Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years
Corresponding Author
Jay N. Giedd
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Child Psychiatry Branch, National Institute of Mental Health, Building 10, Room 6N240, 10 Center Drive MSC 1600, Bethesda, MD 20892-1600Search for more papers by this authorA. Catherine Vaituzis
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorSusan D. Hamburger
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorNicholas Lange
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorJagath C. Rajapakse
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorDebra Kaysen
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorYolanda C. Vauss
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorJudith L. Rapoport
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorCorresponding Author
Jay N. Giedd
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Child Psychiatry Branch, National Institute of Mental Health, Building 10, Room 6N240, 10 Center Drive MSC 1600, Bethesda, MD 20892-1600Search for more papers by this authorA. Catherine Vaituzis
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorSusan D. Hamburger
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorNicholas Lange
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorJagath C. Rajapakse
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorDebra Kaysen
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorYolanda C. Vauss
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorJudith L. Rapoport
Child Psychiatry Branch, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
Search for more papers by this authorAbstract
The volume of the temporal lobe, superior temporal gyrus, amygdala, and hippocampus was quantified from magnetic images of the brains of 99 healthy children and adolescents aged 4–18 years. Variability in volume was high for all structures examined. When adjusted for a 9% larger total cerebral volume in males, there were no significant volume differences between sexes. However, sex-specific maturational changes were noted in the volumes of medial temporal structures, with the left amygdala increasing significantly only in males and with the right hippocampus increasing significantly only in females. Right-greater-than-left laterality effects were found for temporal lobe, superior temporal gyrus, amygdala, and hippocampal volumes. These results are consistent with previous preclinical and human studies that have indicated hormonal responsivity of these structures and extend quantitative morphologic findings from the adult literature. In addition to highlighting the need for large samples and sex-matched controls in pediatric neuroimaging studies, the information from this understudied age group may be of use in evaluating developmental hypotheses of neuropsychiatric disorders. © 1996 Wiley-Liss, Inc.
Literature Cited
- Achenbach, T. M., and C. S. Edelbrock (1983) Manual for Child Behavior Checklist and Revised Behavior Profile. Burlington, VT: Department of Psychiatry, University of Vermont.
- Amaral, D. G., J. L. Price, A. Pitkanen, and S. T. Carmichael (1992) Anatomical organization of the primate amygdaloid complex. In J. P. Aggleton (ed.): The Amygdala. New York: Wiley-Liss, Inc., pp. 1–67.
- Bachevalier, J. (1994) Medial temporal lobe structures and autism: A review of clinical and experimental findings. Neuropsychologia 32: 627–648.
- Benes, F. M., M. Turtle, Y. Khan, and P. Farol (1994) Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch. Gen. Psychiatr. 51: 477–484.
- Bergin, P. S., A. A. Raymond, S. L. Free, S. M. Sisodiya, and J. M. Stevens (1994) Magnetic resonance volumetry, Neurology 44: 1770–1771.
- Bilder, R. M., H. Wu, B. Bogerts, G. Degreef, M. Ashtari, J. M. Alvir, P. J. Snyder, and J. A. Lieberman (1994) Absence of regional hemispheric volume asymmetries in first-episode schizophrenia. Am. J. Psychiatr. 151: 1437–1447.
- Bogerts, B., J. A. Lieberman, M. Ashtari, R. M. Bilder, G. Degreef, G. Lerner, C. Johns, and S. Masiar (1993) Hippocampus-amygdala volumes and psychopathology in chronic schizophrenia. Biol. Psychiatr. 33: 236–246.
- Buchsbaum, M. S., C. S. Mansour, D. G. Teng, A. D. Zia, B. V. Siegel Jr., and D. M. Rice (1992) Adolescent developmental change in topography of EEG amplitude. Schizophrenia Res. 7: 101–107.
- Clark, A. S., N. J. MacLusky, and P. S. Goldman-Rakic (1988) Androgen binding and metabolism in the cerebral cortex of the developing rhesus monkey. Endocrinology 123: 932–940.
- Coffey, C. E., W. E. Wilkinson, I. A. Parashos, S. A. R. Soady, R. J. Sullivan, L. J. Patterson, G. S. Figiel, M. C. Webb, C. E. Spritzer and W. T. Djang (1992) Quantitative cerebral anatomy of the aging brain: A cross sectional study using magnetic resonance imaging. Neurology 42: 527–536.
- Conners, C. K. (1973) Rating scales in drug studies with children. Psychophar macol. Bull., Special issue, Psychopharmacotherapy in Children, 9: 24–28.
- Cook, M. J., D. R. Fish, S. D. Shorvon, K. Straughan, and J. M. Stevens (1992) Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy. Brain 115: 1001–1015.
- Cowell, P. E., B. I. Turetsky, R. C. Gur, R. I. Grossman, D. L. Shtasel, and R. E. Gur (1994) Sex differences in aging of the human frontal and temporal lobes. J. Neurosci. 14: 4748–4755.
- Denckla, M. B. (1985) Revised physical and neurological examination for subtle signs. Psychopharmacol. Bull. 21: 773–800.
- Diamond, M. C., D. Krech, and M. R. Rosenzweig (1964) The effects of an enriched environment on the histology of the rat cerebral cortex. J. Comp. Neurol. 123: 111–120.
- Diener, E., E. Sandvik, and R. F. Larsen (1985) Age and sex effects for affect intensity. Dev. Psychol. 21: 542–546.
- Filipek, P. A., C. Richelme, D. N. Kennedy Jr., and V. S. Caviness (1994) The young adult human brain: An MRI-based morphometric analysis. Cereb. Cortex 4: 344–360.
- Flaum, M., V. W. Swayze, D. S. O'Leary, W. T. C. Yuh J. C. Ehrhardt, S. V. Arndt, and N. C. Andreasen (1996) Brain morphology in schizophrenia: Effects of diagnosis, laterality and gender. Am. J. Psychiatr. (in press).
- Giedd, J. N., J. W. Snell, N. Lange, J. C. Rajapakse, D. Kaysen, A. C. Vaituzis, Y. C. Vauss, S. D. Hamburger, P. L. Kozuch, and J. L. Rapoport (1996) Quantitative magnetic resonance imaging of human brain development: Ages 4–18. Cereb. Cortex (in press).
- Goldberg, T. E., E. F. Torrey, K. F. Berman, and D. R. Weinberger (1994) Relations between neuropsychological performance and brain morphological and physiological measures in monozygotic twins discordant for schizophrenia. Psychiatr. Res. 55: 51–61.
- Gould, E., C. S. Woolley, M. Frankfurt, and B. S. McEwen (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10: 1286–1291.
- Gould, E., C. S. Woolley, and B. S. McEwen (1991) The hippocampal formation: Morphological changes induced by thyroid, gonadal and adrenal hormones. Psychoneuroendocrinology 16: 67–84.
- Goyette, C. H., C. K. Conners, and R. F. Ulrich (1978) Normative data on the Revised Conner's Parent and Teacher Rating Scales. J. Abnorm. Child Psychol. 6: 221–236.
- Hastie, T., and R. Tibshirani (1990) Generalized Additive Models. London: Chapman and Hall.
- Jacobs, L. F., S. J. Gaulin, D. F. Sherry, and G. E. Hoffman (1990) Evolution of spatial cognition: Sex-specific patterns of spatial behavior predict hippocampal size. Proc. Natl. Acad. Sci. USA 87: 6349–6352.
-
Jacobson, M.
(1991)
Developmental Neurobiology.
New York: Plenum Press.
10.1007/978-1-4757-4954-0 Google Scholar
- Jastak, S., and G. S. Wilkinson (1984) Wide Range Achievement Test, Revised Edition. Wilmington, DE: Jastak Assessment Systems.
- Jerslid, A. T. (1963) The Psychology of Adolescence. New York: Macmillan Publishing Company.
- Krebs, J. R., D. F. Sherry, S. D. Healy, V. H. Perry, and A. L. Vaccarino (1989) Hippocampal specialization of food-storing birds. Proc. Natl. Acad. Sci. USA 86: 1388–1392.
- Lencz, T., G. McCarthy, R. A. Bronen, T. M. Scott, J. A. Inserni, K. J. Sass, R. A. Novelly, J. H. Kim, and D. D. Spencer (1992) Quantitative magnetic resonance imaging in temporal lobe epilepsy: Relationship to neuropathology and neuropsychological function. Ann. Neurol. 31: 629–637.
- Miller, M. M., E. Antecka, and R. Sapolsky (1989) Short term effects of glucocorticoids upon hippocampal ultrastructure. Exp. Brain Res. 77: 309–314.
- Morse, J. K., S. W. Scheff, and S. T. de Kosky (1986) Gonadal steroids influence axonal sprouting in the hippocampal dentate gyrus: A sexually dimorphic response. Exp. Neurol. 94: 649–658.
- Murphy, D. G. M., C. de Carli, E. Daly, J. V. Haxby, G. Allen, B. J. White, C. Powell, B. Horowitz, S. I. Rapoport, and M. B. Shapiro (1993) Effects of the X chromosome on female brain: A study of turner syndrome using quantitative magnetic resonance imaging. Lancet 342: 1188–1199.
- Murphy, D. G. M., C. de Carli, A. R. McIntosh, E. Daly, J. Szczepanik, M. B. Schapiro, S. I. Rapoport, and B. Horwitz (1996) Sex differences in human brain morphometry: A quantitative in vivo magnetic resonance imaging study on the effect of aging. Arch. Gen. Psychiatry (in press).
- Nolte, J. (1993) Olfactory and limbic systems. In R. Farrell (ed.): The Human Brain. An Introduction to its Functional Anatomy. St. Louis: Mosby Year Book, Inc., pp. 397–413.
- Rasband, W. (1993) Image (1.6). Bethesda, MD: National Institutes of Health [public domain].
- Sapolsky, R. M. (1990) Glucocorticoids, hippocampal damage and the gluta matergic synapse. Progr. Brain Res. 86: 13–23.
- Sapolsky, R. M., L. C. Krey, and B. S. McEwen (1985) Prolonged glucocorti coid exposure reduces hippocampal neuron number: Implications for aging. J. Neurosci. 5: 1222–1227.
- SAS Institute (1990) SAS, Version 6. Cary, NC: SAS Institute, Inc.
- Shenton, M. E., R. Kikinis, F. A. Jolesz, S. D. Pollak, M. LeMay, C. G. Wible, H. Hokama, J. Martin, D. Metcalf, and M. Coleman (1992) Abnormalities of the left temporal lobe and thought disorder in schizqphrenia. A quantitative magnetic resonance imaging study. N. Engl. J. Med. 327: 604–612.
- Sherry, D. F., A. L. Vaccarino, K. Buckenham, and R. S. Herz (1989) The hippocampal complex of food-storing birds. Brain Behav. Evol. 34: 308–317.
- Sherry, D. F., L. F. Jacobs, and S. J. Gaulin (1992) Spatial memory and adaptive specialization of the hippocampus [see comments]. Trends Neurosci. 15: 298–303.
- Sholl, S. A., and K. L. Kim (1989) Estrogen receptors in the rhesus monkey brain during fetal development. Dev. Brain Res. 50: 189–196.
- Snell, J. W., M. B. Merickel, J. M. Ortega, J. C. Goble, J. R. Brookeman, and N. F. Kassell (1996) Boundary estimation of complex objects using hierarchical active surface templates. J. Pattern Recogn. (in press).
- Swayze V. W. II, N. C. Andreasen, R. J. Alliger, W. T. Yuh, and J. C. Ehrhardt (1992) Subcortical and temporal structures in affective disorder and schizophrenia: A magnetic resonance imaging study [see comments]. Biol. Psychiatr. 31: 221–240.
- Wechsler, D. (1974) Wechsler Intelligence Scale for Children-Revised. New York: The Psychological Corporation.
- Weschler, D. (1981) Wechsler Adult Intelligence Scale-Revised. New York: The Psychological Corporation.
- Weinberger, D. R. (1994) Schizophrenia as a neurodevelopmental disorder: A review of the concept. In S. R. Hirsch and D. R. Weinberger (eds.): Schizophrenia. London: Blackwood Press, pp. 1–74.
- Welner, Z., W. Reich, B. Herjanic, K. Jung, and H. Amado (1987) Reliability, validity and child agreement studies of the diagnostic interview of children and adolescents (DICA). J. Am. Acad. Child Adolesc. Psychiatr. 26: 649–653.
- Woodcock, R. W., and B. B. Johnson (1977) Woodcock-Johnson Psychoeducational Battery. Allen, TX: DLM Teaching Resources.
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