Effects of sex and age on regional prefrontal brain volume in two human cohorts

European Journal of Neuroscience

Volumn 25, Issue 1, 2007, Pages 307-318

  Cowell, Patricia E ^a   Sluming, Vanessa A ^c   Wilkinson, Iain D ^b   Cezayirli, Enis ^c,e   Romanowski, Charles A J ^b   Webb, Jocasta A ^c   Keller, Simon S ^c   Mayes, Andrew ^d   Roberts, Neil ^c  

^a Department of Human Communication Sciences ^*  (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e CELAL BAYAR UNIVERSITY   (Turkey)

Author keywords

Cavalieri method; Cerebral cortex; Healthy adults; MRI; Stereology

Indexed keywords

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; BRAIN REGION; BRAIN SIZE; COHORT ANALYSIS; FEMALE; HEMISPHERE; HUMAN; IMAGE QUALITY; LIFESPAN; MALE; NEUROANATOMY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; REPRODUCIBILITY; SEX DIFFERENCE;

ADULT; AGE FACTORS; AGED; AGING; BRAIN MAPPING; COHORT STUDIES; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PREFRONTAL CORTEX; SEX CHARACTERISTICS; SEX FACTORS;

EID: 33846211807     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05281.x     Document Type: Article

References (71)

1. Bechara, A., Tranel, D. & Damasio, H. (2000) Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain, 123, 2189-2202.
2. Berman, K.F., Schmidt, P.J., Rubinow, D.R., Danaceau, M.A., Van Horn, J.D., Esposito, G., Ostrem, J.L. & Weinberger, D.R. (1997) Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proc. Natl Acad. Sci. USA, 94, 8836-8841.
3. Bixo, M., Backstrom, T., Winblad, B. & Andersson, A. (1995) Estradiol and testosterone in specific regions of the human female brain in different endocrine states. J. Steroid Biochem. Mol. Biol., 55, 297-303.
4. Bland, J. & Altman, D. (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet, 327, 307-310.
5. Bolla, K.I., Eldreth, D.A., Matochik, J.A. & Cadet, J.L. (2004) Sex-related differences in a gambling task and its neurological correlates. Cereb. Cortex, 14, 1226-1232.
6. Boucher, J., Cowell, P., Howard, M., Broks, P., Farrant, A., Roberts, N. & Mayes, A. (2005) A combined clinical, neuropsychological, and neuroanatomical study of adults with high functioning autism. Cognitive Neuropsychiatry, 10, 165-213.
7. Buckner, R.L., Head, D., Parker, J., Fotenos, A.F., Marcus, D., Morris, J.C. & Snyder, A.Z. (2004) A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage, 23, 724-738.
8. Clarke, A. & Goldman-Rakic, P. (1989) Gonadal hormones influence the emergence of cortical function in nonhuman primates. Behav. Neurosci., 103, 1287-1295.
9. Coffey, E., Lucke, J., Saxton, J., Ratcliffe, G., Unitas, L.J., Billig, B. & Bryan, N. (1998) Sex differences in brain aging. Arch. Neurol., 55, 169-179.
10. Cole, T.J. (2000) Secular trends in growth. Proc. Nutr. Soc., 59, 317-324.
11. Convit, A., Wolf, O.T., de Leon, M.J., Patalinjug, M., Kandil, E., Caraos, C., Scherer, A., Saint Louis, L.A. & Cancro, R. (2001) Volumetric analysis of the pre-frontal regions: findings in aging and schizophrenia. Psychiatry Res., 107, 61-73.
12. Cowell, P.E. (2003) Size differences in the corpus callosum: analysis beyond the main effects. In Zaidel, E. & Iacoboni, M. (eds), The Parallel Brain. The Cognitive Neuroscience of the Corpus Callosum. MIT Press, Cambridge, MA, pp. 64-69.
13. Cowell, P.E., Allen, L.S., Zalatimo, N.S. & Denenberg, V.H. (1992) A developmental study of sex and age interactions in the human corpus callosum. Brain Res. Dev. Brain Res., 66, 187-192.
14. Cowell, P. & Denenberg, V. (2002) Development of laterality and the role of the corpus callosum in rodents and humans. In Rogers, L. & Andrew, R. (eds), Comparative Vertebrate Laterality. Cambridge University Press, Cambridge, pp. 274-305.
15. Cowell, P.E., Turetsky, B.I., Gur, R.C., Grossman, R.I., Shtasel, D.L. & Gur, R.E. (1994) Sex differences in aging of the human frontal and temporal lobes. J. Neurosci., 14, 4748-4755.
16. Cruz-Orive, L. (1999) Precision of Cavalieri sections and slices with local errors. J. Microscopy, 193, 182-198.
17. Duncan, J., Burgess, P. & Emslie, H. (1995) Fluid intelligence after frontal lobe lesions. Neuropsychologia, 33, 261-268.
18. Eberling, J.L., Wu, C., Tong-Turnbeaugh, R. & Jagust, W.J. (2004) Estrogen-and tamoxifen-associated effects on brain structure and function. Neuroimage, 21, 364-371.
19. Fernandez, G., Weis, S., Stoffel-Wagner, B., Tendolkar, I., Reuber, M., Beyenburg, S., Klaver, P., Fell, J., de Greiff, A., Ruhlmann, J., Reul, J. & Elger, C.E. (2003) Menstrual cycle-dependent neural plasticity in the adult human brain is hormone, task, and region specific. J. Neurosci., 23, 3790-3795.
20. García-Fiñana, M., Cruz-Orive, L.M., Mackay, C.E., Pakkenberg, B. & Roberts, N. (2003) Comparison of MR imaging against physical sectioning to estimate the volume of human cerebral compartments. Neuroimage, 18, 505-516.
21. Goldman, P., Crawford, H., Stokes, L., Galkin, T. & Rosvold, E. (1974) Sex-dependent behavioural effects of cerebral cortical lesions in the developing rhesus monkey. Science, 186, 540-542.
22. Gong, Q.-Y., Sluming, V., Mayes, A., Keller, S., Barrick, T., Cezayirli, E. & Roberts, N. (2005) Voxel-based morphometry and stereology provide convergent evidence for the importance of medial prefrontal cortex for fluid intelligence in healthy adults. Neuroimage, 25, 1175-1186.
23. Good, C., Johnsrude, I., Ashburner, J., Henson, R., Friston, K. & Frackowiak, R. (2001) Avoxel based morphometric study of aging in 465 normal adult human brains. Neuroimage, 14, 21-36.
24. Gron, G., Wunderlich, A.P., Spitzer, M., Tomczak, R. & Riepe, M.W. (2000) Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat. Neurosci., 3, 404-408.
25. Gur, R.E., Cowell, P.E., Latshaw, A., Turetsky, B.I., Grossman, R.I., Arnold, S.E., Bilker, W.B. & Gur, R.C. (2000) Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. Arch. Gen. Psychiatry, 57, 761-768.
26. Gur, R.C., Gunning-Dixon, F., Bilker, W.B. & Gur, R.E. (2002) Sex differences in temporo-limbic and frontal brain volumes of healthy adults. Cereb. Cortex, 12, 998-1003.
27. Gusnard, D.A., Akbudak, E., Shulman, G.L. & Raichle, M.E. (2001) Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc. Natl Acad. Sci. USA, 98, 4259-4264.
28. Harasty, J., Double, K., Halliday, G., Kril, J. & McRitchie, D. (1997) Language associated cortical regions are proportionally larger in the female brain. Arch. Neurol., 54, 171-176.
29. Henderson, V.W. (1997) Estrogen, cognition, and a woman's risk of Alzheimer's disease. Am. J. Med., 103, 11S-18S.
30. Howard, M.A., Roberts, N., García-Fiñana, M. & Cowell, P.E. (2003) volume estimation of prefrontal cortical subfields using MRI and stereology. Brain Res. Protoc., 10, 125-138.
31. Jäncke, L. & Steinmetz, H. (2003) Brain size: a possible source of interindividual variability in corpus callosum morphology. In Zaidel, E. & Iacoboni, M. (eds), The Parallel Brain: the Cognitive Neuroscience of the Corpus Callosum. MIT Press, Cambridge, MA, pp. 51-63.
32. Jernigan, T.L., Trauner, D.A., Hesselink, J.R. & Tallal, P.A. (1991) Maturation of human cerebrum observed in vivo during adolescence. Brain, 114, 2037-2049.
33. Johnson, M.K., Mitchell, K.J., Raye, C.L. & Greene, E.J. (2004) An age-related deficit in prefrontal cortical function associated with refreshing information. Psychol. Sci., 15, 127-132.
34. Keenan, P.A., Ezzat, W.H., Ginsburg, K. & Moore, G.J. (2001) Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology, 26, 577-590.
35. Kleinbaum, D.G. & Kupper, L.L. (1978) Applied Regression Analysis and Other Multivariable Methods. Duxbury Press, Boston, USA.
36. Klingberg, T., Vaidya, C.J., Gabrieli, J.D., Moseley, M.E. & Hedehus, M. (1999) Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. Neuroreport, 10, 2817-2821.
37. Kohn, M., Tanna, N., Herman, G., Resnick, S., Mozley, D., Gur, R., Alavi, A., Zimmerman, R. & Gur, R. (1991) Analysis of brain and cerebrospinal fluid volumes with MR imaging. Radiology, 178, 115-122.
38. Lamar, M. & Resnick, S.M. (2004) Aging and prefrontal functions: dissociating orbitofrontal and dorsolateral abilities. Neurobiol. Aging, 25, 553-558.
39. Lemaitre, H., Crivello, F., Grassiot, B., Alperovitch, A., Tzourio, C. & Mazoyer, B. (2005) Age- and sex-related effects on the neuroanatomy of healthy elderly. Neuroimage, 26, 900-911.
40. Liu, R.S., Lemieux, L., Bell, G.S., Sisodiya, S.M., Shorvon, S.D., Sander, J.W. & Duncan, J.S. (2003) A longitudinal study of brain morphometrics using quantitative magnetic resonance imaging and difference image analysis. Neuroimage, 20, 22-33.
41. Luciana, M. (2003) The neural and functional development of human prefrontal cortex. In deHaan, M. & Johnson, M.K. (eds), The Cognitive Neuroscience of Development. Psychology Press, Hove, pp. 157-179.
42. Luine, V.N., Richards, S.T., Wu, V.Y. & Beck, K.D. (1998) Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm. Behav., 34, 149-162.
43. Mackay, C., Roberts, N., Mayes, A., Downes, J., Foster, J. & Mann, D. (1998) An exploratory study of the relationship between face recognition memory and the volume of medial temporal lobe structures in healthy young males. Behav. Neurol., 11, 3-20.
44. Murphy, D., deCarli, C., McIntosh, A., Daly, E., Mentis, M., Pietrini, P., Szczepanik, J., Schapiro, M., Grady, C., Horwitz, B. & Rapoport, S. (1996) Sex differences in human brain morphometry and metabolism: an in-vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging. Arch. Gen. Psychiatry, 53, 585-594.
45. Northoff, G. & Bermpohl, F. (2004) Cortical midline structures and the self. Trends Cogn. Sci., 8, 102-107.
46. Overman, W.H. (2004) Sex differences in early childhood, adolescence, and adulthood on cognitive tasks that rely on orbital prefrontal cortex. Brain Cogn., 55, 134-147.
47. Phillips, L.H. & Della Sala, S. (1998) Aging, intelligence, and anatomical segregation in the frontal lobes. Learn. Individ. Differ., 10, 217-243.
48. Rajah, M.N. & D'Esposito, M. (2005) Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. Brain, 128, 1964-1983.
49. Raz, N., Gunning, F., Head, D., Dupuis, J., McQuain, J., Briggs, S., Loken, W., Thornton, A. & Acker, J. (1997) Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb. Cortex, 7, 268-282.
50. Raz, N., Gunning-Dixon, F., Head, D., Rodrigue, K.M., Williamson, A. & Acker, J.D. (2004) Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol. Aging, 25, 377-396.
51. Raz, N., Lindenberger, U., Rodrigue, K.M., Kennedy, K.M., Head, D., Williamson, A., Dahle, C., Gerstorf, D. & Acker, J.D. (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex, 15, 1676-1689.
52. Resnick, S., Goldszal, A., Davatzikos, C., Golski, S., Kraur, M., Metter, J., Bryan, N. & Zonderman, A. (2000) One year age changes in MRI brain volumes in older adults. Cereb. Cortex, 10, 464-472.
53. Roberts, N., Garden, A., Cruz-Orive, L., Whitehouse, G. & Edwards, R. (1994) Estimation of fetal volume by magnetic resonance imaging and stereology. Br. J. Radiol., 67, 1067-1077.
54. Roberts, N., Puddephat, M. & McNulty, V. (2000) The benefit of stereology for quantitative radiology. Br. J. Radiol., 73, 679-697.
55. Salat, D.H., Buckner, R.L., Snyder, A.Z., Greve, D.N., Desikan, R.S., Busa, E., Morris, J.C., Dale, A.M. & Fischl, B. (2004) Thinning of the cerebral cortex in aging. Cereb. Cortex, 14, 721-730.
56. Salat, D.H., Kaye, J.A. & Janowsky, J.S. (2001) Selective preservation and degeneration within the prefrontal cortex in aging and Alzheimer disease. Arch. Neurol., 58, 1403-1408.
57. Scahill, R.I., Frost, C., Jenkins, R., Whitwell, J.L., Rossor, M.N. & Fox, N.C. (2003) A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Arch. Neurol., 60, 989-994.
58. Schnack, H.G., van Haren, N.E., Hulshoff Pol, H.E., Picchioni, M., Weisbrod, M., Sauer, H., Cannon, T., Huttunen, M., Murray, R. & Kahn, R.S. (2004) Reliability of brain volumes from multicenter MRI acquisition: a calibration study. Hum. Brain Mapp., 22, 312-320.
59. Shrout, P. & Fleiss, J. (1979) Intraclass correlations: uses in assessing rater reliability. Psychol. Bull., 86, 420-428.
60. Sluming, V., Barrick, T., Howard, M., Cezayirli, E., Mayes, A. & Roberts, N. (2002) Voxel based morphometry reveals increased gray matter density in Broca's area in male symphony orchestra musicians. Neuroimage, 17, 1613-1622.
61. Sowell, E.R., Peterson, B.S., Thompson, P.M., Welcome, S.E., Henkenius, A.L. & Toga, A.W. (2003) Mapping cortical change across the human life span. Nat. Neurosci., 6, 309-315.
62. Sowell, E.R., Thompson, P.M., Holmes, C.J., Jernigan, T.L. & Toga, A.W. (1999) In vivo evidence for post adolescent brain maturation in the frontal and striatal regions. Nat. Neurosci., 2, 859-861.
63. Sowell, E.R., Thompson, P.M., Tessner, K.D. & Toga, A.W. (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation. J. Neurosci., 21, 8819-8829.
64. Thomsen, T., Hugdahl, K., Ersland, L., Barndon, R., Lundervold, A., Smievoll, A., Roscher, B. & Sundberg, H. (2000) Functional magnetic resonance imaging (fMRI) study of sex differences in a mental rotation task. Med. Sci. Monit., 6, 1186-1196.
65. Tisserand, D.J. & Jolles, J. (2003) On the involvement of prefrontal networks in cognitive ageing. Cortex, 39, 1107-1128.
66. Tisserand, D.J., Pruessner, J.C., Sanz Arigita, E.J., van Boxtel, M.P., Evans, A.C., Jolles, J. & Uylings, H.B. (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage, 17, 657-669.
67. Tisserand, D.J., van Boxtel, M.P., Pruessner, J.C., Hofman, P., Evans, A.C. & Jolles, J. (2004) A voxel-based morphometric study to determine individual differences in gray matter density associated with age and cognitive change over time. Cereb. Cortex, 14, 966-973.
68. Tranel, D., Bechara, A. & Denburg, N.L. (2002) Asymmetric functional roles of right and left ventromedial prefrontal cortices in social conduct, decision-making, and emotional processing. Cortex, 38, 589-612.
69. Wise, P.M., Smith, M.J., Dubal, D.B., Wilson, M.E., Rau, S.W., Cashion, A.B., Bottner, M. & Rosewell, K.L. (2002) Neuroendocrine modulation and repercussions of female reproductive aging. Recent Prog. Horm. Res., 57, 235-256.
70. Witelson, S.F., Kigar, D.L. & Stoner-Beresh, H.J. (2001) Sex differences in the numerical density of neurons in the pyramidal layers of human prefrontal cortex: A stereologic study. Soc. Neurosci. Abstr., 27, 80.18.
71. Yakovlev, P.I. & Lecours, A.-R. (1967) The myelinogenetic cycles of regional maturation of the brain. In Minkowski, A. (ed.), Regional Development of the Brain in Early Life. Blackwell, Oxford, pp. 3-70.