Skip to main content
Top
Published in: Magnetic Resonance Materials in Physics, Biology and Medicine 6/2016

Open Access 01-12-2016 | Research Article

Quantitative T1 and T2 MRI signal characteristics in the human brain: different patterns of MR contrasts in normal ageing

Authors: Michael J. Knight, Bryony McCann, Demitra Tsivos, Elizabeth Couthard, Risto A. Kauppinen

Published in: Magnetic Resonance Materials in Physics, Biology and Medicine | Issue 6/2016

Login to get access

Abstract

Objective

The objective of this study was to examine age-dependent changes in both T1-weighted and T2-weighted image contrasts and spin-echo T2 relaxation time in the human brain during healthy ageing.

Methods

A total of 37 participants between the ages of 49 and 87 years old were scanned with a 3 Tesla system, using T1-weighted, T2 weighted and quantitative spin-echo T2 imaging. Contrast between image intensities and T2 values was calculated for various regions, including between individual hippocampal subfields.

Results

The T1 contrast-to-noise (CNR) and gray:white signal intensity ratio (GWR) did not change in the hippocampus, but it declined in the cingulate cortex with age. In contrast, T2 CNR and GWR declined in both brain regions. T2 relaxation time was almost constant in gray matter and most (but not all) hippocampal subfields, but increased substantially in white matter, pointing to an age effect on water relaxation in white matter.

Conclusions

Changes in T1 and T2 MR characteristics influence the appearance of brain images in later life and should be considered in image analyses of aged subjects. It is speculated that alterations at the cell biology level, with concomitant alterations to the local magnetic environment, reduce dephasing and subsequently prolong spin-echo T2 through reduced diffusion effects in later life.
Appendix
Available only for authorised users
Literature
1.
go back to reference Leenders KL, Perani D, Lammertsma AA, Heather JD, Buckingham P, Healy MJ, Gibbs JM, Wise RJ, Hatazawa J, Herold S et al (1990) Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 113(Pt 1):27–47CrossRefPubMed Leenders KL, Perani D, Lammertsma AA, Heather JD, Buckingham P, Healy MJ, Gibbs JM, Wise RJ, Hatazawa J, Herold S et al (1990) Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 113(Pt 1):27–47CrossRefPubMed
2.
go back to reference Tang Y, Nyengaard JR, Pakkenberg B, Gundersen HJ (1997) Age-induced white matter changes in the human brain: a stereological investigation. Neurobiol Aging 18(6):609–615CrossRefPubMed Tang Y, Nyengaard JR, Pakkenberg B, Gundersen HJ (1997) Age-induced white matter changes in the human brain: a stereological investigation. Neurobiol Aging 18(6):609–615CrossRefPubMed
3.
go back to reference Callaghan MF, Freund P, Draganski B, Anderson E, Cappelletti M, Chowdhury R, Diedrichsen J, Fitzgerald TH, Smittenaar P, Helms G, Lutti A, Weiskopf N (2014) Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging. Neurobiol Aging 35(8):1862–1872CrossRefPubMedPubMedCentral Callaghan MF, Freund P, Draganski B, Anderson E, Cappelletti M, Chowdhury R, Diedrichsen J, Fitzgerald TH, Smittenaar P, Helms G, Lutti A, Weiskopf N (2014) Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging. Neurobiol Aging 35(8):1862–1872CrossRefPubMedPubMedCentral
4.
go back to reference Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RS, Helms G, Weiskopf N (2011) Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 55(4):1423–1434CrossRefPubMedPubMedCentral Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RS, Helms G, Weiskopf N (2011) Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 55(4):1423–1434CrossRefPubMedPubMedCentral
5.
go back to reference Chang L, Ernst T, Poland RE, Jenden DJ (1996) In vivo proton magnetic resonance spectroscopy of the normal aging human brain. Life Sci 58(22):2049–2056CrossRefPubMed Chang L, Ernst T, Poland RE, Jenden DJ (1996) In vivo proton magnetic resonance spectroscopy of the normal aging human brain. Life Sci 58(22):2049–2056CrossRefPubMed
6.
go back to reference House MJ, St Pierre TG, Kowdley KV, Montine T, Connor J, Beard J, Berger J, Siddaiah N, Shankland E, Jin LW (2007) Correlation of proton transverse relaxation rates (R2) with iron concentrations in postmortem brain tissue from Alzheimer’s disease patients. Magn Reson Med 57(1):172–180CrossRefPubMed House MJ, St Pierre TG, Kowdley KV, Montine T, Connor J, Beard J, Berger J, Siddaiah N, Shankland E, Jin LW (2007) Correlation of proton transverse relaxation rates (R2) with iron concentrations in postmortem brain tissue from Alzheimer’s disease patients. Magn Reson Med 57(1):172–180CrossRefPubMed
7.
go back to reference Ogg RJ, Steen RG (1998) Age-related changes in brain T1 are correlated with iron concentration. Magn Reson Med 40(5):749–753CrossRefPubMed Ogg RJ, Steen RG (1998) Age-related changes in brain T1 are correlated with iron concentration. Magn Reson Med 40(5):749–753CrossRefPubMed
9.
go back to reference Salat DH, Lee SY, van der Kouwe AJ, Greve DN, Fischl B, Rosas HD (2009) Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast. Neuroimage 48(1):21–28CrossRefPubMedPubMedCentral Salat DH, Lee SY, van der Kouwe AJ, Greve DN, Fischl B, Rosas HD (2009) Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast. Neuroimage 48(1):21–28CrossRefPubMedPubMedCentral
10.
go back to reference Scahill RI, Fox NC (2007) Longitudinal imaging in dementia. Br J Radiol 80(special_issue_2):S92–S98CrossRefPubMed Scahill RI, Fox NC (2007) Longitudinal imaging in dementia. Br J Radiol 80(special_issue_2):S92–S98CrossRefPubMed
11.
12.
go back to reference Fox NC, Schott JM (2004) Imaging cerebral atrophy: normal ageing to Alzheimer’s disease. Lancet 363(9406):392–394CrossRefPubMed Fox NC, Schott JM (2004) Imaging cerebral atrophy: normal ageing to Alzheimer’s disease. Lancet 363(9406):392–394CrossRefPubMed
13.
go back to reference McDonald CR, McEvoy LK, Gharapetian L, Fennema-Notestine C, Hagler DJ, Holland D, Koyama A, Brewer JB, Dale AM, For the Alzheimer’s Disease Neuroimaging I (2009) Regional rates of neocortical atrophy from normal aging to early Alzheimer disease. Neurology 73(6):457–465CrossRefPubMedPubMedCentral McDonald CR, McEvoy LK, Gharapetian L, Fennema-Notestine C, Hagler DJ, Holland D, Koyama A, Brewer JB, Dale AM, For the Alzheimer’s Disease Neuroimaging I (2009) Regional rates of neocortical atrophy from normal aging to early Alzheimer disease. Neurology 73(6):457–465CrossRefPubMedPubMedCentral
15.
go back to reference Whitwell JL, Przybelski SA, Weigand SD, Knopman DS, Boeve BF, Petersen RC, Jack CR Jr (2007) 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer’s disease. Brain 130(Pt 7):1777–1786CrossRefPubMedPubMedCentral Whitwell JL, Przybelski SA, Weigand SD, Knopman DS, Boeve BF, Petersen RC, Jack CR Jr (2007) 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer’s disease. Brain 130(Pt 7):1777–1786CrossRefPubMedPubMedCentral
16.
go back to reference Li J, Pan P, Huang R, Shang H (2012) A meta-analysis of voxel-based morphometry studies of white matter volume alterations in Alzheimer’s disease. Neurosci Biobehav Rev 36(2):757–763CrossRefPubMed Li J, Pan P, Huang R, Shang H (2012) A meta-analysis of voxel-based morphometry studies of white matter volume alterations in Alzheimer’s disease. Neurosci Biobehav Rev 36(2):757–763CrossRefPubMed
17.
go back to reference Wang WY, Yu JT, Liu Y, Yin RH, Wang HF, Wang J, Tan L, Radua J, Tan L (2015) Voxel-based meta-analysis of grey matter changes in Alzheimer’s disease. Transl Neurodegener 4:6CrossRefPubMedPubMedCentral Wang WY, Yu JT, Liu Y, Yin RH, Wang HF, Wang J, Tan L, Radua J, Tan L (2015) Voxel-based meta-analysis of grey matter changes in Alzheimer’s disease. Transl Neurodegener 4:6CrossRefPubMedPubMedCentral
18.
go back to reference Pan PL, Song W, Yang J, Huang R, Chen K, Gong QY, Zhong JG, Shi HC, Shang HF (2012) Gray matter atrophy in behavioral variant frontotemporal dementia: a meta-analysis of voxel-based morphometry studies. Dement Geriatr Cogn Disord 33(2–3):141–148CrossRefPubMed Pan PL, Song W, Yang J, Huang R, Chen K, Gong QY, Zhong JG, Shi HC, Shang HF (2012) Gray matter atrophy in behavioral variant frontotemporal dementia: a meta-analysis of voxel-based morphometry studies. Dement Geriatr Cogn Disord 33(2–3):141–148CrossRefPubMed
19.
go back to reference Pan PL, Shi HC, Zhong JG, Xiao PR, Shen Y, Wu LJ, Song YY, He GX, Li HL (2013) Gray matter atrophy in Parkinson’s disease with dementia: evidence from meta-analysis of voxel-based morphometry studies. Neurol Sci 34(5):613–619CrossRefPubMed Pan PL, Shi HC, Zhong JG, Xiao PR, Shen Y, Wu LJ, Song YY, He GX, Li HL (2013) Gray matter atrophy in Parkinson’s disease with dementia: evidence from meta-analysis of voxel-based morphometry studies. Neurol Sci 34(5):613–619CrossRefPubMed
20.
go back to reference Shi HC, Zhong JG, Pan PL, Xiao PR, Shen Y, Wu LJ, Li HL, Song YY, He GX, Li HY (2013) Gray matter atrophy in progressive supranuclear palsy: meta-analysis of voxel-based morphometry studies. Neurol Sci 34(7):1049–1055CrossRefPubMed Shi HC, Zhong JG, Pan PL, Xiao PR, Shen Y, Wu LJ, Li HL, Song YY, He GX, Li HY (2013) Gray matter atrophy in progressive supranuclear palsy: meta-analysis of voxel-based morphometry studies. Neurol Sci 34(7):1049–1055CrossRefPubMed
21.
go back to reference Westlye LT, Walhovd KB, Dale AM, Espeseth T, Reinvang I, Raz N, Agartz I, Greve DN, Fischl B, Fjell AM (2009) Increased sensitivity to effects of normal aging and Alzheimer’s disease on cortical thickness by adjustment for local variability in gray/white contrast: a multi-sample MRI study. Neuroimage 47(4):1545–1557CrossRefPubMedPubMedCentral Westlye LT, Walhovd KB, Dale AM, Espeseth T, Reinvang I, Raz N, Agartz I, Greve DN, Fischl B, Fjell AM (2009) Increased sensitivity to effects of normal aging and Alzheimer’s disease on cortical thickness by adjustment for local variability in gray/white contrast: a multi-sample MRI study. Neuroimage 47(4):1545–1557CrossRefPubMedPubMedCentral
22.
go back to reference Salat DH, Chen JJ, van der Kouwe AJ, Greve DN, Fischl B, Rosas HD (2011) Hippocampal degeneration is associated with temporal and limbic gray matter/white matter tissue contrast in Alzheimer’s disease. Neuroimage 54(3):1795–1802CrossRefPubMed Salat DH, Chen JJ, van der Kouwe AJ, Greve DN, Fischl B, Rosas HD (2011) Hippocampal degeneration is associated with temporal and limbic gray matter/white matter tissue contrast in Alzheimer’s disease. Neuroimage 54(3):1795–1802CrossRefPubMed
23.
go back to reference Yushkevich PA, Amaral RS, Augustinack JC, Bender AR, Bernstein JD, Boccardi M, Bocchetta M, Burggren AC, Carr VA, Chakravarty MM, Chetelat G, Daugherty AM, Davachi L, Ding SL, Ekstrom A, Geerlings MI, Hassan A, Huang Y, Iglesias JE, La Joie R, Kerchner GA, LaRocque KF, Libby LA, Malykhin N, Mueller SG, Olsen RK, Palombo DJ, Parekh MB, Pluta JB, Preston AR, Pruessner JC, Ranganath C, Raz N, Schlichting ML, Schoemaker D, Singh S, Stark CE, Suthana N, Tompary A, Turowski MM, Van Leemput K, Wagner AD, Wang L, Winterburn JL, Wisse LE, Yassa MA, Zeineh MM (2015) Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: towards a harmonized segmentation protocol. Neuroimage 111:526–541CrossRefPubMedPubMedCentral Yushkevich PA, Amaral RS, Augustinack JC, Bender AR, Bernstein JD, Boccardi M, Bocchetta M, Burggren AC, Carr VA, Chakravarty MM, Chetelat G, Daugherty AM, Davachi L, Ding SL, Ekstrom A, Geerlings MI, Hassan A, Huang Y, Iglesias JE, La Joie R, Kerchner GA, LaRocque KF, Libby LA, Malykhin N, Mueller SG, Olsen RK, Palombo DJ, Parekh MB, Pluta JB, Preston AR, Pruessner JC, Ranganath C, Raz N, Schlichting ML, Schoemaker D, Singh S, Stark CE, Suthana N, Tompary A, Turowski MM, Van Leemput K, Wagner AD, Wang L, Winterburn JL, Wisse LE, Yassa MA, Zeineh MM (2015) Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: towards a harmonized segmentation protocol. Neuroimage 111:526–541CrossRefPubMedPubMedCentral
24.
go back to reference Magnaldi S, Ukmar M, Vasciaveo A, Longo R, Pozzi-Mucelli RS (1993) Contrast between white and grey matter: MRI appearance with ageing. Eur Radiol 3(6):513–519CrossRef Magnaldi S, Ukmar M, Vasciaveo A, Longo R, Pozzi-Mucelli RS (1993) Contrast between white and grey matter: MRI appearance with ageing. Eur Radiol 3(6):513–519CrossRef
25.
go back to reference Kim DM, Xanthakos SA, Tupler LA, Barboriak DP, Charles HC, MacFall JR, Krishnan KR (2002) MR signal intensity of gray matter/white matter contrast and intracranial fat: effects of age and sex. Psychiatry Res 114(3):149–161CrossRefPubMed Kim DM, Xanthakos SA, Tupler LA, Barboriak DP, Charles HC, MacFall JR, Krishnan KR (2002) MR signal intensity of gray matter/white matter contrast and intracranial fat: effects of age and sex. Psychiatry Res 114(3):149–161CrossRefPubMed
26.
go back to reference Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20(1):45–57CrossRefPubMed Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20(1):45–57CrossRefPubMed
27.
go back to reference Wood B, Knight MJ, Tsivos D, Oliver R, Coulthard E, Kauppinen RA (2015) Magnetic resonance scanning and image segmentation procedure at 3 T for volumetry of human hippocampal subfields. Biomed Spectrosc Imaging 4(2):197–208 Wood B, Knight MJ, Tsivos D, Oliver R, Coulthard E, Kauppinen RA (2015) Magnetic resonance scanning and image segmentation procedure at 3 T for volumetry of human hippocampal subfields. Biomed Spectrosc Imaging 4(2):197–208
28.
go back to reference Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW (2010) Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer’s disease. Hum Brain Mapp 31(9):1339–1347CrossRefPubMedPubMedCentral Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW (2010) Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer’s disease. Hum Brain Mapp 31(9):1339–1347CrossRefPubMedPubMedCentral
29.
go back to reference Barnes J, Godbolt AK, Frost C, Boyes RG, Jones BF, Scahill RI, Rossor MN, Fox NC (2007) Atrophy rates of the cingulate gyrus and hippocampus in AD and FTLD. Neurobiol Aging 28(1):20–28CrossRefPubMed Barnes J, Godbolt AK, Frost C, Boyes RG, Jones BF, Scahill RI, Rossor MN, Fox NC (2007) Atrophy rates of the cingulate gyrus and hippocampus in AD and FTLD. Neurobiol Aging 28(1):20–28CrossRefPubMed
30.
go back to reference Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J (2006) The hippocampus book. Oxford University Press, OxfordCrossRef Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J (2006) The hippocampus book. Oxford University Press, OxfordCrossRef
31.
go back to reference Peters A (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31(8–9):581–593CrossRefPubMed Peters A (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31(8–9):581–593CrossRefPubMed
32.
go back to reference Bock NA, Kocharyan A, Liu JV, Silva AC (2009) Visualizing the entire cortical myelination pattern in marmosets with magnetic resonance imaging. J Neurosci Methods 185(1):15–22CrossRefPubMedPubMedCentral Bock NA, Kocharyan A, Liu JV, Silva AC (2009) Visualizing the entire cortical myelination pattern in marmosets with magnetic resonance imaging. J Neurosci Methods 185(1):15–22CrossRefPubMedPubMedCentral
33.
go back to reference Glasser MF, Goyal MS, Preuss TM, Raichle ME, Van Essen DC (2014) Trends and properties of human cerebral cortex: correlations with cortical myelin content. Neuroimage 93(Pt 2):165–175CrossRefPubMed Glasser MF, Goyal MS, Preuss TM, Raichle ME, Van Essen DC (2014) Trends and properties of human cerebral cortex: correlations with cortical myelin content. Neuroimage 93(Pt 2):165–175CrossRefPubMed
34.
go back to reference Lutti A, Dick F, Sereno MI, Weiskopf N (2014) Using high-resolution quantitative mapping of R1 as an index of cortical myelination. Neuroimage 93(Pt 2):176–188CrossRefPubMed Lutti A, Dick F, Sereno MI, Weiskopf N (2014) Using high-resolution quantitative mapping of R1 as an index of cortical myelination. Neuroimage 93(Pt 2):176–188CrossRefPubMed
35.
go back to reference Alonso-Ortiz E, Levesque IR, Pike GB (2015) MRI-based myelin water imaging: a technical review. Magn Reson Med 73(1):70–81CrossRefPubMed Alonso-Ortiz E, Levesque IR, Pike GB (2015) MRI-based myelin water imaging: a technical review. Magn Reson Med 73(1):70–81CrossRefPubMed
36.
go back to reference Wilhelm MJ, Ong HH, Wehrli SL, Li C, Tsai P-H, Hackney DB, Wehrli FW (2012) Direct magnetic resonance detection of myelin and prospects for quantitative imaging of myelin density. Proc Natl Acad Sci USA 109(24):9605–9610CrossRefPubMedPubMedCentral Wilhelm MJ, Ong HH, Wehrli SL, Li C, Tsai P-H, Hackney DB, Wehrli FW (2012) Direct magnetic resonance detection of myelin and prospects for quantitative imaging of myelin density. Proc Natl Acad Sci USA 109(24):9605–9610CrossRefPubMedPubMedCentral
37.
go back to reference Kochunov P, Williamson DE, Lancaster J, Fox P, Cornell J, Blangero J, Glahn DC (2012) Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiol Aging 33(1):9–20CrossRefPubMed Kochunov P, Williamson DE, Lancaster J, Fox P, Cornell J, Blangero J, Glahn DC (2012) Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiol Aging 33(1):9–20CrossRefPubMed
38.
go back to reference Besson JA, Best PV, Skinner ER (1992) Post-mortem proton magnetic resonance spectrometric measures of brain regions in patients with a pathological diagnosis of Alzheimer’s disease and multi-infarct dementia. Br J Psychiatry 160:187–190CrossRefPubMed Besson JA, Best PV, Skinner ER (1992) Post-mortem proton magnetic resonance spectrometric measures of brain regions in patients with a pathological diagnosis of Alzheimer’s disease and multi-infarct dementia. Br J Psychiatry 160:187–190CrossRefPubMed
39.
go back to reference Sedlacik J, Boelmans K, Lobel U, Holst B, Siemonsen S, Fiehler J (2014) Reversible, irreversible and effective transverse relaxation rates in normal aging brain at 3T. Neuroimage 84:1032–1041CrossRefPubMed Sedlacik J, Boelmans K, Lobel U, Holst B, Siemonsen S, Fiehler J (2014) Reversible, irreversible and effective transverse relaxation rates in normal aging brain at 3T. Neuroimage 84:1032–1041CrossRefPubMed
40.
go back to reference Biagi L, Abbruzzese A, Bianchi MC, Alsop DC, Del Guerra A, Tosetti M (2007) Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling. J Magn Reson Imaging 25(4):696–702CrossRefPubMed Biagi L, Abbruzzese A, Bianchi MC, Alsop DC, Del Guerra A, Tosetti M (2007) Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling. J Magn Reson Imaging 25(4):696–702CrossRefPubMed
41.
go back to reference Liu Y, Zhu X, Feinberg D, Guenther M, Gregori J, Weiner MW, Schuff N (2012) Arterial spin labeling MRI study of age and gender effects on brain perfusion hemodynamics. Magn Reson Med 68(3):912–922CrossRefPubMed Liu Y, Zhu X, Feinberg D, Guenther M, Gregori J, Weiner MW, Schuff N (2012) Arterial spin labeling MRI study of age and gender effects on brain perfusion hemodynamics. Magn Reson Med 68(3):912–922CrossRefPubMed
42.
go back to reference McConathy J, Sheline YI (2015) Imaging biomarkers associated with cognitive decline: a review. Biol Psychiatry 77(8):685–692CrossRefPubMed McConathy J, Sheline YI (2015) Imaging biomarkers associated with cognitive decline: a review. Biol Psychiatry 77(8):685–692CrossRefPubMed
43.
go back to reference Barnes J, Bartlett JW, van de Pol LA, Loy CT, Scahill RI, Frost C, Thompson P, Fox NC (2009) A meta-analysis of hippocampal atrophy rates in Alzheimer’s disease. Neurobiol Aging 30(11):1711–1723CrossRefPubMed Barnes J, Bartlett JW, van de Pol LA, Loy CT, Scahill RI, Frost C, Thompson P, Fox NC (2009) A meta-analysis of hippocampal atrophy rates in Alzheimer’s disease. Neurobiol Aging 30(11):1711–1723CrossRefPubMed
44.
go back to reference Hänggi J, Streffer J, Jäncke L, Hock C (2011) Volumes of lateral temporal and parietal structures distinguish between healthy aging, mild cognitive impairment, and Alzheimer’s disease. J Alzheimers Dis 26(4):719–734PubMed Hänggi J, Streffer J, Jäncke L, Hock C (2011) Volumes of lateral temporal and parietal structures distinguish between healthy aging, mild cognitive impairment, and Alzheimer’s disease. J Alzheimers Dis 26(4):719–734PubMed
45.
go back to reference Leung KK, Bartlett JW, Barnes J, Manning EN, Ourselin S, Fox NC (2013) Cerebral atrophy in mild cognitive impairment and Alzheimer disease: rates and acceleration. Neurology 80(7):648–654CrossRefPubMedPubMedCentral Leung KK, Bartlett JW, Barnes J, Manning EN, Ourselin S, Fox NC (2013) Cerebral atrophy in mild cognitive impairment and Alzheimer disease: rates and acceleration. Neurology 80(7):648–654CrossRefPubMedPubMedCentral
46.
go back to reference Pengas G, Hodges JR, Watson P, Nestor PJ (2010) Focal posterior cingulate atrophy in incipient Alzheimer’s disease. Neurobiol Aging 31(1):25–33CrossRefPubMed Pengas G, Hodges JR, Watson P, Nestor PJ (2010) Focal posterior cingulate atrophy in incipient Alzheimer’s disease. Neurobiol Aging 31(1):25–33CrossRefPubMed
47.
go back to reference Winterburn JL, Pruessner JC, Chavez S, Schira MM, Lobaugh NJ, Voineskos AN, Chakravarty MM (2013) A novel in vivo atlas of human hippocampal subfields using high-resolution 3 T magnetic resonance imaging. Neuroimage 74:254–265CrossRefPubMed Winterburn JL, Pruessner JC, Chavez S, Schira MM, Lobaugh NJ, Voineskos AN, Chakravarty MM (2013) A novel in vivo atlas of human hippocampal subfields using high-resolution 3 T magnetic resonance imaging. Neuroimage 74:254–265CrossRefPubMed
48.
go back to reference Wisse LE, Gerritsen L, Zwanenburg JJ, Kuijf HJ, Luijten PR, Biessels GJ, Geerlings MI (2012) Subfields of the hippocampal formation at 7 T MRI: in vivo volumetric assessment. Neuroimage 61(4):1043–1049CrossRefPubMed Wisse LE, Gerritsen L, Zwanenburg JJ, Kuijf HJ, Luijten PR, Biessels GJ, Geerlings MI (2012) Subfields of the hippocampal formation at 7 T MRI: in vivo volumetric assessment. Neuroimage 61(4):1043–1049CrossRefPubMed
49.
go back to reference La Joie R, Fouquet M, Mezenge F, Landeau B, Villain N, Mevel K, Pelerin A, Eustache F, Desgranges B, Chetelat G (2010) Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage 53(2):506–514CrossRefPubMed La Joie R, Fouquet M, Mezenge F, Landeau B, Villain N, Mevel K, Pelerin A, Eustache F, Desgranges B, Chetelat G (2010) Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage 53(2):506–514CrossRefPubMed
50.
go back to reference Maurin H, Chong SA, Kraev I, Davies H, Kremer A, Seymour CM, Lechat B, Jaworski T, Borghgraef P, Devijver H, Callewaert G, Stewart MG, Van Leuven F (2014) Early structural and functional defects in synapses and myelinated axons in stratum lacunosum moleculare in two preclinical models for tauopathy. PLoS ONE 9(2):e87605CrossRefPubMedPubMedCentral Maurin H, Chong SA, Kraev I, Davies H, Kremer A, Seymour CM, Lechat B, Jaworski T, Borghgraef P, Devijver H, Callewaert G, Stewart MG, Van Leuven F (2014) Early structural and functional defects in synapses and myelinated axons in stratum lacunosum moleculare in two preclinical models for tauopathy. PLoS ONE 9(2):e87605CrossRefPubMedPubMedCentral
51.
go back to reference Salat DH, Tuch DS, van der Kouwe AJ, Greve DN, Pappu V, Lee SY, Hevelone ND, Zaleta AK, Growdon JH, Corkin S, Fischl B, Rosas HD (2010) White matter pathology isolates the hippocampal formation in Alzheimer’s disease. Neurobiol Aging 31(2):244–256CrossRefPubMedPubMedCentral Salat DH, Tuch DS, van der Kouwe AJ, Greve DN, Pappu V, Lee SY, Hevelone ND, Zaleta AK, Growdon JH, Corkin S, Fischl B, Rosas HD (2010) White matter pathology isolates the hippocampal formation in Alzheimer’s disease. Neurobiol Aging 31(2):244–256CrossRefPubMedPubMedCentral
Metadata
Title
Quantitative T1 and T2 MRI signal characteristics in the human brain: different patterns of MR contrasts in normal ageing
Authors
Michael J. Knight
Bryony McCann
Demitra Tsivos
Elizabeth Couthard
Risto A. Kauppinen
Publication date
01-12-2016
Publisher
Springer Berlin Heidelberg
Published in
Magnetic Resonance Materials in Physics, Biology and Medicine / Issue 6/2016
Print ISSN: 0968-5243
Electronic ISSN: 1352-8661
DOI
https://doi.org/10.1007/s10334-016-0573-0

Other articles of this Issue 6/2016

Magnetic Resonance Materials in Physics, Biology and Medicine 6/2016 Go to the issue