi, G., Lai, M. C., Baron-Cohen, S., Lombardo, M. V., Tait, R. J., & Suckling, J. (2014). A meta-analysis of sex differences in human brain structure. Neuroscience and Biobehavioral Reviews, 39, 3450. doi:10.1016/j.neubiorev.2013.12.004CrossRefGoogle ScholarPubMed
Schriber, R. A., Anbari, Z., Robins, R. W., Conger, R. D., Hastings, P. D., & Guyer, A. E. (2017). Hippocampal volume as an amplifier of the effect of social context on adolescent depression. Clinical Psychological Science, 5, 632649. doi:10.1177/2167702617699277CrossRefGoogle ScholarPubMed
Schwartz, C. E., Kunwar, P. S., Greve, D. N., Kagan, J., Snidman, N. C., & Bloch, R. B. (2012). A phenotype of early infancy predicts reactivity of the amygdala in male adults. Molecular Psychiatry, 17, 10421050. doi:10.1038/mp.2011.96CrossRefGoogle ScholarPubMed
Schwartz, C. E., Wright, C. I., Shin, L. M., Kagan, J., & Rauch, S. L. (2003). Inhibited and uninhibited infants “grown up”: Adult amygdalar response to novelty. Science, 300, 19521953. doi:10.1126/science.1083703CrossRefGoogle ScholarPubMed
Sergerie, K., Chochol, C., & Armony, J. L. (2008). The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 32, 811830.CrossRefGoogle ScholarPubMed
Slagt, M., Dubas, J. S., Dekovic, M., & van Aken, M. A. (2016). Differences in sensitivity to parenting depending on child temperament: A meta-analysis. Psychological Bulletin. doi:10.1037/bul0000061CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, NJoliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273289.CrossRefGoogle ScholarPubMed
Whittle, S., Yap, M. B. H., Sheeber, L., Dudgeon, P., Yuecel, M., Pantelis, C., … Allen, N. B. (2011). Hippocampal volume and sensitivity to maternal aggressive behavior: A prospective study of adolescent depressive symptoms. Development and Psychopathology, 23, 115129. doi:10.1017/s0954579410000684CrossRefGoogle ScholarPubMed
Whitwell, J. L. (2009). Voxel-based morphometry: An automated technique for assessing structural changes in the brain. Journal of Neuroscience, 29, 96619664. doi:10.1523/jneurosci.2160-09.2009CrossRefGoogle Scholar
Wilke, M., Holland, S. K., Altaye, M., & Gaser, C.. (2008). Template-O-Matic: A toolbox for creating customized pediatric templates. NeuroImage, 41(3), 903913. doi:10.1016/j.neuroimage.2008.02.056.CrossRefGoogle ScholarPubMed
Wolf, M., van Doorn, G. S., & Weissing, F. J. (2008). Evolutionary emergence of responsive and unresponsive personalities. Proceedings of the National Academy of Sciences of the United States of America, 105, 1582515830. doi:10.1073/pnas.0805473105CrossRefGoogle ScholarPubMed
Yap, M. B., Whittle, S., Yucel, M., Sheeber, L., Pantelis, C., Simmons, J. G., & Allen, N. B. (2008). Interaction of parenting experiences and brain structure in the prediction of depressive symptoms in adolescents. Archives of General Psychiatry, 65, 13771385. doi:10.1001/archpsyc.65.12.1377CrossRefGoogle ScholarPubMed
Zuckerman, M. (1999). Vulnerability to psychopathology: A biosocial model. Washington, DC: American Psychological Association.CrossRefGoogle Scholar
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