Skip to main content
SpringerLink
Log in

Structural correlates of cognitive domains in normal aging with diffusion tensor imaging

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The involvement of brain structures in specific cognitive functions is not straightforward. In order to characterize the brain micro-structural correlates of cognitive domains, 52 healthy subjects, age 25–82 years, completed a computerized neuropsychological battery and were scanned using magnetic resonance diffusion tensor imaging. Factor analysis of 44 different cognitive scores was performed, isolating three cognitive domains—executive function, information processing speed and memory. Partial correlation was conducted between DTI parameters and each of the three cognitive domains controlling for age and motor function. Regions showing significant correlations with cognitive domains are domain-specific and are consistent with previous knowledge. While executive function was correlated with diffusion tensor imaging (DTI) parameters in frontal white matter and in the superior longitudinal fasciculus, information processing speed was correlated with DTI parameters in the cingulum, corona radiata, inferior longitudinal fasciculus, parietal white matter and in the thalamus. Memory performance was correlated with DTI measures in temporal and frontal gray matter and white matter regions, including the cingulate cortex and the parahippocampus. Thus, inter-subject variability in cognitive performance and tissue morphology, as expressed by diffusion tensor magnetic resonance imaging, can be used to relate tissue microstructure with cognitive performance and to provide information to corroborate other functional localization techniques.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alvarez JA, Emory E (2006) Executive function and the frontal lobes: a meta-analytic review. Neuropsychol Rev 16(1):17–42. doi:10.1007/s11065-006-9002-x

    Article  PubMed  Google Scholar 

  • Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11(6 Pt 1):805–821

    Article  PubMed  CAS  Google Scholar 

  • Basser PJ, Pierpaoli C (1998) A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 39(6):928–934

    Article  PubMed  CAS  Google Scholar 

  • Bauer RH, Fuster JM (1976) Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. J Comp Physiol Psychol 90(3):293–302

    Article  PubMed  CAS  Google Scholar 

  • Bench CJ, Frith CD, Grasby PM, Friston KJ, Paulesu E, Frackowiak RS, Dolan RJ (1993) Investigations of the functional anatomy of attention using the Stroop test. Neuropsychologia 31(9):907–922. ppi: 0028-3932(93)90147-R

    Article  PubMed  CAS  Google Scholar 

  • Blumenfeld-Katzir T, Pasternak O, Dagan M, Assaf Y (2011) Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS One 6(6):e20678. doi:10.1371/journal.pone.0020678

  • Bookstein FL (2001) “Voxel-based morphometry” should not be used with imperfectly registered images. Neuroimage 14(6):1454–1462. doi:10.1006/nimg.2001.0770

    Article  PubMed  CAS  Google Scholar 

  • Bush G, Whalen PJ, Rosen BR, Jenike MA, McInerney SC, Rauch SL (1998) The counting Stroop: an interference task specialized for functional neuroimaging—validation study with functional MRI. Hum Brain Mapp 6(4):270–282. doi:10.1002/(SICI)1097-0193(1998)6:4<270:AID-HBM6>3.0.CO;2-0

    Article  PubMed  CAS  Google Scholar 

  • Cabeza R, Nyberg L (2000) Imaging cognition ii: an empirical review of 275 pet and fMRI studies. J Cogn Neurosci 12(1):1–47

    Article  PubMed  CAS  Google Scholar 

  • Carpenter PA, Just MA, Reichle ED (2000) Working memory and executive function: evidence from neuroimaging. Curr Opin Neurobiol 10(2):195–199. pii: S0959-4388(00)00074-X

    Article  PubMed  CAS  Google Scholar 

  • Carter CS, Mintun M, Cohen JD (1995) Interference and facilitation effects during selective attention: An h215o pet study of Stroop task performance. Neuroimage 2(4):264–272. doi:10.1006/nimg.1995.1034

    Article  PubMed  CAS  Google Scholar 

  • Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129(Pt 3):564–583. doi:10.1093/brain/awl004

    Article  PubMed  Google Scholar 

  • Charlton RA, Barrick TR, McIntyre DJ, Shen Y, O’Sullivan M, Howe FA, Clark CA, Morris RG, Markus HS (2006) White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology 66(2):217–222

    Article  PubMed  CAS  Google Scholar 

  • Constable RT, Carpentier A, Pugh K, Westerveld M, Oszunar Y, Spencer DD (2000) Investigation of the human hippocampal formation using a randomized event-related paradigm and z-shimmed functional MRI. Neuroimage 12(1):55–62. doi:10.1006/nimg.2000.0583

    Article  PubMed  CAS  Google Scholar 

  • Cowell SF, Egan GF, Code C, Harasty J, Watson JD (2000) The functional neuroanatomy of simple calculation and number repetition: a parametric pet activation study. Neuroimage 12(5):565–573

    Article  PubMed  CAS  Google Scholar 

  • Craik FI, Byrd M, Swanson JM (1987) Patterns of memory loss in three elderly samples. Psychol Aging 2(1):79–86

    Article  PubMed  CAS  Google Scholar 

  • Davachi L, Wagner AD (2002) Hippocampal contributions to episodic encoding: insights from relational and item-based learning. J Neurophysiol 88(2):982–990

    PubMed  Google Scholar 

  • Dehaene S, Tzourio N, Frak V, Raynaud L, Cohen L, Mehler J, Mazoyer B (1996) Cerebral activations during number multiplication and comparison: a pet study. Neuropsychologia 34(11):1097–1106

    Article  PubMed  CAS  Google Scholar 

  • D’Esposito M, Aguirre GK, Zarahn E, Ballard D, Shin RK, Lease J (1998) Functional MRI studies of spatial and nonspatial working memory. Brain Res Cogn Brain Res 7(1):1–13. pii: S0926-6410(98)00004-4

    Article  PubMed  Google Scholar 

  • Drewe EA (1974) The effect of type and area of brain lesion on wisconsin card sorting test performance. Cortex 10(2):159–170

    PubMed  CAS  Google Scholar 

  • Duzel E, Habib R, Rotte M, Guderian S, Tulving E, Heinze HJ (2003) Human hippocampal and parahippocampal activity during visual associative recognition memory for spatial and nonspatial stimulus configurations. J Neurosci 23(28):9439–9444. pii: 23/28/9439

    PubMed  Google Scholar 

  • Dwolatzky T, Whitehead V, Doniger GM, Simon ES, Schweiger A, Jaffe D, Chertkow H (2003) Validity of a novel computerized cognitive battery for mild cognitive impairment. BMC Geriatr 3:4

    Article  PubMed  Google Scholar 

  • Forstmann BU, Jahfari S, Scholte HS, Wolfensteller U, van den Wildenberg WP, Ridderinkhof KR (2008) Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: a model-based approach. J Neurosci 28(39):9790–9796. doi:10.1523/JNEUROSCI.1465-08.2008

    Article  PubMed  CAS  Google Scholar 

  • Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130. doi:10.1038/nrn1607

    Article  PubMed  CAS  Google Scholar 

  • Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61(2):331–349

    PubMed  CAS  Google Scholar 

  • Funahashi S, Bruce CJ, Goldman-Rakic PS (1993) Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic “Scotomas”. J Neurosci 13(4):1479–1497

    PubMed  CAS  Google Scholar 

  • Geschwind N (1965a) Disconnexion syndromes in animals and man I. Brain 88(2):237–294

    Article  PubMed  CAS  Google Scholar 

  • Geschwind N (1965b) Disconnexion syndromes in animals and man Ii. Brain 88(3):585–644

    Article  PubMed  CAS  Google Scholar 

  • Giovanello KS, Schnyer DM, Verfaellie M (2004) A critical role for the anterior hippocampus in relational memory: Evidence from an fMRI study comparing associative and item recognition. Hippocampus 14(1):5–8. doi:10.1002/hipo.10182

    Article  PubMed  Google Scholar 

  • Gold BT, Powell DK, Xuan L, Jicha GA, Smith CD (2008) Age-related slowing of task switching is associated with decreased integrity of frontoparietal white matter. Neurobiol Aging 31(3):512–522. doi:10.1016/j.neurobiolaging.2008.04.005

    Article  PubMed  Google Scholar 

  • Gouw AA, Seewann A, Vrenken H, van der Flier WM, Rozemuller JM, Barkhof F, Scheltens P, Geurts JJ (2008) Heterogeneity of white matter hyperintensities in alzheimer’s disease: post-mortem quantitative MRI and neuropathology. Brain 131(Pt 12):3286–3298. doi:10.1093/brain/awn265

    Article  PubMed  CAS  Google Scholar 

  • Grabner RH, Ansari D, Reishofer G, Stern E, Ebner F, Neuper C (2007) Individual differences in mathematical competence predict parietal brain activation during mental calculation. Neuroimage 38(2):346–356

    Article  PubMed  Google Scholar 

  • Grieve SM, Williams LM, Paul RH, Clark CR, Gordon E (2007) Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor mr imaging study. AJNR Am J Neuroradiol 28(2):226–235. pii: 28/2/226

    PubMed  CAS  Google Scholar 

  • Heilman KM, Pandya DN, Geschwind N (1970) Trimodal inattention following parietal lobe ablations. Trans Am Neurol Assoc 95:259–261

    PubMed  CAS  Google Scholar 

  • Henke K, Weber B, Kneifel S, Wieser HG, Buck A (1999) Human hippocampus associates information in memory. Proc Natl Acad Sci USA 96(10):5884–5889

    Article  PubMed  CAS  Google Scholar 

  • Henson R (2005) A mini-review of fMRI studies of human medial temporal lobe activity associated with recognition memory. Q J Exp Psychol B 58(3–4):340–360

    PubMed  Google Scholar 

  • Hu Y, Geng F, Tao L, Hu N, Du F, Fu K, Chen F (2011) Enhanced white matter tracts integrity in children with abacus training. Hum Brain Mapp 32(1):10–21

    Google Scholar 

  • Hultsch DF (1998) Memory change in the aged. Cambridge University Press, New York

    Google Scholar 

  • Klingberg T, Hedehus M, Temple E, Salz T, Gabrieli JD, Moseley ME, Poldrack RA (2000) Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging. Neuron 25(2):493–500. pii: S0896-6273(00)80911-3

    Article  PubMed  CAS  Google Scholar 

  • Leung HC, Skudlarski P, Gatenby JC, Peterson BS, Gore JC (2000) An event-related functional MRI study of the Stroop color word interference task. Cereb Cortex 10(6):552–560

    Article  PubMed  CAS  Google Scholar 

  • Lichtheim L (1885) On aphasia. Brain 7:433–484

    Google Scholar 

  • Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 21(3):1174–1181. doi:10.1016/j.neuroimage.2003.11.004

    Article  PubMed  Google Scholar 

  • Madden DJ, Spaniol J, Costello MC, Bucur B, White LE, Cabeza R, Davis SW, Dennis NA, Provenzale JM, Huettel SA (2009) Cerebral white matter integrity mediates adult age differences in cognitive performance. J Cogn Neurosci 21(2):289–302

    Article  PubMed  Google Scholar 

  • Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239

    Article  PubMed  Google Scholar 

  • Milner B (1971) Interhemispheric differences in the localization of psychological processes in man. Br Med Bull 27(3):272–277

    PubMed  CAS  Google Scholar 

  • Pardo JV, Pardo PJ, Janer KW, Raichle ME (1990) The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proc Natl Acad Sci USA 87(1):256–259

    Article  PubMed  CAS  Google Scholar 

  • Perret E (1974) The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. Neuropsychologia 12(3):323–330

    Article  PubMed  CAS  Google Scholar 

  • Perry ME, McDonald CR, Hagler DJ Jr, Gharapetian L, Kuperman JM, Koyama AK, Dale AM, McEvoy LK (2009) White matter tracts associated with set-shifting in healthy aging. Neuropsychologia 47(13):2835–2842

    Article  PubMed  Google Scholar 

  • Persson J, Nyberg L, Lind J, Larsson A, Nilsson LG, Ingvar M, Buckner RL (2006) Structure-function correlates of cognitive decline in aging. Cereb Cortex 16(7):907–915

    Article  PubMed  Google Scholar 

  • Petersen RC, Smith G, Kokmen E, Ivnik RJ, Tangalos EG (1992) Memory function in normal aging. Neurology 42(2):396–401

    PubMed  CAS  Google Scholar 

  • Peterson BS, Skudlarski P, Gatenby JC, Zhang H, Anderson AW, Gore JC (1999) An fMRI study of Stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems. Biol Psychiatry 45(10):1237–1258. pii: S0006-3223(99)00056-6

    Article  PubMed  CAS  Google Scholar 

  • Posner MI, Dehaene S (1994) Attentional networks. Trends Neurosci 17(2):75–79

    Article  PubMed  CAS  Google Scholar 

  • Posner MI, Petersen SE (1990) The attention system of the human brain. Annu Rev Neurosci 13:25–42. doi:10.1146/annurev.ne.13.030190.000325

    Article  PubMed  CAS  Google Scholar 

  • Rickard TC, Romero SG, Basso G, Wharton C, Flitman S, Grafman J (2000) The calculating brain: an fMRI study. Neuropsychologia 38(3):325–335

    Article  PubMed  CAS  Google Scholar 

  • Rocha FT, Rocha AF, Massad E, Menezes R (2005) Brain mappings of the arithmetic processing in children and adults. Brain Res Cogn Brain Res 22(3):359–372. doi:10.1016/j.cogbrainres.2004.09.008

    Article  PubMed  CAS  Google Scholar 

  • Rowe AD, Bullock PR, Polkey CE, Morris RG (2001) “Theory of mind” Impairments and their relationship to executive functioning following frontal lobe excisions. Brain 124(Pt 3):600–616

    Article  PubMed  CAS  Google Scholar 

  • Salthouse TA (2000) Aging and measures of processing speed. Biol Psychol 54(1–3):35–54. pii: S0301051100000521

    Article  PubMed  CAS  Google Scholar 

  • Sasson E, Doniger GM, Pasternak O, Assaf Y (2010) Structural correlates of memory performance with diffusion tensor imaging. Neuroimage 50(3):1231–1242. doi:10.1016/j.neuroimage.2009.12.079

    Article  PubMed  Google Scholar 

  • Schaie KW (1996) Intellectual development in adulthood: the seattle longitudinal study. Cambridge University Press, New York

    Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20(1):11–21

    Article  PubMed  CAS  Google Scholar 

  • Small SA (2001) Age-related memory decline: current concepts and future directions. Arch Neurol 58(3):360–364

    Article  PubMed  CAS  Google Scholar 

  • Sullivan EV, Adalsteinsson E, Pfefferbaum A (2006) Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb Cortex 16(7):1030–1039

    Article  PubMed  Google Scholar 

  • Swartz BE, Halgren E, Fuster JM, Simpkins E, Gee M, Mandelkern M (1995) Cortical metabolic activation in humans during a visual memory task. Cereb Cortex 5(3):205–214

    Article  PubMed  CAS  Google Scholar 

  • Tanabe H, Sawada T, Inoue N, Ogawa M, Kuriyama Y, Shiraishi J (1987) Conduction aphasia and arcuate fasciculus. Acta Neurol Scand 76(6):422–427

    Article  PubMed  CAS  Google Scholar 

  • Taylor SF, Kornblum S, Lauber EJ, Minoshima S, Koeppe RA (1997) Isolation of specific interference processing in the Stroop task: pet activation studies. Neuroimage 6(2):81–92. doi:10.1006/nimg.1997.0285

    Article  PubMed  CAS  Google Scholar 

  • Thompson RF, Kim JJ (1996) Memory systems in the brain and localization of a memory. Proc Natl Acad Sci USA 93(24):13438–13444

    Article  PubMed  CAS  Google Scholar 

  • Tuch DS, Salat DH, Wisco JJ, Zaleta AK, Hevelone ND, Rosas HD (2005) Choice reaction time performance correlates with diffusion anisotropy in white matter pathways supporting visuospatial attention. Proc Natl Acad Sci USA 102(34):12212–12217. doi:10.1073/pnas.0407259102

    Article  PubMed  CAS  Google Scholar 

  • van Eimeren L, Grabner RH, Koschutnig K, Reishofer G, Ebner F, Ansari D (2010) Structure-function relationships underlying calculation: a combined diffusion tensor imaging and fMRI study. Neuroimage 52(1):358–363. doi:10.1016/j.neuroimage.2010.04.001

    Article  PubMed  Google Scholar 

  • Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, Quinn BT, Salat D, Makris N, Fischl B (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26(9):1261–1270 (discussion 1275–1268)

    Article  PubMed  Google Scholar 

  • Youngjohn JR, Crook TH 3rd (1993) Learning, forgetting, and retrieval of everyday material across the adult life span. J Clin Exp Neuropsychol 15(4):447–460

    Article  PubMed  CAS  Google Scholar 

  • Zahr NM, Rohlfing T, Pfefferbaum A, Sullivan EV (2009) Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: a quantitative fiber tracking study. Neuroimage 44(3):1050–1062

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Y.A. wishes to thank the Israel Science Foundation (ISF grant no. 994/08) and the BIRAX program of the British council for grant support. The Future and Emerging Technologies (FET) program of the ICT - EU FP7 framework fund the CONNECT consortium (http://www.brain-connect.eu), which supports this work.

E.S. wishes to thank the Myers-JDC-Brookdale institute of gerontology and human development, and Eshel - The association for the planning and development of services for the aged in Israel, for grant support.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Faculty of Life Sciences, Tel Aviv University, 69978, Tel Aviv, Israel

    Efrat Sasson & Yaniv Assaf

  2. Department of Clinical Science, NeuroTrax Corporation, Fresh Meadows, NY, USA

    Glen M. Doniger

  3. Psychiatry Neourimaging Laboratory, Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Ofer Pasternak

  4. Department of Psychology, Tel Aviv University, Tel Aviv, Israel

    Ricardo Tarrasch

Authors
  1. Efrat Sasson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Glen M. Doniger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ofer Pasternak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo Tarrasch
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaniv Assaf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Efrat Sasson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 25 kb)

Supplementary Figure (TIF 273 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sasson, E., Doniger, G.M., Pasternak, O. et al. Structural correlates of cognitive domains in normal aging with diffusion tensor imaging. Brain Struct Funct 217, 503–515 (2012). https://doi.org/10.1007/s00429-011-0344-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-011-0344-7

Keywords

Search

Navigation