The brain subcortical white matter and aging: A quantitative fractional anisotropy analysis

Engelhardt, Eliasz; Moreira, Denise Madeira; Laks, Jerson

doi:10.1590/S1980-57642009DN30300009

Abstract

To study the integrity of hemispheric subcortical white matter by comparing normal young and elderly subjects using quantitative fractional anisotropy (DTI-FA).

Methods:

Subjects of two different age groups (young=12, elderly=12) were included. MR - GE Signa Horizon - 1.5T scans were performed. Cases with Fazekas scores £3 were assessed on FLAIR sequence. Standard parameters for DTI-FA were used. ROIs were placed at various sites of the subcortical white matter, and the genu and splenium of the midline corpus callosum. Analysis was performed using Functool. Statistics for anterior and posterior white matter, as well as the genu and splenium were compared between the groups. The study was approved by the Ethics Committee of IPUB-UFRJ and informed consent obtained.

Results:

DTI-FA showed lower anisotropy values in the anterior region (subcortical white matter and genu), but not in the posterior region (subcortical white matter and splenium), in elderly normal subjects compared to young subjects.

Conclusion:

The results may represent loss of integrity of anterior (frontal) white matter fibers in the elderly subjects. These fibers constitute important intra- and inter-hemispheric tracts, components of neural networks that provide cognitive, behavioral, motor and sensory integration. The loss of integrity of the anterior segments of the studied fiber systems with ageing, represents a disconnection process that may underlie clinical manifestations found in elderly subjects such as executive dysfunction.

Key words:
white matter; corpus callosum; fractional anisotropy; aging.

Resumo

Estudar a integridade da substância branca hemisférica subcortical, comparando sujeitos normais jovens e idosos, com anisotropia fracionada quantitativa (DTI-FA).

Métodos:

Foram incluídos sujeitos de dois grupos etários (jovem=12, idoso=12). Obtidas imagens de MR - GE Signa Horizon - 1.5T. Escore de Fazekas £3 avaliado na sequência em FLAIR. Utilizados parâmetros padrão para DTI-FA. ROIs colocados em locais variados da substância branca subcortical, e no joelho e esplênio do corpo caloso na linha média. Análise com Functool. Estatística para comparar a substância branca anterior e posterior entre os grupos. Aprovado pela Comissão de Ética do IPUB-UFRJ, consentimento informado obtido.

Resultados:

DTI-FA mostrou redução dos valores de anisotropia na região anterior (substância branca subcortical e joelho), porém não na região posterior (substância branca subcortical e esplênio), nos sujeitos normais idosos em comparação aos jovens.

Conclusão:

Os resultados podem ser considerados como representando perda da integridade das fibras da substância branca anterior (frontal) no sujeitos do grupo idoso. Tais fibras constituem os importantes feixes intra- e inter-hemisféricos, componentes de redes neurais relacionadas com integração cognitiva, comportamental, motora e sensorial. A perda da integridade com o envelhecimento dos segmentos anteriores dos sistemas de fibras estudados representa um processo de desconexão que pode estar subjacente a manifestações clínicas, como a disfunção executiva, eventualmente encontradas em sujeitos idosos.

Palavras-chave:
substância branca; corpo caloso; anisotropia fracionada; envelhecimento.

Texto completo disponível apenas em PDF.

Full text available only in PDF format.

References

¹
Engelhardt E, Moreira DM. A substância branca cerebral: dissecção virtual dos principais feixes: tratografia. Rev Bras Neurol 2008;44(2):19-34.
²
Engelhardt E, Moreira DM. A substância branca cerebral: localização dos principais feixes com anisotropia fracionada direcional. Rev Bras Neurol 2008;44(4):19-34.
³
Mori S, Oishi K, Jiang H, et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008;40:570-582.
⁴
Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 2008;34:51-61.
⁵
Hasan KM, Kamali A, Kramer LA, Papnicolaou AC, Fletcher JM, Ewing-Cobbs L. Diffusion tensor quantification of the human midsagittal corpus callosum subdivisions across the lifespan. Brain Res 2008;1227:52-67.
⁶
Sullivan EV, Pfefferbaum A. Diffusion tensor imaging and aging. Neurosci Biobehav Rev 2006;30:749-761.
⁷
Taylor WD, Hsu E, Krishnan KRR, MacFall JR. Diffusion tensor imaging: background, potential, and utility in psychiatric research. Biol Psychiatry 2004;55:201-207.
⁸
Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316-329.
⁹
Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006; 51:527-539.
¹⁰
Schiavone F, Charlton RA, Barrick TR, Morris RG, Markus HS. Imaging age-related cognitive decline: A comparison of diffusion tensor and magnetization transfer MRI. J Magn Reson Imaging 2009;29:23-30.
¹¹
Hasan KM, Gupta RK, Santos RM, Wolinsky JS, Narayana PA. Diffusion tensor fractional anisotropy of the normal-appearing seven segments of the corpus callosum in healthy adults and relapsing-remitting multiple sclerosis patients. J Magn Reson Imaging 2005;21:735-743.
¹²
O'Sullivan M, Summers PE, Jones DK, et al. Normal-appearing white matter in ischemic leukoaraiosis: A diffusion tensor MRI study. Neurology 2001;57:2307-2310.
¹³
Allen JS, Bruss J, Brown CK, Damasio H. Normal neuroanatomical variation due to age: The major lobes and a parcellation of the temporal region. Neurobiol Aging 2005;26:1245-1260.
¹⁴
Salthouse TA. When does age-related cognitive decline begin? Neurobiol Aging 2009;30:507-514.
¹⁵
Goldman WP and Morris JC. Evidence That Age-Associated Memory Impairment Is Not a Normal Variant of Aging. Alz Dis Ass Dis 2001;15:72-79.
¹⁶
Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.
¹⁷
Hughes CP, Berg L, Danziger WL, et al. A new clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-572.
¹⁸
Hachinski VC, Iliff LD, Zilhka E, et al. Cerebral blood flow in dementia. Arch Neurol 1975;32:632-637.
¹⁹
Fazekas F, Chawluk JB, Alavi A, et al. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. Am J Neuroradiol 1987;8:421-426.
²⁰
Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004;230:77-87.
²¹
VassarStats: Statistical Computation Web Site. Disponível em: <http://faculty.vassar.edu/lowry/VassarStats.html>. Acessado em: jun. de 2008.
» http://faculty.vassar.edu/lowry/VassarStats.html
²²
Head D, Buckner RL, Shimony JS, et al. Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cereb Cortex 2004;14:410-423.
²³
O'Sullivan M, Morris RG, Huckstep B, Jones DK, Williams SC, Markus HS. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004;75:441-447.
²⁴
Abe O, Aoki S, Hayashi N, et al. Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 2002;23:433-441.
²⁵
Chepuri NB, Yen YF, Burdette JH, Li H, Moody DM, Maldjian JA. Diffusion anisotropy in the corpus callosum. AJNRAm J Neuroradiol . 2002;23:803-808.
²⁶
Ota M, Obata T, Akine Y, et al. Age-related degeneration of corpus callosum measured with diffusion tensor imaging. Neuroimage 2006;31:1445-1452.
²⁷
Sullivan EV, Rohlfing T, Pfefferbaum A. Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: Relations to timed performance. Neurobiol Aging 2008 [in press].
²⁸
Zahr NM, Rohlfing T, Pfefferbaum A, Sullivan EV. Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: a quantitative fiber tracking study. Neuroimage 2009;44:1050-1062.
²⁹
Doron KW, Gazzaniga MS. Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 2008;44:1023-1029.
³⁰
Gazzaniga MS. Cerebral specialization and interhemispheric communication. Does the corpus callosum enable the human condition? Brain 2000;123:1293-1326.
³¹
Putnam MC, Wig GS, Grafton ST, et al. Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere. J Neurosci 2008;28:2912-2918.
³²
Stephan KE, Marshall JC, Penny WD, et al. Interhemispheric Integration of Visual Processing during Task-Driven Lateralization. J Neurosci 2007;7:3512-3522.
³³
Salat DH, Tuch DS, Greve DN, et al. Age-related alterations in white matter microstructure measured by diffusion tensor imaging, Neurobiol Aging 2005;26:1215-1227.
³⁴
Sullivan EV, Adalsteinsson E, Pfefferbaum A. Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb Cortex . 2006;16: 1030-1039.
³⁵
Catani M, Ffytche DH. The rises and falls of disconnection syndromes. Brain 2005;128:2224-2239.
³⁶
Catani M, Mesulam M. What is a disconnection syndrome? Cortex 2008;44:911-913.
³⁷
Pfefferbaum A, Adalsteinsson E, Sullivan EV. Frontal circuitry degradation marks healthy adult aging: Evidence from diffusion tensor imaging. Neuroimage 2005;26:891-899.
³⁸
O'Sullivan M, Jones DK, Summers PE, Morris RG, Williams SCR, Markus HS. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 2001; 57:632-638.
³⁹
Andrews-Hanna JR, Snyder AZ, Vincent JL, et al. Disruption of large-scale brain systems in advanced aging, Neuron 2007; 56:924-935.
⁴⁰
Badre D. Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes, Trends Cogn Sci 2008;12: 193-200.
⁴¹
Charlton RA, Barrick TR, McIntyre DJ, et al. White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology 2006;66:217-222.
⁴²
Masterman DL, Cummings JL. Frontal-subcortical circuits: the anatomic basis of executive, social and motivated behaviors. J Psychopharmacol 2007;11:107-114.
⁴³
Salat DH, Tuch DS, Hevelone ND, et al. Age-related changes in prefrontal white matter measured by diffusion tensor imaging. Ann N Y Acad Sci 2005;1064:37-49.
⁴⁴
Schmahmann JD, Pandya DN. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. 7
⁴⁵
Zhang YT, Zhang CY, Zhang J, Li W. Age-related changes of normal adult brain structure: analysed with diffusion tensor imaging. Chin Med J (Engl) 2005;118:1059-1065.

Publication Dates

Publication in this collection
Jul-Sep 2009

History

Received
21 May 2009
Accepted
06 Aug 2009

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹
Engelhardt E, Moreira DM. A substância branca cerebral: dissecção virtual dos principais feixes: tratografia. Rev Bras Neurol 2008;44(2):19-34.

[2] ²
Engelhardt E, Moreira DM. A substância branca cerebral: localização dos principais feixes com anisotropia fracionada direcional. Rev Bras Neurol 2008;44(4):19-34.

[3] ³
Mori S, Oishi K, Jiang H, et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008;40:570-582.

[4] ⁴
Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 2008;34:51-61.

[5] ⁵
Hasan KM, Kamali A, Kramer LA, Papnicolaou AC, Fletcher JM, Ewing-Cobbs L. Diffusion tensor quantification of the human midsagittal corpus callosum subdivisions across the lifespan. Brain Res 2008;1227:52-67.

[6] ⁶
Sullivan EV, Pfefferbaum A. Diffusion tensor imaging and aging. Neurosci Biobehav Rev 2006;30:749-761.

[7] ⁷
Taylor WD, Hsu E, Krishnan KRR, MacFall JR. Diffusion tensor imaging: background, potential, and utility in psychiatric research. Biol Psychiatry 2004;55:201-207.

[8] ⁸
Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316-329.

[9] ⁹
Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006; 51:527-539.

[10] ¹⁰
Schiavone F, Charlton RA, Barrick TR, Morris RG, Markus HS. Imaging age-related cognitive decline: A comparison of diffusion tensor and magnetization transfer MRI. J Magn Reson Imaging 2009;29:23-30.

[11] ¹¹
Hasan KM, Gupta RK, Santos RM, Wolinsky JS, Narayana PA. Diffusion tensor fractional anisotropy of the normal-appearing seven segments of the corpus callosum in healthy adults and relapsing-remitting multiple sclerosis patients. J Magn Reson Imaging 2005;21:735-743.

[12] ¹²
O'Sullivan M, Summers PE, Jones DK, et al. Normal-appearing white matter in ischemic leukoaraiosis: A diffusion tensor MRI study. Neurology 2001;57:2307-2310.

[13] ¹³
Allen JS, Bruss J, Brown CK, Damasio H. Normal neuroanatomical variation due to age: The major lobes and a parcellation of the temporal region. Neurobiol Aging 2005;26:1245-1260.

[14] ¹⁴
Salthouse TA. When does age-related cognitive decline begin? Neurobiol Aging 2009;30:507-514.

[15] ¹⁵
Goldman WP and Morris JC. Evidence That Age-Associated Memory Impairment Is Not a Normal Variant of Aging. Alz Dis Ass Dis 2001;15:72-79.

[16] ¹⁶
Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.

[17] ¹⁷
Hughes CP, Berg L, Danziger WL, et al. A new clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-572.

[18] ¹⁸
Hachinski VC, Iliff LD, Zilhka E, et al. Cerebral blood flow in dementia. Arch Neurol 1975;32:632-637.

[19] ¹⁹
Fazekas F, Chawluk JB, Alavi A, et al. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. Am J Neuroradiol 1987;8:421-426.

[20] ²⁰
Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004;230:77-87.

[21] ²¹
VassarStats: Statistical Computation Web Site. Disponível em: <http://faculty.vassar.edu/lowry/VassarStats.html>. Acessado em: jun. de 2008.
» http://faculty.vassar.edu/lowry/VassarStats.html

[22] ²²
Head D, Buckner RL, Shimony JS, et al. Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cereb Cortex 2004;14:410-423.

[23] ²³
O'Sullivan M, Morris RG, Huckstep B, Jones DK, Williams SC, Markus HS. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004;75:441-447.

[24] ²⁴
Abe O, Aoki S, Hayashi N, et al. Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 2002;23:433-441.

[25] ²⁵
Chepuri NB, Yen YF, Burdette JH, Li H, Moody DM, Maldjian JA. Diffusion anisotropy in the corpus callosum. AJNRAm J Neuroradiol . 2002;23:803-808.

[26] ²⁶
Ota M, Obata T, Akine Y, et al. Age-related degeneration of corpus callosum measured with diffusion tensor imaging. Neuroimage 2006;31:1445-1452.

[27] ²⁷
Sullivan EV, Rohlfing T, Pfefferbaum A. Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: Relations to timed performance. Neurobiol Aging 2008 [in press].

[28] ²⁸
Zahr NM, Rohlfing T, Pfefferbaum A, Sullivan EV. Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: a quantitative fiber tracking study. Neuroimage 2009;44:1050-1062.

[29] ²⁹
Doron KW, Gazzaniga MS. Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 2008;44:1023-1029.

[30] ³⁰
Gazzaniga MS. Cerebral specialization and interhemispheric communication. Does the corpus callosum enable the human condition? Brain 2000;123:1293-1326.

[31] ³¹
Putnam MC, Wig GS, Grafton ST, et al. Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere. J Neurosci 2008;28:2912-2918.

[32] ³²
Stephan KE, Marshall JC, Penny WD, et al. Interhemispheric Integration of Visual Processing during Task-Driven Lateralization. J Neurosci 2007;7:3512-3522.

[33] ³³
Salat DH, Tuch DS, Greve DN, et al. Age-related alterations in white matter microstructure measured by diffusion tensor imaging, Neurobiol Aging 2005;26:1215-1227.

[34] ³⁴
Sullivan EV, Adalsteinsson E, Pfefferbaum A. Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb Cortex . 2006;16: 1030-1039.

[35] ³⁵
Catani M, Ffytche DH. The rises and falls of disconnection syndromes. Brain 2005;128:2224-2239.

[36] ³⁶
Catani M, Mesulam M. What is a disconnection syndrome? Cortex 2008;44:911-913.

[37] ³⁷
Pfefferbaum A, Adalsteinsson E, Sullivan EV. Frontal circuitry degradation marks healthy adult aging: Evidence from diffusion tensor imaging. Neuroimage 2005;26:891-899.

[38] ³⁸
O'Sullivan M, Jones DK, Summers PE, Morris RG, Williams SCR, Markus HS. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 2001; 57:632-638.

[39] ³⁹
Andrews-Hanna JR, Snyder AZ, Vincent JL, et al. Disruption of large-scale brain systems in advanced aging, Neuron 2007; 56:924-935.

[40] ⁴⁰
Badre D. Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes, Trends Cogn Sci 2008;12: 193-200.

[41] ⁴¹
Charlton RA, Barrick TR, McIntyre DJ, et al. White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology 2006;66:217-222.

[42] ⁴²
Masterman DL, Cummings JL. Frontal-subcortical circuits: the anatomic basis of executive, social and motivated behaviors. J Psychopharmacol 2007;11:107-114.

[43] ⁴³
Salat DH, Tuch DS, Hevelone ND, et al. Age-related changes in prefrontal white matter measured by diffusion tensor imaging. Ann N Y Acad Sci 2005;1064:37-49.

[44] ⁴⁴
Schmahmann JD, Pandya DN. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. 7

[45] ⁴⁵
Zhang YT, Zhang CY, Zhang J, Li W. Age-related changes of normal adult brain structure: analysed with diffusion tensor imaging. Chin Med J (Engl) 2005;118:1059-1065.

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