Deactivation of somatosensory and visual cortices during vestibular stimulation is associated with older age and poorer balance
Autoři:
Fatemeh Noohi aff001; Catherine Kinnaird aff003; Yiri De Dios aff004; Igor Kofman aff004; Scott J. Wood aff005; Jacob J. Bloomberg aff005; Ajitkumar P. Mulavara aff004; Kathleen H. Sienko aff003; Thad A. Polk aff002; Rachael D. Seidler aff006
Působiště autorů:
Department of Kinesiology, University of Michigan, Ann Arbor, MI, United States of America
aff001; Department of Psychology, University of Michigan, Ann Arbor, MI, United States of America
aff002; Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI, United States of America
aff003; KBRwyle, Houston, TX, United States of America
aff004; NASA Johnson Space Center, Houston, TX, United States of America
aff005; Department of Applied Physiology & Kinesiology, University of Florida, Gainesville, FL, United States of America
aff006
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0221954
Souhrn
Aging is associated with peripheral and central declines in vestibular processing and postural control. Here we used functional MRI to investigate age differences in neural vestibular representations in response to pneumatic tap stimulation. We also measured the amount of body sway in multiple balance tasks outside of the MRI scanner to assess the relationship between individuals’ balance ability and their vestibular neural response. We found a general pattern of activation in canonical vestibular cortex and deactivation in cross modal sensory regions in response to vestibular stimulation. We found that activation amplitude of the vestibular cortex was correlated with age, with younger individuals exhibiting higher activation. Deactivation of visual and somatosensory regions increased with age and was associated with poorer balance. The results demonstrate that brain activations and deactivations in response to vestibular stimuli are correlated with balance, and the pattern of these correlations varies with age. The findings also suggest that older adults exhibit less sensitivity to vestibular stimuli, and may compensate by differentially reweighting visual and somatosensory processes.
Klíčová slova:
Biology and life sciences – Physical sciences – Research and analysis methods – Neuroscience – Cognitive science – Psychology – Social sciences – People and places – Population groupings – Mathematics – Medicine and health sciences – Physiology – Diagnostic medicine – Cognitive neuroscience – Age groups – Imaging techniques – Brain mapping – Functional magnetic resonance imaging – Neuroimaging – Diagnostic radiology – Magnetic resonance imaging – Radiology and imaging – Elderly – Sensory perception – Vision – Young adults – Biological locomotion – Geometry – Motor reactions – Postural control – Gait analysis – Ellipses
Zdroje
1. Sturnieks DL., St George R, Lord SR.. Balance disorders in the elderly. Neurophysiol Clin. 2008;38: 467–478. doi: 10.1016/j.neucli.2008.09.001 19026966
2. Zalewski CK. Aging of the Human Vestibular System Balance Function and The Role of The Vestibular System Epidemiology of Dizziness. 2015;
3. Allen D, Ribeiro L, Arshad Q, Seemungal BM. Age-Related Vestibular Loss: Current Understanding and Future Research Directions. Front Neurol. 2016;7: 231. doi: 10.3389/fneur.2016.00231 28066316
4. Smith PF. Age-Related Neurochemical Changes in the Vestibular Nuclei. Front Neurol. 2016;7: 20. doi: 10.3389/fneur.2016.00020 26973593
5. Matheson AJ, Darlington CL, Smith PF. Dizziness in the Elderly and Age-related Degeneration of the Vestibular System. New Zealand Journal of Psychology. 1999. pp. 10–16. 11543297
6. Lopez I, Honrubia V, Baloh RW. Aging and the Human Vestibular Nucleus. J Vestib Res. 1997;
7. Schlindwein P, Mueller M, Bauermann T, Brandt T, Stoeter P, Dieterich M. Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. Neuroimage. 2008;39: 19–31. doi: 10.1016/j.neuroimage.2007.08.016 17919936
8. Zu Eulenburg P, Caspers S, Roski C, Eickhoff SB. Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage. 2012;60: 162–169. doi: 10.1016/j.neuroimage.2011.12.032 22209784
9. Lopez C, Blanke O, Mast FW. The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience. 2012;212: 159–79. doi: 10.1016/j.neuroscience.2012.03.028 22516007
10. Karim HT, Sparto PJ, Aizenstein HJ, Furman JM, Huppert TJ, Erickson KI, et al. Functional MR imaging of a simulated balance task. Brain Res. 2014;1555: 20–27. doi: 10.1016/j.brainres.2014.01.033 24480476
11. Karim HT, Fuhrman SI, Furman JM, Huppert TJ. Neuroimaging to detect cortical projection of vestibular response to caloric stimulation in young and older adults using functional near-infrared spectroscopy (fNIRS). Neuroimage. 2013;76: 1–10. doi: 10.1016/j.neuroimage.2013.02.061 23523804
12. Lin C-C, Barker JW, Sparto PJ, Furman JM, Huppert TJ. Functional near-infrared spectroscopy (fNIRS) brain imaging of multi-sensory integration during computerized dynamic posturography in middle-aged and older adults. Exp Brain Res. 2017;235: 1247–1256. doi: 10.1007/s00221-017-4893-8 28197672
13. Cyran CAM, Boegle R, Stephan T, Dieterich M, Glasauer S. Age-related decline in functional connectivity of the vestibular cortical network. Brain Struct Funct. 2016;221: 1443–1463. doi: 10.1007/s00429-014-0983-6 25567421
14. Sullivan E V, Rose J, Rohlfing T, Pfefferbaum A. Postural sway reduction in aging men and women: relation to brain structure, cognitive status, and stabilizing factors. Neurobiol Aging. 2009;30: 793–807. doi: 10.1016/j.neurobiolaging.2007.08.021 17920729
15. Impe A Van, Coxon JP, Goble DJ, Doumas M, Swinnen SP. White matter fractional anisotropy predicts balance performance in older adults. NBA. 2012;33: 1900–1912. doi: 10.1016/j.neurobiolaging.2011.06.013
16. Yuan J, Blumen HM, Verghese J, Holtzer R. Functional connectivity associated with gait velocity during walking and walking-while-talking in aging: A resting-state fMRI study. Hum Brain Mapp. 2015;36: 1484–1493. doi: 10.1002/hbm.22717 25504964
17. Reuter-Lorenz PA, Cappell KA. Neurocognitive Aging and the Compensation Hypothesis. Curr Dir Psychol Sci. 2008;17: 177–182. doi: 10.1111/j.1467-8721.2008.00570.x
18. Reuter-Lorenz PA, Park DC. Human Neuroscience and the Aging Mind: A New Look at Old Problems. Journals Gerontol Ser B Psychol Sci Soc Sci. 2010;65B: 405–415. doi: 10.1093/geronb/gbq035 20478901
19. Heuninckx S, Wenderoth N, Swinnen SP. Systems Neuroplasticity in the Aging Brain: Recruiting Additional Neural Resources for Successful Motor Performance in Elderly Persons. J Neurosci. 2008;28: 91–99. doi: 10.1523/JNEUROSCI.3300-07.2008 18171926
20. Eyler LT, Sherzai A, Kaup AR, Jeste D V. A review of functional brain imaging correlates of successful cognitive aging. Biol Psychiatry. 2011;70: 115–122. doi: 10.1016/j.biopsych.2010.12.032 21316037
21. Li HJ, Hou XH, Liu HH, Yue CL, Lu GM, Zuo XN. Putting age-related task activation into large-scale brain networks: A meta-analysis of 114 fMRI studies on healthy aging. Neurosci Biobehav Rev. 2015;57: 156–174. doi: 10.1016/j.neubiorev.2015.08.013 26318367
22. Cabeza R, Anderson ND, Locantore JK, McIntosh AR. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage. 2002;17: 1394–402. Available: http://www.ncbi.nlm.nih.gov/pubmed/12414279 12414279
23. Seidler RD, Bernard J a, Burutolu TB, Fling BW, Gordon MT, Gwin JT, et al. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 2010;34: 721–33. doi: 10.1016/j.neubiorev.2009.10.005 19850077
24. Noohi F, Kinnaird C, DeDios Y, Kofman IS, Wood S, Bloomberg J, et al. Functional brain activation in response to a clinical vestibular test correlates with balance. Front Syst Neurosci. 2017;11. doi: 10.3389/fnsys.2017.00011 28344549
25. Furman JM, Redfern MS. Effect of aging on the otolith-ocular reflex. J Vestib Res. 2001;
26. Nasreddine ZS, Phillips NA, BÃdirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment. J Am Geriatr Soc. 2005;53: 695–699. doi: 10.1111/j.1532-5415.2005.53221.x 15817019
27. Sienko K, Oddsson L, Wall C. Effects of multi-directional vibrotactile feedback on vestibular-deficient postural performance during continuous multi-directional support surface perturbations. J Vestib Res. 2008;18: 273–285. Available: https://pdfs.semanticscholar.org/c508/720d0a90c2c9d725b4061c07a2ef816bc864.pdf 19542601
28. Jayakaran P, Johnson GM, Sullivan SJ. Concurrent validity of the Sensory Organization Test measures in unilateral transtibial amputees. Prosthet Orthot Int. 2013;37: 65–69. doi: 10.1177/0309364612448391 22760518
29. Ruhe A, Fejer R, Walker B. The test-retest reliability of centre of pressure measures in bipedal static task conditions—A systematic review of the literature. Gait Posture. 2010;32: 436–445. doi: 10.1016/j.gaitpost.2010.09.012 20947353
30. Bloem BR, Grimbergen YAM, Cramer M, Willemsen M, Zwinderman AH. Prospective assessment of falls in Parkinson’s disease. J Neurol. 2001;248: 950–958. doi: 10.1007/s004150170047 11757958
31. Chun-Ju Chang C-J, Yu-Shin Chang Y-S, Sai-Wei Yang S-W. Using single leg standing time to predict the fall risk in elderly. 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). IEEE; 2013. pp. 7456–7458. doi:10.1109/EMBC.2013.6611282
32. Maki BE, Holliday PJ, Topper AK. A prospective study of postural balance and risk of falling in an ambulatory and independent elderly population. J Gerontol. 1994;49: M72–84. Available: http://www.ncbi.nlm.nih.gov/pubmed/8126355 8126355
33. Matsuda PN, Taylor CS, Shumway-Cook A. Evidence for the Validity of the Modified Dynamic Gait Index Across Diagnostic Groups. Phys Ther. 2014;94: 996–1004. doi: 10.2522/ptj.20130294 24557650
34. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther. 2000;80: 896–903. Available: http://www.ncbi.nlm.nih.gov/pubmed/10960937 10960937
35. Huang S-L, Hsieh C-L, Wu R-M, Tai C-H, Lin C-H, Lu W-S. Minimal Detectable Change of the Timed “Up & Go” Test and the Dynamic Gait Index in People With Parkinson Disease. Phys Ther. 2011;91: 114–121. doi: 10.2522/ptj.20090126 20947672
36. Podsiadlo D, Richardson S. The timed "Up & Go": a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39: 142–8. Available: http://www.ncbi.nlm.nih.gov/pubmed/1991946 1991946
37. Shumway-Cook A, Taylor CS, Matsuda PN, Studer MT, Whetten BK. Expanding the Scoring System for the Dynamic Gait Index. Phys Ther. 2013;93: 1493–1506. doi: 10.2522/ptj.20130035 23813090
38. Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med. 2000;44: 162–7. Available: http://www.ncbi.nlm.nih.gov/pubmed/10893535 10893535
39. Cornell ED, Burgess AM, MacDougall HG, Curthoys IS. Vertical and horizontal eye movement responses to unilateral and bilateral bone conducted vibration to the mastoid. J Vestib Res. 2009;19: 41–47. doi: 10.3233/VES-2009-0338 19893196
40. Curthoys IS, Vulovic V, Burgess AM, Cornell ED, Mezey LE, Macdougall HG, et al. The basis for using bone-conducted vibration or air-conducted sound to test otolithic function. Ann N Y Acad Sci. 2011;1233: 231–241. doi: 10.1111/j.1749-6632.2011.06147.x 21950999
41. Curthoys IS, Kim J, McPhedran SK, Camp AJ. Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig. Exp Brain Res. 2006;175: 256–267. doi: 10.1007/s00221-006-0544-1 16761136
42. Curthoys IS, Burgess AM, MacDougall HG, McGarvie LA, Halmagyi GM, Smulders YE, et al. Testing human otolith function using bone-conducted vibration. Ann N Y Acad Sci. 2009;1164: 344–346. doi: 10.1111/j.1749-6632.2008.03728.x 19645924
43. Iwasaki S, Smulders YE, Burgess AM, McGarvie LA, Macdougall HG, Halmagyi GM, et al. Ocular vestibular evoked myogenic potentials to bone conducted vibration of the midline forehead at Fz in healthy subjects. Clin Neurophysiol. 2008;119: 2135–47. doi: 10.1016/j.clinph.2008.05.028 18639490
44. Nguyen KD, Welgampola MS, Carey JP. Test-retest reliability and age-related characteristics of the ocular and cervical vestibular evoked myogenic potential tests. Otol Neurotol. 2010;31: 793–802. doi: 10.1097/MAO.0b013e3181e3d60e 20517167
45. Wackym PA, Ratigan JA, Birck JD, Johnson SH, Doornink J, Bottlang M, et al. Rapid cVEMP and oVEMP responses elicited by a novel head striker and recording device. Otol Neurotol. 2012;33: 1392–400. doi: 10.1097/MAO.0b013e318268d234 22935811
46. Lee B-C, Kim J, Chen S, Sienko KH. Cell phone based balance trainer. J Neuroeng Rehabil. 2012;9: 10. doi: 10.1186/1743-0003-9-10 22316167
47. Sienko K, Oddsson L, Wall C. Effects of multi-directional vibrotactile feedback on vestibular-deficient postural performance during continuous multi-directional support surface perturbations. J Vestib Res. 2008;18: 273–285. 19542601
48. Friston KJ, Ashburner J, Frith CD, Poline J-B, Heather JD, Frackowiak RSJ. Spatial registration and normalization of images. Hum Brain Mapp. 1995;3: 165–189. doi: 10.1002/hbm.460030303
49. NITRC: Artifact Detection Tools (ART): Tool/Resource Info [Internet]. [cited 6 Jan 2018]. Available: https://www.nitrc.org/projects/artifact_detect/
50. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage. 2009;46: 39–46. doi: 10.1016/j.neuroimage.2009.01.045 19457380
51. Diedrichsen J, Zotow E. Surface-Based Display of Volume-Averaged Cerebellar Imaging Data. PLoS One. 2015;10: e0133402. doi: 10.1371/journal.pone.0133402 26230510
52. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage. 2006;33: 127–138. doi: 10.1016/j.neuroimage.2006.05.056 16904911
53. Diedrichsen J, Maderwald S, Küper M, Thürling M, Rabe K, Gizewski ER, et al. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage. 2011;54: 1786–94. doi: 10.1016/j.neuroimage.2010.10.035 20965257
54. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 2002;15: 1–25. Available: http://www.ncbi.nlm.nih.gov/pubmed/11747097 11747097
55. BSPMVIEW | bspmview [Internet]. [cited 6 Jan 2018]. Available: http://www.bobspunt.com/bspmview/
56. Bernard JA, Peltier SJ, Wiggins JL, Jaeggi SM, Buschkuehl M, Fling BW, et al. Disrupted cortico-cerebellar connectivity in older adults. Neuroimage. 2013;83: 103–19. doi: 10.1016/j.neuroimage.2013.06.042 23792980
57. Wilke M, Schmithorst VJ. A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data. Neuroimage. 2006;33: 522–530. doi: 10.1016/J.NEUROIMAGE.2006.07.010 16938470
58. Wilke M, Lidzba K. LI-tool: A new toolbox to assess lateralization in functional MR-data. J Neurosci Methods. 2007;163: 128–136. doi: 10.1016/J.JNEUMETH.2007.01.026 17386945
59. Pascual B, Masdeu JC, Hollenbeck M, Makris N, Insausti R, Ding SL, et al. Large-scale brain networks of the human left temporal pole: A functional connectivity MRI study. Cereb Cortex. 2015;25: 680–702. doi: 10.1093/cercor/bht260 24068551
60. Brandt T, Glasauer S, Stephan T, Bense S, Yousry T a, Deutschlander A, et al. Visual-vestibular and visuovisual cortical interaction: new insights from fMRI and pet. Ann N Y Acad Sci. 2002;956: 230–241. doi: 10.1111/j.1749-6632.2002.tb02822.x 11960807
61. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M. Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol. 2001;85: 886–899. Available: http://www.ncbi.nlm.nih.gov/pubmed/11160520 11160520
62. Deutschländer A, Bense S, Stephan T, Schwaiger M, Brandt T, Dieterich M. Sensory system interactions during simultaneous vestibular and visual stimulation in PET. Hum Brain Mapp. 2002;16: 92–103. doi: 10.1002/hbm.10030 11954059
63. Laurienti PJ, Burdette JH, Wallace MT, Yen Y-F, Field AS, Stein BE. Deactivation of Sensory-Specific Cortex by Cross-Modal Stimuli. J Cogn Neurosci. 2002;14: 420–429. doi: 10.1162/089892902317361930 11970801
64. Uludağ K, Dubowitz DJ, Yoder EJ, Restom K, Liu TT, Buxton RB. Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. Neuroimage. 2004;23: 148–155. doi: 10.1016/J.NEUROIMAGE.2004.05.013 15325361
65. Costello MC, Bloesch EK. Are Older Adults Less Embodied? A Review of Age Effects through the Lens of Embodied Cognition. Front Psychol. 2017;8: 267. doi: 10.3389/fpsyg.2017.00267 28289397
66. Anson E, Bigelow RT, Swenor B, Deshpande N, Studenski S, Jeka JJ, et al. Loss of Peripheral Sensory Function Explains Much of the Increase in Postural Sway in Healthy Older Adults. Front Aging Neurosci. 2017;9: 202. doi: 10.3389/fnagi.2017.00202 28676758
67. Pasma JH, Engelhart D, Maier AB, Schouten AC, van der Kooij H, Meskers CGM. Changes in sensory reweighting of proprioceptive information during standing balance with age and disease. J Neurophysiol. 2015;114: 3220–33. doi: 10.1152/jn.00414.2015 26424578
68. Wiesmeier IK, Dalin D, Wehrle A, Granacher U, Muehlbauer T, Dietterle J, et al. Balance Training Enhances Vestibular Function and Reduces Overactive Proprioceptive Feedback in Elderly. Front Aging Neurosci. 2017;9: 273. doi: 10.3389/fnagi.2017.00273 28848430
69. Bao T, Carender WJ, Kinnaird C, Barone VJ, Peethambaran G, Whitney SL, et al. Effects of long-term balance training with vibrotactile sensory augmentation among community-dwelling healthy older adults: a randomized preliminary study. J Neuroeng Rehabil. 2018;15: 5. doi: 10.1186/s12984-017-0339-6 29347946
70. Nelson-Wong E, Appell R, McKay M, Nawaz H, Roth J, Sigler R, et al. Increased fall risk is associated with elevated co-contraction about the ankle during static balance challenges in older adults. Eur J Appl Physiol. 2012;112: 1379–1389. doi: 10.1007/s00421-011-2094-x 21811766
71. Kannurpatti SS, Motes MA, Rypma B, Biswal BB. Neural and vascular variability and the fMRI-BOLD response in normal aging. Magn Reson Imaging. 2010;28: 466–476. doi: 10.1016/j.mri.2009.12.007 20117893
72. Hesselmann V, Zaro Weber O, Wedekind C, Krings T, Schulte O, Kugel H, et al. Age related signal decrease in functional magnetic resonance imaging during motor stimulation in humans. Neurosci Lett. 2001;308: 141–144. doi: 10.1016/S0304-3940(01)01920-6 11479008
73. Bürki CN, Bridenbaugh SA, Reinhardt J, Stippich C, Kressig RW, Blatow M. Imaging gait analysis: An fMRI dual task study. Brain Behav. 2017;7: 1–13. doi: 10.1002/brb3.724 28828204
74. Donath L, Kurz E, Roth R, Zahner L, Faude O. Different ankle muscle coordination patterns and co-activation during quiet stance between young adults and seniors do not change after a bout of high intensity training. BMC Geriatr. 2015;15: 1–8. doi: 10.1186/1471-2318-15-1 25559550
75. Centers for Disease Control & Prevention [Internet]. Available: https://www.cdc.gov/homeandrecreationalsafety/falls/adultfalls.html
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania