Advertisement

Neuroradiology

, Volume 57, Issue 8, pp 851–861 | Cite as

The association of brain structure with gait velocity in older adults: a quantitative volumetric analysis of brain MRI

  • Ali EzzatiEmail author
  • Mindy J. Katz
  • Michael L. Lipton
  • Richard B. Lipton
  • Joe Verghese
Functional Neuroradiology

Abstract

Introduction

While cortical processes play an important role in controlling locomotion, the underlying structural brain changes associated with slowing of gait in aging are not yet fully established. Our study aimed to examine the relationship between cortical gray matter volume (GM), white matter volume (WM), ventricular volume (VV), hippocampal and hippocampal subfield volumes, and gait velocity in older adults free of dementia.

Methods

Gait and cognitive performance was tested in 112 community-residing adults, age 70 years and over, participating in the Einstein Aging Study. Gait velocity (cm/s) was obtained using an instrumented walkway. Volumetric MRI measures were estimated using a FreeSurfer software. We examined the cross-sectional relationship of GM, WM, VV, and hippocampal total and subfield volumes and gait velocity using linear regression models. In complementary models, the effect of memory performance on the relationship between gait velocity and regional volumes was evaluated.

Results

Slower gait velocity was associated with smaller cortical GM and total hippocampal volumes. There was no association between gait velocity and WM or VV. Among hippocampal subfields, only smaller presubiculum volume was significantly associated with decrease in gait velocity. Addition of the memory performance to the models attenuated the association between gait velocity and all volumetric measures.

Conclusions

Our findings indicate that total GM and hippocampal volumes as well as specific hippocampal subfield volumes are inversely associated with locomotor function. These associations are probably affected by cognitive status of study population.

Keywords

Volumetric MRI Gait velocity Cortical volume Hippocampal subfields Memory 

Notes

Acknowledgments

This research was supported by National Institute on Aging Grants AG03949 and AG026728, The Leonard and Sylva Marx Foundation and the Czap Foundation.

Ethical standards and patient consent

We declare that all human studies have been approved by the Albert Einstein College of Medicine Ethics Committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all participants gave informed consent prior to inclusion in this study.

Conflict of interest

We declare that we have no conflict of interest.

References

  1. 1.
    Verghese J, Wang C, Lipton RB, Holtzer R, Xue X (2007) Quantitative gait dysfunction and risk of cognitive decline and dementia. J Neurol Neurosurg Psychiatry 78(9):929–935. doi: 10.1136/jnnp.2006.106914 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Abellan van Kan G, Rolland Y, Andrieu S, Bauer J, Beauchet O, Bonnefoy M, Cesari M, Donini LM, Gillette Guyonnet S, Inzitari M, Nourhashemi F, Onder G, Ritz P, Salva A, Visser M, Vellas B (2009) Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an International Academy on Nutrition and Aging (IANA) Task Force. J Nutr Health Aging 13(10):881–889CrossRefPubMedGoogle Scholar
  3. 3.
    Verghese J, Annweiler C, Ayers E, Barzilai N, Beauchet O, Bennett DA, Bridenbaugh SA, Buchman AS, Callisaya ML, Camicioli R, Capistrant B, Chatterji S, De Cock AM, Ferrucci L, Giladi N, Guralnik JM, Hausdorff JM, Holtzer R, Kim KW, Kowal P, Kressig RW, Lim JY, Lord S, Meguro K, Montero-Odasso M, Muir-Hunter SW, Noone ML, Rochester L, Srikanth V, Wang C (2014) Motoric cognitive risk syndrome: multicountry prevalence and dementia risk. Neurology 83(8):718–726. doi: 10.1212/WNL.0000000000000717 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Kilgour AH, Todd OM, Starr JM (2014) A systematic review of the evidence that brain structure is related to muscle structure and their relationship to brain and muscle function in humans over the lifecourse. BMC Geriatr 14:85. doi: 10.1186/1471-2318-14-85 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34(5):721–733CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    de Laat KF, Reid AT, Grim DC, Evans AC, Kotter R, van Norden AG, de Leeuw FE (2012) Cortical thickness is associated with gait disturbances in cerebral small vessel disease. NeuroImage 59(2):1478–1484. doi: 10.1016/j.neuroimage.2011.08.005 CrossRefPubMedGoogle Scholar
  7. 7.
    Callisaya ML, Beare R, Phan TG, Blizzard L, Thrift AG, Chen J, Srikanth VK (2013) Brain structural change and gait decline: a longitudinal population-based study. J Am Geriatr Soc 61(7):1074–1079. doi: 10.1111/jgs.12331 CrossRefPubMedGoogle Scholar
  8. 8.
    de Laat KF, Tuladhar AM, van Norden AG, Norris DG, Zwiers MP, de Leeuw FE (2011) Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain 134(Pt 1):73–83. doi: 10.1093/brain/awq343 CrossRefPubMedGoogle Scholar
  9. 9.
    Scherder E, Eggermont L, Swaab D, van Heuvelen M, Kamsma Y, de Greef M, van Wijck R, Mulder T (2007) Gait in ageing and associated dementias; its relationship with cognition. Neurosci Biobehav Rev 31(4):485–497. doi: 10.1016/j.neubiorev.2006.11.007 CrossRefPubMedGoogle Scholar
  10. 10.
    Van Petten C (2004) Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia 42(10):1394–1413CrossRefPubMedGoogle Scholar
  11. 11.
    Zimmerman ME, Lipton RB, Pan JW, Hetherington HP, Verghese J (2009) MRI- and MRS-derived hippocampal correlates of quantitative locomotor function in older adults. Brain Res 1291:73–81. doi: 10.1016/j.brainres.2009.07.043 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65(1):7–19. doi: 10.1016/j.neuron.2009.11.031 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Ezzati A, Zimmerman ME, Katz MJ, Sundermann EE, Smith JL, Lipton ML, Lipton RB (2014) Hippocampal subfields differentially correlate with chronic pain in older adults. Brain Res 1573:54–62. doi: 10.1016/j.brainres.2014.05.025 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Elvsashagen T, Westlye LT, Boen E, Hol PK, Andersson S, Andreassen OA, Boye B, Malt UF (2013) Evidence for reduced dentate gyrus and fimbria volume in bipolar II disorder. Bipolar Disord 15(2):167–176. doi: 10.1111/bdi.12046 CrossRefPubMedGoogle Scholar
  15. 15.
    Hanseeuw BJ, Van Leemput K, Kavec M, Grandin C, Seron X, Ivanoiu A (2011) Mild cognitive impairment: differential atrophy in the hippocampal subfields. AJNR Am J Neuroradiol 32(9):1658–1661. doi: 10.3174/ajnr.A2589 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Wang Z, Neylan TC, Mueller SG, Lenoci M, Truran D, Marmar CR, Weiner MW, Schuff N (2010) Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Arch Gen Psychiatry 67(3):296–303. doi: 10.1001/archgenpsychiatry.2009.205 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ferguson GD, Anagnostaras SG, Silva AJ, Herschman HR (2000) Deficits in memory and motor performance in synaptotagmin IV mutant mice. Proc Natl Acad Sci U S A 97(10):5598–5603. doi: 10.1073/pnas.100104597 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Sams-Dodd F, Lipska BK, Weinberger DR (1997) Neonatal lesions of the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood. Psychopharmacology 132(3):303–310CrossRefPubMedGoogle Scholar
  19. 19.
    Katz MJ, Lipton RB, Hall CB, Zimmerman ME, Sanders AE, Verghese J, Dickson DW, Derby CA (2012) Age-specific and sex-specific prevalence and incidence of mild cognitive impairment, dementia, and alzheimer dementia in blacks and whites: a report from the Einstein aging study. Alzheimer Dis Assoc Disord 26(4):335–343. doi: 10.1097/WAD.0b013e31823dbcfc CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Verghese J, Katz MJ, Derby CA, Kuslansky G, Hall CB, Lipton RB (2004) Reliability and validity of a telephone-based mobility assessment questionnaire. Age Ageing 33(6):628–632. doi: 10.1093/ageing/afh210 CrossRefPubMedGoogle Scholar
  21. 21.
    Prince F, Corriveau H, Hébert R, Winter DA (1997) Gait in the elderly. Gait Posture 5(2):128–135CrossRefGoogle Scholar
  22. 22.
    Buschke H (1984) Cued recall in amnesia. J Clin Neuropsychol 6(4):433–440CrossRefPubMedGoogle Scholar
  23. 23.
    American Psychiatric Association., American Psychiatric Association. Task Force on DSM-IV (2000) Diagnostic and statistical manual of mental disorders : DSM-IV-TR, 4th edn. American Psychiatric Association, WashingtonGoogle Scholar
  24. 24.
    Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355CrossRefPubMedGoogle Scholar
  25. 25.
    Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, Snyder AZ (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(2):724–738. doi: 10.1016/j.neuroimage.2004.06.018 CrossRefPubMedGoogle Scholar
  26. 26.
    Van Leemput K, Bakkour A, Benner T, Wiggins G, Wald LL, Augustinack J, Dickerson BC, Golland P, Fischl B (2009) Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 19(6):549–557. doi: 10.1002/hipo.20615 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Krogsrud SK, Tamnes CK, Fjell AM, Amlien I, Grydeland H, Sulutvedt U, Due-Tonnessen P, Bjornerud A, Solsnes AE, Haberg AK, Skrane J, Walhovd KB (2014) Development of hippocampal subfield volumes from 4 to 22 years. Hum Brain Mapp. doi: 10.1002/hbm.22576 PubMedGoogle Scholar
  28. 28.
    Šidák Z (1967) Rectangular confidence regions for the means of multivariate normal distributions. J Am Stat Assoc 62(318):626–633Google Scholar
  29. 29.
    Rosano C, Aizenstein HJ, Studenski S, Newman AB (2007) A regions-of-interest volumetric analysis of mobility limitations in community-dwelling older adults. J Gerontol A: Biol Med Sci 62(9):1048–1055CrossRefGoogle Scholar
  30. 30.
    Rosano C, Aizenstein H, Brach J, Longenberger A, Studenski S, Newman AB (2008) Special article: gait measures indicate underlying focal gray matter atrophy in the brain of older adults. J Gerontol A: Biol Med Sci 63(12):1380–1388CrossRefGoogle Scholar
  31. 31.
    Buschke H, Kuslansky G, Katz M, Stewart WF, Sliwinski MJ, Eckholdt HM, Lipton RB (1999) Screening for dementia with the memory impairment screen. Neurology 52(2):231–238CrossRefPubMedGoogle Scholar
  32. 32.
    Bradley W, Quencer R (1999) Hydrocephalus and cerebrospinal fluid flow. Magnetic resonance imaging, 3rd edn. Mosby, St Louis, pp 1483–1508Google Scholar
  33. 33.
    Longstreth WT Jr, Arnold AM, Manolio TA, Burke GL, Bryan N, Jungreis CA, O’Leary D, Enright PL, Fried L (2000) Clinical correlates of ventricular and sulcal size on cranial magnetic resonance imaging of 3,301 elderly people. The cardiovascular health study. Neuroepidemiology 19(1):30–42CrossRefPubMedGoogle Scholar
  34. 34.
    Annweiler C, Beauchet O, Bartha R, Montero-Odasso M, Knowledge WT-WgA-Lf (2013) Slow gait in MCI is associated with ventricular enlargement: results from the gait and brain study. J Neural Transm 120(7):1083–1092. doi: 10.1007/s00702-012-0926-4 CrossRefPubMedGoogle Scholar
  35. 35.
    Camicioli R, Moore MM, Sexton G, Howieson DB, Kaye JA (1999) Age-related brain changes associated with motor function in healthy older people. J Am Geriatr Soc 47(3):330–334CrossRefPubMedGoogle Scholar
  36. 36.
    Rosano C, Kuller LH, Chung H, Arnold AM, Longstreth WT Jr, Newman AB (2005) Subclinical brain magnetic resonance imaging abnormalities predict physical functional decline in high-functioning older adults. J Am Geriatr Soc 53(4):649–654. doi: 10.1111/j.1532-5415.2005.53214.x CrossRefPubMedGoogle Scholar
  37. 37.
    Beauchet O, Launay CP, Annweiler C, Allali G (2015) Hippocampal volume, early cognitive decline and gait variability: which association? Exp Gerontol 61:98–104. doi: 10.1016/j.exger.2014.11.002 CrossRefPubMedGoogle Scholar
  38. 38.
    Rosso AL, Olson Hunt MJ, Yang M, Brach JS, Harris TB, Newman AB, Satterfield S, Studenski SA, Yaffe K, Aizenstein HJ, Rosano C, Health ABCs (2014) Higher step length variability indicates lower gray matter integrity of selected regions in older adults. Gait Posture 40(1):225–230. doi: 10.1016/j.gaitpost.2014.03.192 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Annweiler C, Montero-Odasso M, Bartha R, Drozd J, Hachinski V, Beauchet O (2014) Association between gait variability and brain ventricle attributes: a brain mapping study. Exp Gerontol 57:256–263. doi: 10.1016/j.exger.2014.06.015 CrossRefPubMedGoogle Scholar
  40. 40.
    Shi F, Liu B, Zhou Y, Yu C, Jiang T (2009) Hippocampal volume and asymmetry in mild cognitive impairment and Alzheimer’s disease: meta-analyses of MRI studies. Hippocampus 19(11):1055–1064. doi: 10.1002/hipo.20573 CrossRefPubMedGoogle Scholar
  41. 41.
    Jahn K, Deutschlander A, Stephan T, Strupp M, Wiesmann M, Brandt T (2004) Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. NeuroImage 22(4):1722–1731. doi: 10.1016/j.neuroimage.2004.05.017 CrossRefPubMedGoogle Scholar
  42. 42.
    Lafleur MF, Jackson PL, Malouin F, Richards CL, Evans AC, Doyon J (2002) Motor learning produces parallel dynamic functional changes during the execution and imagination of sequential foot movements. NeuroImage 16(1):142–157. doi: 10.1006/nimg.2001.1048 CrossRefPubMedGoogle Scholar
  43. 43.
    Igloi K, Doeller CF, Berthoz A, Rondi-Reig L, Burgess N (2010) Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proc Natl Acad Sci U S A 107(32):14466–14471. doi: 10.1073/pnas.1004243107 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Nedelska Z, Andel R, Laczo J, Vlcek K, Horinek D, Lisy J, Sheardova K, Bures J, Hort J (2012) Spatial navigation impairment is proportional to right hippocampal volume. Proc Natl Acad Sci U S A 109(7):2590–2594. doi: 10.1073/pnas.1121588109 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Arque G, de Lagran MM, Arbones ML, Dierssen M (2009) Age-associated motor and visuo-spatial learning phenotype in Dyrk1A heterozygous mutant mice. Neurobiol Dis 36(2):312–319. doi: 10.1016/j.nbd.2009.07.027 CrossRefPubMedGoogle Scholar
  46. 46.
    Leung LS, Shen B, Rajakumar N, Ma J (2003) Cholinergic activity enhances hippocampal long-term potentiation in CA1 during walking in rats. J Neurosci Off J Soc Neurosci 23(28):9297–9304Google Scholar
  47. 47.
    Pereira JB, Junque C, Bartres-Faz D, Ramirez-Ruiz B, Marti MJ, Tolosa E (2013) Regional vulnerability of hippocampal subfields and memory deficits in Parkinson’s disease. Hippocampus 23(8):720–728. doi: 10.1002/hipo.22131 CrossRefPubMedGoogle Scholar
  48. 48.
    Liu MG, Chen J (2009) Roles of the hippocampal formation in pain information processing. Neurosci Bull 25(5):237–266. doi: 10.1007/s12264-009-0905-4 CrossRefPubMedGoogle Scholar
  49. 49.
    Henke PG (1982) The telencephalic limbic system and experimental gastric pathology: a review. Neurosci Biobehav Rev 6(3):381–390CrossRefPubMedGoogle Scholar
  50. 50.
    Meibach RC, Siegel A (1977) Efferent connections of the hippocampal formation in the rat. Brain Res 124(2):197–224CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ali Ezzati
    • 1
    • 2
    Email author
  • Mindy J. Katz
    • 1
  • Michael L. Lipton
    • 3
    • 4
  • Richard B. Lipton
    • 1
    • 5
  • Joe Verghese
    • 1
    • 6
  1. 1.Saul B. Korey Department of NeurologyAlbert Einstein College of Medicine of Yeshiva UniversityBronxUSA
  2. 2.Department of NeurologyMontefiore Medical CenterBronxUSA
  3. 3.The Gruss Magnetic Resonance Research Center and Departments of Radiology, Psychiatry and Behavioral Sciences and the Dominick P. Purpura Department of NeuroscienceAlbert Einstein College of Medicine of Yeshiva UniversityBronxUSA
  4. 4.The Department of RadiologyMontefiore Medical CenterBronxUSA
  5. 5.Department of Epidemiology and Population HealthAlbert Einstein College of Medicine of Yeshiva UniversityBronxUSA
  6. 6.Division of Cognitive & Motor AgingAlbert Einstein College of MedicineBronxUSA

Personalised recommendations