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A Comparison of Mental Workload in Individuals with Transtibial and Transfemoral Lower Limb Loss during Dual-Task Walking under Varying Demand

Published online by Cambridge University Press:  29 August 2019

Emma P. Shaw ,
Jeremy C. Rietschel ,
Brad D. Hendershot ,
Alison L. Pruziner ,
Erik J. Wolf ,
Christopher L. Dearth ,
Matthew W. Miller ,
Bradley D. Hatfield  and
Rodolphe J. Gentili
Emma P. Shaw
Affiliation:
Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD, 20742, USA Department of Kinesiology, School of Public Health, University of Maryland, College Park, MD, 20742, USA Department of Rehabilitation, Walter Reed National Military Medical Center, Bethesda, MD, 20889, USA
Jeremy C. Rietschel
Affiliation:
Department of Kinesiology, School of Public Health, University of Maryland, College Park, MD, 20742, USA Baltimore Veterans Affairs Medical Center, Baltimore, MD, 21201, USA
Brad D. Hendershot
Affiliation:
Department of Rehabilitation, Walter Reed National Military Medical Center, Bethesda, MD, 20889, USA DoD-VA Extremity Trauma and Amputation Center of Excellence, Bethesda, MD, 20889, USA Department of Rehabilitation Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD, 20814, USA
Alison L. Pruziner
Affiliation:
Department of Rehabilitation, Walter Reed National Military Medical Center, Bethesda, MD, 20889, USA DoD-VA Extremity Trauma and Amputation Center of Excellence, Bethesda, MD, 20889, USA Department of Rehabilitation Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD, 20814, USA
Erik J. Wolf
Affiliation:
Department of Rehabilitation, Walter Reed National Military Medical Center, Bethesda, MD, 20889, USA DoD-VA Extremity Trauma and Amputation Center of Excellence, Bethesda, MD, 20889, USA Department of Rehabilitation Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD, 20814, USA
Christopher L. Dearth
Affiliation:
Department of Rehabilitation, Walter Reed National Military Medical Center, Bethesda, MD, 20889, USA DoD-VA Extremity Trauma and Amputation Center of Excellence, Bethesda, MD, 20889, USA Department of Surgery, Uniformed Services University of the Health Sciences, Bethesda, MD, 20814, USA
Matthew W. Miller
Affiliation:
School of Kinesiology, Auburn University, Auburn, AL, 36849, USA Center for Neuroscience, Auburn University, Auburn, AL, 36849, USA
Bradley D. Hatfield
Affiliation:
Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD, 20742, USA Department of Kinesiology, School of Public Health, University of Maryland, College Park, MD, 20742, USA
Rodolphe J. Gentili*
Affiliation:
Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD, 20742, USA Department of Kinesiology, School of Public Health, University of Maryland, College Park, MD, 20742, USA Maryland Robotics Center, University of Maryland, College Park, MD, 20742, USA
*
Correspondence and reprint requests to: Rodolphe J. Gentili, Department of Kinesiology, School of Public Health (Bldg #255), University of Maryland, Room #2138, College Park, MD 20742, USA. E-mail: [email protected]
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Abstract

Objectives: This study aimed to evaluate the influence of lower limb loss (LL) on mental workload by assessing neurocognitive measures in individuals with unilateral transtibial (TT) versus those with transfemoral (TF) LL while dual-task walking under varying cognitive demand. Methods: Electroencephalography (EEG) was recorded as participants performed a task of varying cognitive demand while being seated or walking (i.e., varying physical demand). Results: The findings revealed both groups of participants (TT LL vs. TF LL) exhibited a similar EEG theta synchrony response as either the cognitive or the physical demand increased. Also, while individuals with TT LL maintained similar performance on the cognitive task during seated and walking conditions, those with TF LL exhibited performance decrements (slower response times) on the cognitive task during the walking in comparison to the seated conditions. Furthermore, those with TF LL neither exhibited regional differences in EEG low-alpha power while walking, nor EEG high-alpha desynchrony as a function of cognitive task difficulty while walking. This lack of alpha modulation coincided with no elevation of theta/alpha ratio power as a function of cognitive task difficulty in the TF LL group. Conclusions: This work suggests that both groups share some common but also different neurocognitive features during dual-task walking. Although all participants were able to recruit neural mechanisms critical for the maintenance of cognitive-motor performance under elevated cognitive or physical demands, the observed differences indicate that walking with a prosthesis, while concurrently performing a cognitive task, imposes additional cognitive demand in individuals with more proximal levels of amputation.

Keywords

Mental loadEEG dynamicsSpectral powerAmputation levelsAlpha and theta bandsProsthesisConcurrent secondary taskLocomotion
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 9 , October 2019 , pp. 985 - 997
Copyright
Copyright © INS. Published by Cambridge University Press, 2019. 

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References

REFERENCES

Alderman, B.L., Olson, R.L., Bates, M.E., Selby, E.A., Buckman, J.F., Brush, C.J., Panza, E.A., Kranzler, A., Eddie, D., & Shors, T.J. (2015). Rumination in major depressive disorder is associated with impaired neural activation during conflict monitoring. Frontiers in Human Neuroscience, 9, 296.CrossRefGoogle ScholarPubMed
Babu Henry Samuel, I., Wang, C., Hu, Z., & Ding, M. (2018) The frequency of alpha oscillations: Task-dependent modulation and its functional significance. Neuroimage, 183, 897–906.CrossRefGoogle ScholarPubMed
Baldwin, C.L., Roberts, D.M., Barragan, D., Lee, J.D., Lerner, N., & Higgins, J.S. (2017). Detecting and quantifying mind wandering during simulated driving. Frontiers in Human Neuroscience, 11, 406.CrossRefGoogle ScholarPubMed
Basar-Eroglu, C., Struber, D., Schurmann, M., Stadler, M., & Basar, E. (1996). Gamma-band responses in the brain: A short review of psychophysiological correlates and functional significance. International Journal of Psychophysiology, 24, 101–112.CrossRefGoogle Scholar
Beurskens, R., Steinberg, F., Antoniewicz, F., Wolff, W., & Granacher, U. (2016). Neural correlates of dual-task walking: Effects of cognitive versus motor interference in young adults. Neural Plasticity, 2016, 9.CrossRefGoogle ScholarPubMed
Bhatnagar, V., Richard, E., Melcer, T., Walker, J., & Galarneau, M. (2015). Lower-limb amputation and effect of posttraumatic stress disorder on Department of Veterans Affairs outpatient cost trends. The Journal of Rehabilitation of Research Development, 52(7), 827–38.CrossRefGoogle ScholarPubMed
Bhuvaneswar, C.G., Epstein, L.A., & Stern, T.A. (2007). Reactions to amputation: Recognition and treatment. Primary Care Companion to The Journal of Clinical Psychiatry, 9(4), 303–308.CrossRefGoogle ScholarPubMed
Borghini, G., Arico, P., Di Flumeri, G., Cartocci, G., Colosimo, A., Bonelli, S., Golfetti, A., Imbert, J.P., Granger, G., Benhacene, R., Pozzi, S., & Babiloni, F. (2017). EEG-based cognitive control behavior assessment: An ecological study with professional air traffic controllers. Scientific Reports, 7, 547.CrossRefGoogle ScholarPubMed
Braboszcz, C., & Delorme, A. (2011). Lost in thoughts: Neural markers of low alertness during mind wandering. NeuroImage, 54, 3040–3047.CrossRefGoogle ScholarPubMed
Bradford, J.C., Lukos, J.R., & Ferris, D.P. (2016). Electrocortical activity distinguishes between uphill and level walking in humans. Journal of Neurophysiology, 115, 958–966.CrossRefGoogle ScholarPubMed
Brooks, J. & Kerick, S. (2015). Event-related alpha perturbations related to the scaling of steering wheel corrections. Physiology & Behavior, 149, 287–293.CrossRefGoogle ScholarPubMed
Castermans, T., Duvinage, M., Cheron, G., & Dutoit, T. (2014). About the cortical origin of the low-delta and high-gamma rhythms observed in EEG signals during treadmill walking. Neuroscience Letters, 561, 166–170.CrossRefGoogle ScholarPubMed
Cheng, M.Y., Hung, C.L., Huang, C.J., Chang, Y.K., Lo, L.-C., Shen, C., & Hung, T.M. (2015). Expert-novice differences in SMR activity during dart throwing. Biological Psychology, 110, 212–218.CrossRefGoogle ScholarPubMed
Chuang, L.Y., Huang, C.J., & Hung, T.M. (2013). The differences in frontal midline theta power between successful and unsuccessful basketball free throws of elite basketball players. International Journal of Psychophysiology, 90(3), 321–328.CrossRefGoogle ScholarPubMed
De Sanctis, P., Butler, J.S., Malcolm, B.R., & Foxe, J.J. (2014). Recalibration of inhibitory control systems during walking-related dual-task interference: A mobile brain-body imaging (MOBI) study. NeuroImage, 94, 55–64.CrossRefGoogle ScholarPubMed
Dyke, F.B., Leiker, A.M., Grand, K.F., Godwin, M.M., Thompson, A.G., Rietschel, J.C., McDonald, C.G., & Miller, M. W. (2015). The efficacy of auditory probes in indexing cognitive workload is dependent on stimulus complexity. International Journal of Psychophysiology, 95(1), 56–62.CrossRefGoogle ScholarPubMed
Gentili, R.J., Bradberry, T.J., Oh, H., Hatfield, B.D., & Contreras-Vidal, J.L. (2011). Cerebral cortical dynamics during visuomotor transformation: Adaptation to a cognitive-motor executive challenge. Psychophysiology, 48, 813–824.CrossRefGoogle ScholarPubMed
Gentili, R.J., Jaquess, K.J., Shuggi, I.M., Shaw, E.P., Oh, H., Lo, L.-C., Tan, Y.Y., Domingues, C.A., Blanco, J.A., Rietschel, J.C., Miller, M.W., & Hatfield, B.D. (2018). Combined assessment of attentional reserve and cognitive-motor effort under various levels of challenge with a dry EEG system. Psychophysiology, 55(6), e13059.CrossRefGoogle ScholarPubMed
Gevins, A., & Smith, M.E. (2003). Neurophysiological measures of cognitive workload during human-computer interaction. Theoretical Issues in Ergonomics Science, 4(1–2), 113–131.CrossRefGoogle Scholar
Gwin, J.T., Gramann, K., Makeig, S., & Ferris, D.P. (2010). Removal of movement artifact from high-density EEG recorded during walking and running. Journal of Neurophysiology, 103, 3526–3534.CrossRefGoogle ScholarPubMed
Hart, S.G. & Staveland, L.E. (1988). Development of NASA-TLX (task load index): Results of empirical and theoretical research. In Hancock, P. A. & Meshkati, N. (Eds.). Human mental workload. Amsterdam: North Holland Press.Google Scholar
Hockey, G.R.J., Nickel, P., Roberts, A.C., & Roberts, M.H. (2009). Sensitivity of candidate markers of psychophysiological strain to cyclical changes in manual control load during simulated process control. Applied Ergonomics, 40(6), 1011–1018.CrossRefGoogle ScholarPubMed
Holm, A., Lukander, K., Korpela, J., Sallinen, M., & Müller, K.M.I. (2009). Estimating brain load from the EEG. The Scientific World Journal, 9, 639–651.CrossRefGoogle ScholarPubMed
Howard, M.W., Rizzuto, D.S., Caplan, J.B., Madsen, J.R., Lisman, J., Aschenbrenner-Schebe, R., Schulze-Bonhage, A., & Kahana, M.J. (2003). Gamma oscillations correlate with working memory load in humans. Cerebral Cortex, 13, 1369–1374.CrossRefGoogle ScholarPubMed
Howard, C.L., Wallace, C., Abbas, J., & Stokic, D.S. (2017). Residual standard deviation: Validation of a new measure of dual-task cost in below-knee prosthesis users. Gait & Posture, 51, 91–96.CrossRefGoogle Scholar
Jaiswal, N., Ray, W., & Slobounov, S. (2010). Encoding of visual-spatial information in working memory requires more cerebral efforts than retrieval: Evidence from EEG and virtual reality study. Brain Research, 1347, 80–89.CrossRefGoogle ScholarPubMed
Jaquess, K.J., Lo, L.C., Oh, H., Lu, C., Ginsberg, A., Tan, Y.Y., Lohse, K.R., Miller, M.W., Hatfield, B.D., & Gentili, R.J. (2018). Changes in mental workload and motor performance throughout multiple practice sessions under various levels of task difficulty. Neuroscience, 393, 305–318.CrossRefGoogle ScholarPubMed
Kao, S.C., Huang, C.J., & Hung, T.M. (2013). Frontal midline theta is a specific indicator of optimal attentional engagement during skilled putting performance. Journal of Sport & Exercise Psychology, 35(5), 470–478.CrossRefGoogle ScholarPubMed
Kerick, S.E., Hatfield, B.D., & Allender, L.E. (2007). Event-related cortical dynamics of soldiers during shooting as a function of varied task demand. Aviation, Space, and Environmental Medicine, 78(5), B153–B164.Google ScholarPubMed
Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis. Brain Research, 29, 169–195.CrossRefGoogle ScholarPubMed
Kline, J.E., Huang, H.J., Snyder, K.L., & Ferris, D.P. (2015). Isolating gait-related movement artifacts in electroencephalography during human walking. Journal of Neural Engineering, 12, 046022.CrossRefGoogle ScholarPubMed
Lobo, I., Portugal, L.C., Figueira, I., Volchan, E., David, I., Pereira, M.G., & de Oliveira, L. (2015). EEG correlates of the severity of posttraumatic stress symptoms: A systematic review of the dimensional PTSD literature. Journal of Affective Disorders, 183, 210–220.CrossRefGoogle ScholarPubMed
Lockhart, T. & Liu, J. (2008). Differentiating fall-prone and healthy adults using local dynamics stability. Ergonomics, 51(12), 1860–1872.CrossRefGoogle Scholar
Malcolm, B.R., Foxe, J.J., Butler, J.S., & De Sanctis, P. (2015). The aging brain shows less flexible reallocation of cognitive resources during dual-task walking: A mobile brain/body imaging (MoBI) study. NeuroImage, 117, 230–242.CrossRefGoogle ScholarPubMed
Marcar, V.L., Bridenbaugh, S.A., Kool, J., Niedermann, K., & Kressig, R.W. (2014). A simple procedure to synchronize concurrent measurements of gait and brain electrical activity and preliminary results from a pilot measurement involving motor-cognitive dual-tasking in healthy older and young volunteers. Journal of Neuroscience Methods, 228, 46–49.CrossRefGoogle ScholarPubMed
Michels, L., Bucher, K., Lüchinger, R., Klaver, P., Martin, E., Jeanmonod, D., & Brandeis, D. (2010). Simultaneous EEG-fMRI during a working memory task: Modulations in low and high frequency bands. PLoS One, 5(4), e10298.CrossRefGoogle ScholarPubMed
Miller, W.C., Speechley, M., & Deathe, B. (2001). The prevalence and risk factors of falling and fear of falling among lower extremity amputees. Archives of Physical Medicine and Rehabilitation, 82(8), 1031–1037.CrossRefGoogle ScholarPubMed
Morgan, S.J., Hafner, B.J., & Kelly, V.E. (2015). The effects of a concurrent task on walking in persons with transfemoral amputation compared to persons without limb loss. Prosthetics and Orthotics International, 40(4), 490–496.CrossRefGoogle ScholarPubMed
Morgan, S.J., Hafner, B.J., & Kelly, V.E. (2017). Dual-task walking over a compliant foam surface: A comparison of people with transfemoral amputation and controls. Gait & Posture, 58, 41–45.CrossRefGoogle Scholar
Morgenroth, D., Orendurff, M., Shakir, A., Segal, A., Shofer, J., & Czerniecki, J. (2010). The relationship between lumbar spine kinematics during gait and low-back pain in transfemoral amputees. American Journal of Physical Medicine & Rehabilitation, 89(8), 635–643.CrossRefGoogle ScholarPubMed
Murray, N.P. & Janelle, C.M. (2007). Event-related potential evidence for the processing efficiency theory. Journal of Sports Science, 25(2), 161–171.CrossRefGoogle ScholarPubMed
Nathan, K. & Contreras-Vidal, J.L. (2016). Negligible motion artifacts in scalp electroencephalography (EEG) during treadmill walking. Frontiers in Human Neuroscience, 9, 708.CrossRefGoogle ScholarPubMed
Onton, J., Westerfield, M., Townsend, J., & Makeig, S. (2006). Imaging human EEG dynamics using independent component analysis. Neuroscience and Biobehavioral Reviews, 30, 808–822.CrossRefGoogle ScholarPubMed
Pascalis, D. & Ray, W.J. (1998). Effects of memory load on event-related patterns of 40-Hz EEG during cognitive and motor tasks. International Journal of Psychophysiology, 28, 301–315.CrossRefGoogle ScholarPubMed
Pizzagalli, D.A. (2007). Electroencephalography and high-density electrophysiological source localization disorders, In Cacioppo, J.T., Tassinary, L.G., & Berntson, G. (Eds.), Handbook of psychophysiology (pp. 60–61). New York: Cambridge University Press.Google Scholar
Pruziner, A.L., Shaw, E.P., Rietschel, J.C., Hendershot, B.D., Miller, M.M., Wolf, E.J., Hatfield, B.D., Dearth, C.L., & Gentili, R.J. (2019) Biomechanical and neurocognitive performance outcomes of walking with transtibial limb loss while challenged by a concurrent task. Experimental Brain Research, 237(2), 477–491.CrossRefGoogle ScholarPubMed
Reis, P.M.R., Hebenstreit, F., Gabsteiger, F., von Tscharner, V., & Lochmann, M. (2014). Methodological aspects of EEG and body dynamics measurements during motion. Frontiers in Human Neuroscience, 8, 156.CrossRefGoogle ScholarPubMed
Rietschel, J.C., Miller, M.W., Gentili, R.J., Goodman, R.N., McDonald, C.G., & Hatfield, B.D. (2012). Cerebral-cortical networking and activation increase as a function of cognitive-motor task difficulty. Biological Psychology, 90, 127–133.CrossRefGoogle ScholarPubMed
Shaw, E.P., Rietschel, J.C., Hendershot, B.D., Pruziner, A.L., Miller, M.M., Hatfield, B.D., & Gentili, R.J. (2018). Measurement of attentional reserve and mental effort for cognitive workload assessment under various task demands during dual-task walking. Biological Psychology, 134, 39–51.CrossRefGoogle ScholarPubMed
Sipp, A.R., Gwin, J.T., Makeig, S., & Ferris, D.P. (2013). Loss of balance during beam walking elicits a multifocal theta band electrocortical response. Journal of Neurophysiology, 110, 2050–2060.CrossRefGoogle ScholarPubMed
Slobounov, S.M., Ray, W., Johnson, B., Slobounov, E., & Newell, K.M. (2015). Modulation of cortical activity in 2D versus 3D virtual reality environments: An EEG study. International Journal of Psychophysiology, 95(3), 254–260.CrossRefGoogle Scholar
Slobounov, S.M., Teel, L., & Newell, K.M. (2013). Modulation of cortical activity in response to visually induced postural perturbation: Combined VR and EEG study. Neuroscience Letters, 547, 6–9.CrossRefGoogle ScholarPubMed
Wagner, J., Solis-Escalante, T., Grieshofer, P., Neuper, C., Müller-Putz, G.R., & Scherer, R. (2012). Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects. NeuroImage, 63, 1203–1211.CrossRefGoogle ScholarPubMed
Wagner, J., Solis-Escalante, T., Scherer, R., Neuper, C., & Muller-Putz, G. (2014). It’s how you get there: Walking down a virtual alley activates premotor and parietal areas. Frontiers in Human Neuroscience, 9, 93.Google Scholar
Wang, C., Rajagovindan, R., Han, S.M., & Ding, M. (2016). Top-down control of visual alpha oscillations: Sources of control signals and their mechanisms of action. Frontiers in Human Neuroscience, 10, 15.CrossRefGoogle ScholarPubMed
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