Abstract
The aim of the study was to develop a novel approach for quantifying stair-step** in a trajectory tracking task with the goal of understanding how age and stroke-related differences in motor control contribute to force control deficits. Nine stroke participants, nine age-matched controls, and nine young healthy adults performed an isometric grip** task while squeezing, holding, and releasing a cylindrical device. The visual tracking task involved three different rates of force production (5, 10, and 20% maximal force/s). Four outcome measures determined force control deficits: (a) root mean square error, (b) standard deviation, (c) step number, and (d) mean pause duration. Our findings indicate that step number, and especially mean pause duration, differentiated force control deficits in the three groups more effectively than the traditional root mean square error. Moreover, stroke participants showed the largest force control deficits during the grip release phase compared to age-matched and young healthy controls. Importantly, step number and mean pause duration quantified stair-step** while measuring different constructs than root mean square error. Distinct step and duration interruptions in force modulation by persons post-stroke during the grip release phase provide new information with implications for motor recovery during rehabilitation.
Similar content being viewed by others
Notes
Either MLP-50; range 50 lbs or MLP-200; range 200 lbs Transducer Techniques, 4.16 × 1.27 × 1.90 cm, 0.1% sensitivity.
15LT Grass Technologies Physio-data Amplifier System (Astro-Med Inc., Warwick, RI).
A/D; NI cDAQ-9172 + NI-9215, National Instruments, Austin, TX.
8.1; National Instruments, Austin, TX.
Version 2007, Microsoft Corporation, Redmond, WA.
Version 7.0, SAS Campus Drive, Cary, NC.
Abbreviations
- MVC:
-
Maximal voluntary contraction
- RMSE:
-
Root mean square error
- SD:
-
Standard deviation of force trace
- SEM:
-
Standard error of measurement
- SRD:
-
Smallest real difference
References
Aymard C, Katz R, Lafitte C, Lo E, Penicaud A, Pradat-Diehl P, Raoul S (2000) Presynaptic inhibition and homosynaptic depression: a comparison between lower and upper limbs in normal human subjects and patients with hemiplegia. Brain 123:1688–1702
Barry BK, Warman GE, Carson RG (2005) Age-related differences in rapid muscle activation after rate of force development training of the elbow flexors. Exp Brain Res 162:122–132
Beckerman H, Roebroeck ME, Lankhorst GJ, Becher JG, Bezemer PD, Verbeek AL (2001) Smallest real difference, a link between reproducibility and responsiveness. Qual Life Res 10:571–578
Bigland-Ritchie B, Johansson R, Lippold OC, Smith S, Woods JJ (1983) Changes in motoneurone firing rates during sustained maximal voluntary contractions. J Physiol 340:335–346
Blennerhassett JM, Carey LM, Matyas TA (2006) Grip force regulation during pinch grip lifts under somatosensory guidance: comparison between people with stroke and healthy controls. Arch Phys Med Rehabil 87:418–429
Bohannon RW (2007) Muscle strength and muscle training after stroke. J Rehabil Med 39:14–20
Bohannon RW, Smith MB (1987) Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 67:206–207
Brunnstrom S (1970) Movement therapy in hemiplegia: a neurophysiological approach. Harper & Row, New York
Budingen HJ, Freund HJ (1976) The relationship between the rate of rise of isometric tension and motor unit recruitment in a human forearm muscle. Pflugers Arch 362:61–67
Canning CG, Ada L, O’Dwyer NJ (2000) Abnormal muscle activation characteristics associated with loss of dexterity after stroke. J Neurol Sci 176:45–56
Chae J, Yang G, Park BK, Labatia I (2002) Muscle weakness and cocontraction in upper limb hemiparesis: relationship to motor impairment and physical disability. Neurorehabil Neural Repair 16:241–248
Christou EA, Tracy BL (2006) Aging and variability in motor output. In: Davids K, Bennett S, Newell KM (eds) Movement system variability. Human Kinetics, Champaign, pp 199–215
Christou EA, Poston B, Enoka JA, Enoka RM (2007) Different neural adjustments improve endpoint accuracy with practice in young and old adults. J Neurophysiol 97:3340–3350
Coombes SA, Gamble KM, Cauraugh JH, Janelle CM (2008) Emotional states alter force control during a feedback occluded motor task. Emotion 8:104–113
Corcos DM, Chen CM, Quinn NP, McAuley J, Rothwell JC (1996) Strength in Parkinson’s disease: relationship to rate of force generation and clinical status. Ann Neurol 39:79–88
Cruz EG, Waldinger HC, Kamper DG (2005) Kinetic and kinematic workspaces of the index finger following stroke. Brain 128:1112–1121
Darling WG, Cooke JD, Brown SH (1989) Control of simple arm movements in elderly humans. Neurobiol Aging 10:149–157
De Luca CJ, Le Fever RS, McCue MP, Xenakis AP (1982) Behaviour of human motor units in different muscles during linearly varying contractions. J Physiol 329:113–128
Duncan PW, Bode RK, Min Lai S, Perera S (2003) Rasch analysis of a new stroke-specific outcome scale: the Stroke Impact Scale. Arch Phys Med Rehabil 84:950–963
Enoka RM (1997) Neural strategies in the control of muscle force. Muscle Nerve Suppl 5:66–69
Enoka RM, Christou EA, Hunter SK, Kornatz WK, Semmler JG, Taylor AM, Tracy BL (2003) Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 13:1–12
Fearnhead L, Eales CJ, Fritz VU (1999) Arm function after stroke—can we make a difference? S Afr J Physiother 55:4–7
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”, A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198
Ford AB, Katz S (1966) Prognosis after strokes. I. A critical review. Medicine (Baltimore) 45:223–246
Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13–31
Galganski ME, Fuglevand AJ, Enoka RM (1993) Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol 69:2108–2115
Hammond MC, Fitts SS, Kraft GH, Nutter PB, Trotter MJ, Robinson LM (1988) Co-contraction in the hemiparetic forearm: quantitative EMG evaluation. Arch Phys Med Rehabil 69:348–351
Hermsdorfer J, Mai N (1996) Disturbed grip-force control following cerebral lesions. J Hand Ther 9:33–40
Hermsdorfer J, Hagl E, Nowak DA, Marquardt C (2003) Grip force control during object manipulation in cerebral stroke. Clin Neurophysiol 114:915–929
Hook P, Sriramoju V, Larsson L (2001) Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am J Physiol Cell Physiol 280:782–788
Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med 30:1–15
Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564
Kamen G (1983) The acquisition of maximal isometric plantar flexor strength: a force-time curve analysis. J Mot Behav 15:63–73
Kamen G, De Luca CJ (1989) Unusual motor unit firing behavior in older adults. Brain Res 482:136–140
Kamper DG, Rymer WZ (2001) Impairment of voluntary control of finger motion following stroke: role of inappropriate muscle coactivation. Muscle Nerve 24:673–681
Krakauer JW (2006) Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr Opin Neurol 19:84–90
Kriz G, Hermsdorfer J, Marquardt C, Mai N (1995) Feedback-based training of grip force control in patients with brain damage. Arch Phys Med Rehabil 76:653–659
Kurillo G, Bajd T, Tercelj M (2004a) The effect of age on the grip force control in lateral grip. Conf Proc IEEE Eng Med Biol Soc 6:4657–4660
Kurillo G, Zupan A, Bajd T (2004b) Force tracking system for the assessment of grip force control in patients with neuromuscular diseases. Clin Biomech 19:1014–1021
Kurillo G, Gregoric M, Goljar N, Bajd T (2005) Grip force tracking system for assessment and rehabilitation of hand function. Technol Health Care 13:137–149
Laidlaw DH, Bilodeau M, Enoka RM (2000) Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23:600–612
Lang CE, Wagner JM, Bastian AJ, Hu Q, Edwards DF, Sahrmann SA, Dromerick AW (2005) Deficits in grasp versus reach during acute hemiparesis. Exp Brain Res 166:126–136
Larsson L, Li X, Frontera WR (1997) Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 272:638–649
Levin MF (1996) Interjoint coordination during pointing movements is disrupted in spastic hemiparesis. Brain 119:281–293
Lewis GN, McNair PJ (2009) Muscle inhibition following tendon stimulation is reduced in chronic stroke. Clin Neurophysiol 120:1732–1740
Lindberg P, Ody C, Feydy A, Maier MA (2009) Precision in isometric precision grip force is reduced in middle-aged adults. Exp Brain Res 193:213–224
Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J (2010) Heart disease and stroke statistics–2010 update: a report from the American Heart Association. Circulation 121:e46–e215
Lodha N, Naik SK, Coombes SA, Cauraugh JH (2010) Force control and degree of motor impairments in chronic stroke. Clin Neurophysiol 121:1952–1961
Milner-Brown HS, Stein RB, Yemm R (1973) Changes in firing rate of human motor units during linearly changing voluntary contractions. J Physiol 230:371–390
Morgan M, Phillips JG, Bradshaw JL, Mattingley JB, Iansek R, Bradshaw JA (1994) Age-related motor slowness: simply strategic? J Gerontol 49:133–139
Muntner P, Garrett E, Klag MJ, Coresh J (2002) Trends in stroke prevalence between 1973 and 1991 in the US population 25 to 74 years of age. Stroke 33:1209–1213
Nakashima K, Rothwell JC, Day BL, Thompson PD, Shannon K, Marsden CD (1989) Reciprocal inhibition between forearm muscles in patients with writer’s cramp and other occupational cramps, symptomatic hemidystonia and hemiparesis due to stroke. Brain 112:681–697
Newell KM, Corcos DM (1993) Variability and Motor Control. Human Kinetics, Champaign
Nowak DA, Hermsdorfer J, Topka H (2003) Deficits of predictive grip force control during object manipulation in acute stroke. J Neurol 250:850–860
Orizio C, Baruzzi E, Gaffurini P, Diemont B, Gobbo M (2010) Electromyogram and force fluctuation during different linearly varying isometric motor tasks. J Electromyogr Kinesiol 20:732–741
Patten C (2000) Reeducating muscle force control in older persons through strength training. Top Geriatr Rehabil 15:47–59
Patten C, Kothari D, Whitney J, Lexell J, Lum PS (2003) Reliability and responsiveness of elbow trajectory tracking in chronic poststroke hemiparesis. J Rehabil Res Dev 40:487–500
Patten C, Lexell J, Brown HE (2004) Weakness and strength training in persons with poststroke hemiplegia: rationale, method, and efficacy. J Rehabil Res Dev 41:293–312
Perdan J, Kamnik R, Obreza P, Kurillo G, Bajd T, Munih M (2008) Design and evaluation of a functional electrical stimulation system for hand sensorimotor augmentation. Neuromodulation 11:208–215
Robichaud JA, Pfann KD, Vaillancourt DE, Comella CL, Corcos DM (2005) Force control and disease severity in Parkinson’s disease. Mov Disord 20:441–450
Ryan ED, Beck TW, Herda TJ, Hartman MJ, Stout JR, Housh TJ, Cramer JT (2008) Mechanomyographic amplitude and mean power frequency responses during isometric ramp vs. step muscle actions. J Neurosci Methods 168:293–305
Seo NJ, Rymer WZ, Kamper DG (2009) Delays in grip initiation and termination in persons with stroke: effects of arm support and active muscle stretch exercise. J Neurophysiol 101:3108–3115
Sosnoff JJ, Newell KM (2006a) Are age-related increases in force variability due to decrements in strength? Exp Brain Res 174:86–94
Sosnoff JJ, Newell KM (2006b) The generalization of perceptual-motor intra-individual variability in young and old adults. J Gerontol B Psychol Sci Soc Sci 61:304–310
Spiegel KM, Stratton J, Burke JR, Glendinning DS, Enoka RM (1996) The influence of age on the assessment of motor unit activation in a human hand muscle. Exp Physiol 81:805–819
Spraker MB, Corcos DM, Vaillancourt DE (2009) Cortical and subcortical mechanisms for precisely controlled force generation and force relaxation. Cereb Cortex 19:2640–2650
Stoeckmann TM, Sullivan KJ, Scheidt RA (2009) Elastic, viscous, and mass load effects on poststroke muscle recruitment and co-contraction during reaching: a pilot study. Phys Ther 89:665–678
Takahashi CD, Reinkensmeyer DJ (2003) Hemiparetic stroke impairs anticipatory control of arm movement. Exp Brain Res 149:131–140
Tubiana R (1981) Architecture and functions of the hand. In: Tubiana R (ed) The hand. W B Saunders, Philadelphia
Vaillancourt DE, Newell KM (2003) Aging and the time and frequency structure of force output variability. J Appl Physiol 94:903–912
Vaillancourt DE, Larsson L, Newell KM (2003) Effects of aging on force variability, single motor unit discharge patterns, and the structure of 10, 20, and 40 Hz EMG activity. Neurobiol Aging 24:25–35
Vidoni ED, Boyd LA (2009) Preserved motor learning after stroke is related to the degree of proprioceptive deficit. Behav Brain Funct 5:36
Voelcker-Rehage C, Alberts JL (2005) Age-related changes in gras** force modulation. Exp Brain Res 166:61–70
Wenzelburger R, Kopper F, Frenzel A, Stolze H, Klebe S, Brossmann A, Kuhtz-Buschbeck J, Golge M, Illert M, Deuschl G (2005) Hand coordination following capsular stroke. Brain 128:64–74
Winstein CJ, Merians AS, Sullivan KJ (1999) Motor learning after unilateral brain damage. Neuropsychologia 37:975–987
Author information
Authors and Affiliations
Corresponding author
Appendix: stair-step** calculations
Appendix: stair-step** calculations
Stair-step**
Interruptions in force production during the force tracking task were termed steps. We operationally defined a step using two criteria:
-
(a)
Temporal—if the performed rate of force modulation lagged the criterion rate by 50% or more as defined by
-
(b)
constant force production—less than 2% change in absolute force over the relevant epoch
A step was confirmed only when both these conditions were satisfied simultaneously.
Step detection—temporal component
Force data were sampled at 100 Hz (i.e., 100 samples/1000 ms) offering the following criteria for step detection.
Criterion rate of force production | Temporal epoch, 1% MVC (ms) | Lag (ms) | Samples |
---|---|---|---|
5% MVC/s | 200 | ≥100 | 10 |
10% MVC/s | 100 | ≥50 | 5 |
20% MVC/s | 50 | ≥25 | 2.5 (3) |
Example: 5% MVC/s rate of force production means change of 1% of MVC force requires 100/5 = 20 samples (i.e., 20 × 10 = 200 ms). Therefore, applying temporal definition of step, defines lag as (200 × 50)/100 = 100 ms. Similarly, 20% MVC/s rate of force production implies that 100/20 = 5 samples (i.e., 5 × 10 = 50 ms) are required to change 1% MVC force, which defines temporal component as (50 × 50)/100 = 25 ms.
Step detection—constant force component
In Fig. 6a,
Point 1: At time 2250 ms, force produced was 34.04 N
Point 2: At time 2580 ms, force produced was 34.56 N
Step number: Change of produced force from arrow 1 to 2 is 0.52, less than 2% of absolute force (0.52) at arrow 1 (34.04 N). The time lag is 330 ms. Based on our operational definitions, this phase met both criteria and was therefore defined as a step.
Pause duration: Point 3 represents time between points 1 and 2, which was termed as pause duration for this step (330 ms).
Similarly, Fig. 6b demonstrates representative step and pause duration for 20% MVC/s rate of force production.
Rights and permissions
About this article
Cite this article
Naik, S.K., Patten, C., Lodha, N. et al. Force control deficits in chronic stroke: grip formation and release phases. Exp Brain Res 211, 1–15 (2011). https://doi.org/10.1007/s00221-011-2637-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-011-2637-8