pp 1–12 | Cite as

The effect of fear of falling on prefrontal cortex activation and efficiency during walking in older adults

  • Roee HoltzerEmail author
  • Rebecca Kraut
  • Meltem Izzetoglu
  • Kenny Ye
Original Article


Neural inefficiency is inferred when higher brain activations are associated with similar or worse performance. Improved neural efficiency is achieved when task-related brain activations are reduced after practice. No information is available on the effect of fear-of-falling (FOF) on brain activation during walking. We hypothesized that the presence of FOF would be associated with neural inefficiency and with a delay in improving neural efficiency during dual-task walking. Task conditions included single-task walk (STW), Alpha (cognitive interference), and dual-task walk (DTW). Functional near-infrared spectroscopy (fNIRS)-derived HbO2 in the prefrontal cortex (PFC) was used to quantify task-related changes in brain activation. Practice included three repeated counterbalanced trials for each task. Participants with FOF (n = 19; mean age = 79.84 ± 6.01 years; %female = 68.42) and without FOF (n = 56; mean age = 76.73 ± 6.39 years; %female = 44.64) were included. The presence of FOF was associated with slower stride velocity (estimate = − 12.354; p = 0.0154) and with greater increases in PFC HbO2 from STW to DTW (estimate = 0.303, p = 0.0009) and from Alpha to DTW (estimate = 0.387, p < 0.0001). Compared to controls, participants reporting FOF demonstrated an attenuated decline in PFC HbO2 from the first to the second DTW trials (estimate = 0.264; p = 0.0173). In contrast, compared to controls, participants with FOF demonstrated greater decline in Alpha PFC HbO2 from trial 1 to trial 2 (estimate = − 0.419, p < 0.0001) and from trial 1 to 3 (estimate = − 0.281, p = 0.0006). The change in PFC HbO2 over repeated STW trials was not significant and was not moderated by FOF status. The presence of FOF was associated with higher and inefficient PFC activation during DTW in older adults.


Fear-of-falling Dual-task walking Prefrontal cortex, neural efficiency, functional-near-infrared spectroscopy 


Funding information

This research was supported by the National Institutes on Aging grants (R01AG036921, R01AG044007).

Compliance with ethical standards

The study was in compliance with the Code of Ethics of the World Medical Association (Declaration of Helsinki). Participants signed written informed consents in the first in-person study visit. The Institutional Review Board approved this study.

Conflicts of interest

Dr. Izzetoglu has a very minor share in the company that manufactures the fNIRS device used in this study. All other authors have no conflicts of interest to report in relation to the current article.

Supplementary material

11357_2019_56_MOESM1_ESM.docx (28 kb)
ESM 1 (DOCX 28 kb)


  1. Albinet CT, Mandrick K, Bernard PL, Perrey S, Blain H (2014) Improved cerebral oxygenation response and executive performance as a function of cardiorespiratory fitness in older women: a fNIRS study. Front Aging Neurosci 6:272. CrossRefGoogle Scholar
  2. Arfken CL, Lach HW, Birge SJ, Miller JP (1994) The prevalence and correlates of fear of falling in elderly persons living in the community. Am J Public Health 84(4):565–570CrossRefGoogle Scholar
  3. Ayaz H, Izzetoglu M, Platek SM, Bunce S, Izzetoglu K, Pourrezaei K, Onaral B (2006) Registering fNIR data to brain surface image using MRI templates. Conf Proc IEEE Eng Med Biol Soc 1:2671–2674. CrossRefGoogle Scholar
  4. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using. J Stat Softw 67(1):1–48.
  5. Beck AT, Epstein N, Brown G, Steer RA (1988) An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 56(6):893–897CrossRefGoogle Scholar
  6. Bruce DG, Devine A, Prince RL (2002) Recreational physical activity levels in healthy older women: the importance of fear of falling. J Am Geriatr Soc 50(1):84–89CrossRefGoogle Scholar
  7. Chen M, Blumen HM, Izzetoglu M, Holtzer R (2017) Spatial coregistration of functional near-infrared spectroscopy to brain MRI. J Neuroimaging 27(5):453–460. CrossRefGoogle Scholar
  8. Cumming RG, Salkeld G, Thomas M, Szonyi G (2000) Prospective study of the impact of fear of falling on activities of daily living, SF-36 scores, and nursing home admission. J Gerontol A Biol Sci Med Sci 55(5):M299–M305CrossRefGoogle Scholar
  9. Daselaar SM, Iyengar V, Davis SW, Eklund K, Hayes SM, Cabeza RE (2015) Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity. Cereb Cortex 25(4):983–990. CrossRefGoogle Scholar
  10. Delbaere K, Crombez G, Vanderstraeten G, Willems T, Cambier D (2004) Fear-related avoidance of activities, falls and physical frailty. A prospective community-based cohort study. Age Ageing 33(4):368–373. CrossRefGoogle Scholar
  11. Deshpande N, Metter EJ, Lauretani F, Bandinelli S, Guralnik J, Ferrucci L (2008) Activity restriction induced by fear of falling and objective and subjective measures of physical function: a prospective cohort study. J Am Geriatr Soc 56(4):615–620. CrossRefGoogle Scholar
  12. Donoghue OA, Cronin H, Savva GM, O'Regan C, Kenny RA (2013) Effects of fear of falling and activity restriction on normal and dual task walking in community dwelling older adults. Gait Posture 38(1):120–124. CrossRefGoogle Scholar
  13. Duff K, Humphreys Clark JD, O’Bryant SE, Mold JW, Schiffer RB, Sutker PB (2008) Utility of the RBANS in detecting cognitive impairment associated with Alzheimer’s disease: sensitivity, specificity, and positive and negative predictive powers. Arch Clin Neuropsychol 23(5):603–612. CrossRefGoogle Scholar
  14. England SE, Verghese J, Mahoney JR, Trantzas C, Holtzer R (2015) Three-level rating of turns while walking. Gait Posture 41(1):300–303. CrossRefGoogle Scholar
  15. Friedman SM, Munoz B, West SK, Rubin GS, Fried LP (2002) Falls and fear of falling: which comes first? A longitudinal prediction model suggests strategies for primary and secondary prevention. J Am Geriatr Soc 50(8):1329–1335CrossRefGoogle Scholar
  16. Gage WH, Sleik RJ, Polych MA, McKenzie NC, Brown LA (2003) The allocation of attention during locomotion is altered by anxiety. Exp Brain Res 150(3):385–394. CrossRefGoogle Scholar
  17. Gramigna V, Pellegrino G, Cerasa A, Cutini S, Vasta R, Olivadese G, …, Quattrone A (2017) Near-infrared spectroscopy in gait disorders: is it time to begin? Neurorehabil Neural Repair 31(5):402–412.
  18. Harada T, Miyai I, Suzuki M, Kubota K (2009) Gait capacity affects cortical activation patterns related to speed control in the elderly. Exp Brain Res 193(3):445–454. CrossRefGoogle Scholar
  19. Hayes SM, Hayes JP, Cadden M, Verfaellie M (2013) A review of cardiorespiratory fitness-related neuroplasticity in the aging brain. Front Aging Neurosci 5:31. CrossRefGoogle Scholar
  20. Hernandez ME, Holtzer R, Chaparro G, Jean K, Balto JM, Sandroff BM, …, Motl RW (2016) Brain activation changes during locomotion in middle-aged to older adults with multiple sclerosis. J Neurol Sci 370:277–283. doi:
  21. Holtzer R, Verghese J, Wang C, Hall CB, Lipton RB (2008) Within-person across-neuropsychological test variability and incident dementia. JAMA 300(7):823–830. CrossRefGoogle Scholar
  22. Holtzer R, Mahoney JR, Izzetoglu M, Izzetoglu K, Onaral B, Verghese J (2011) fNIRS Study of Walking and Walking While Talking in Young and Old Individuals. J Gerontol A Biol Sci Med Sci 66(8):879–887. CrossRefGoogle Scholar
  23. Holtzer R, Wang C, Lipton R, Verghese J (2012a) The protective effects of executive functions and episodic memory on gait speed decline in aging defined in the context of cognitive reserve. J Am Geriatr Soc 60(11):2093–2098. CrossRefGoogle Scholar
  24. Holtzer R, Wang C, Verghese J (2012b) The relationship between attention and gait in aging: facts and fallacies. Mot Control 16(1):64–80CrossRefGoogle Scholar
  25. Holtzer R, Mahoney J, Verghese J (2014a) Intraindividual variability in executive functions but not speed of processing or conflict resolution predicts performance differences in gait speed in older adults. J Gerontol A Biol Sci Med Sci 69(8):980–986. CrossRefGoogle Scholar
  26. Holtzer R, Wang C, Verghese J (2014b) Performance variance on walking while talking tasks: theory, findings, and clinical implications. Age (Dordr) 36(1):373–381. CrossRefGoogle Scholar
  27. Holtzer R, Mahoney JR, Izzetoglu M, Wang C, England S, Verghese J (2015) Online fronto-cortical control of simple and attention-demanding locomotion in humans. Neuroimage 112:152–159. CrossRefGoogle Scholar
  28. Holtzer R, Verghese J, Allali G, Izzetoglu M, Wang C, Mahoney JR (2016a) Neurological gait abnormalities moderate the functional brain signature of the posture first hypothesis. Brain Topogr 29(2):334–343.
  29. Holtzer R, Yuan J, Verghese J, Mahoney JR, Izzetoglu M, Wang C (2016b) Interactions of subjective and objective measures of fatigue defined in the context of brain control of locomotion. J Gerontol A Biol Sci Med Sci:glw167.
  30. Holtzer R, Schoen C, Demetriou E, Mahoney JR, Izzetoglu M, Wang C, Verghese J (2017) Stress and gender effects on prefrontal cortex oxygenation levels assessed during single and dual-task walking conditions. Eur J Neurosci 45(5):660–670. CrossRefGoogle Scholar
  31. Holtzer R, George CJ, Izzetoglu M, Wang C (2018a) The effect of diabetes on prefrontal cortex activation patterns during active walking in older adults. Brain Cogn 125:14–22. CrossRefGoogle Scholar
  32. Holtzer R, Izzetoglu M, Chen M, Wang C (2018b) Distinct fNIRS-derived HbO2 trajectories during the course and over repeated walking trials under single and dual-task conditions: implications for within session learning and prefrontal cortex efficiency in older adults. J Gerontol A Biol Sci Med Sci.
  33. Howland J, Lachman ME, Peterson EW, Cote J, Kasten L, Jette A (1998) Covariates of fear of falling and associated activity curtailment. Gerontologist 38(5):549–555CrossRefGoogle Scholar
  34. Izzetoglu M, Devaraj A, Bunce S, Onaral B (2005) Motion artifact cancellation in NIR spectroscopy using Wiener filtering. IEEE Trans Biomed Eng 52(5):934–938. CrossRefGoogle Scholar
  35. Lach HW, Parsons JL (2013) Impact of fear of falling in long term care: an integrative review. J Am Med Dir Assoc 14(8):573–577. CrossRefGoogle Scholar
  36. Li KZ, Lindenberger U, Freund AM, Baltes PB (2001) Walking while memorizing: age-related differences in compensatory behavior. Psychol Sci 12(3):230–237CrossRefGoogle Scholar
  37. Litwin H, Erlich B, Dunsky A (2018) The complex association between fear of falling and mobility limitation in relation to late-life falls: a SHARE-based analysis. J Aging Health 30(6):987–1008. CrossRefGoogle Scholar
  38. Lucas M, Wagshul ME, Izzetoglu M, Holtzer R (2018) Moderating effect of white matter integrity on brain activation during dual-task walking in older adults. J Gerontol A Biol Sci Med Sci.
  39. Maidan I, Nieuwhof F, Bernad-Elazari H, Reelick MF, Bloem BR, Giladi N, …, Mirelman A (2016) The role of the frontal lobe in complex walking among patients with Parkinson’s disease and healthy older adults: an fNIRS study. Neurorehabil Neural Repair 30(10):963–971. doi:
  40. Maidan I, Bernad-Elazari H, Giladi N, Hausdorff JM, Mirelman A (2017) When is higher level cognitive control needed for locomotor tasks among patients with Parkinson’s disease? Brain Topogr 30(4):531–538. CrossRefGoogle Scholar
  41. Mihara M, Miyai I, Hatakenaka M, Kubota K, Sakoda S (2007) Sustained prefrontal activation during ataxic gait: a compensatory mechanism for ataxic stroke? Neuroimage 37(4):1338–1345. CrossRefGoogle Scholar
  42. Mihara M, Miyai I, Hatakenaka M, Kubota K, Sakoda S (2008) Role of the prefrontal cortex in human balance control. NeuroImage 43:329–336. CrossRefGoogle Scholar
  43. Mirelman A, Maidan I, Bernad-Elazari H, Shustack S, Giladi N, Hausdorff JM (2017) Effects of aging on prefrontal brain activation during challenging walking conditions. Brain Cogn 115:41–46. CrossRefGoogle Scholar
  44. Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, …, Kubota K (2001) Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 14(5):1186–1192. doi:
  45. Murphy SL, Dubin JA, Gill TM (2003) The development of fear of falling among community-living older women: predisposing factors and subsequent fall events. J Gerontol A Biol Sci Med Sci 58(10):M943–M947CrossRefGoogle Scholar
  46. Neubauer AC, Fink A (2009) Intelligence and neural efficiency. Neurosci Biobehav Rev 33(7):1004–1023. CrossRefGoogle Scholar
  47. Oh-Park M, Xue X, Holtzer R, Verghese J (2011) Transient versus persistent fear of falling in community-dwelling older adults: incidence and risk factors. J Am Geriatr Soc 59(7):1225–1231. CrossRefGoogle Scholar
  48. Reelick MF, van Iersel MB, Kessels RP, Rikkert MG (2009) The influence of fear of falling on gait and balance in older people. Age Ageing 38(4):435–440. CrossRefGoogle Scholar
  49. Scheffer AC, Schuurmans MJ, van Dijk N, van der Hooft T, de Rooij SE (2008) Fear of falling: measurement strategy, prevalence, risk factors and consequences among older persons. Age Ageing 37(1):19–24. CrossRefGoogle Scholar
  50. Suzuki M, Miyai I, Ono T, Kubota K (2008) Activities in the frontal cortex and gait performance are modulated by preparation. An fNIRS study. Neuroimage 39(2):600–607. CrossRefGoogle Scholar
  51. Tinetti ME, Williams TF, Mayewski R (1986) Fall risk index for elderly patients based on number of chronic disabilities. Am J Med 80(3):429–434CrossRefGoogle Scholar
  52. Tinetti ME, Mendes de Leon CF, Doucette JT, Baker DI (1994) Fear of falling and fall-related efficacy in relationship to functioning among community-living elders. J Gerontol 49(3):M140–M147CrossRefGoogle Scholar
  53. Tuerk C, Zhang H, Sachdev P, Lord SR, Brodaty H, Wen W, Delbaere K (2016) Regional gray matter volumes are related to concern about falling in older people: a voxel-based morphometric study. J Gerontol A Biol Sci Med Sci 71(1):138–144. CrossRefGoogle Scholar
  54. Uemura K, Yamada M, Nagai K, Tanaka B, Mori S, Ichihashi N (2012) Fear of falling is associated with prolonged anticipatory postural adjustment during gait initiation under dual-task conditions in older adults. Gait Posture 35(2):282–286. CrossRefGoogle Scholar
  55. Vellas BJ, Wayne SJ, Romero LJ, Baumgartner RN, Garry PJ (1997) Fear of falling and restriction of mobility in elderly fallers. Age Ageing 26(3):189–193CrossRefGoogle Scholar
  56. Verghese J, Holtzer R, Lipton RB, Wang C (2012) Mobility stress test approach to predicting frailty, disability, and mortality in high-functioning older adults. J Am Geriatr Soc 60(10):1901–1905. CrossRefGoogle Scholar
  57. Verghese J, Wang C, Ayers E, Izzetoglu M, Holtzer R (2016) Brain activation in high-functioning older adults and falls: prospective cohort study. Neurology 88:191–197. CrossRefGoogle Scholar
  58. Vitorio R, Stuart S, Rochester L, Alcock L, Pantall A (2017) fNIRS response during walking - artefact or cortical activity? A systematic review. Neurosci Biobehav Rev 83:160–172. CrossRefGoogle Scholar
  59. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17(1):37–49CrossRefGoogle Scholar
  60. Young WR, Mark Williams A (2015) How fear of falling can increase fall-risk in older adults: applying psychological theory to practical observations. Gait Posture 41(1):7–12. CrossRefGoogle Scholar

Copyright information

© American Aging Association 2019

Authors and Affiliations

  1. 1.Albert Einstein College of Medicine BronxBronxUSA
  2. 2.Yeshiva University BronxNew YorkUSA
  3. 3.Villanova University Electrical and Computer EngineeringVillanovaUSA

Personalised recommendations