Original research| Volume 99, ISSUE 3, P491-500, March 2018

Modification of Spastic Stretch Reflexes at the Elbow by Flexion Synergy Expression in Individuals With Chronic Hemiparetic Stroke

  • Jacob G. McPherson
    Department of Physical Therapy and Human Movement Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL
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  • Arno H. Stienen
    Department of Physical Therapy and Human Movement Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL
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  • Justin M. Drogos
    Department of Physical Therapy and Human Movement Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL
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  • Julius P. Dewald
    Corresponding author Julius P. Dewald, PT, PhD, Department of Physical Therapy and Human Movement Sciences, Northwestern University, 645 N Michigan Ave, Ste 1100, Chicago, IL 60611.
    Department of Physical Therapy and Human Movement Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL

    Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL

    Department of Biomedical Engineering, Northwestern University McCormick School of Engineering, Chicago, IL
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      To systematically characterize the effect of flexion synergy expression on the manifestation of elbow flexor stretch reflexes poststroke, and to relate these findings to elbow flexor stretch reflexes in individuals without neurologic injury.


      Controlled cohort study.


      Academic medical center.


      Participants (N=20) included individuals with chronic hemiparetic stroke (n=10) and a convenience sample of individuals without neurologic or musculoskeletal injury (n=10).


      Participants with stroke were interfaced with a robotic device that precisely manipulated flexion synergy expression (by regulating shoulder abduction loading) while delivering controlled elbow extension perturbations over a wide range of velocities. This device was also used to elicit elbow flexor stretch reflexes during volitional elbow flexor activation, both in the cohort of individuals with stroke and in a control cohort. In both cases, the amplitude of volitional elbow flexor preactivation was matched to that generated involuntarily during flexion synergy expression.

      Main Outcome Measures

      The amplitude of short- and long-latency stretch reflexes in the biceps brachii, assessed by electromyography, and expressed as a function of background muscle activation and stretch velocity.


      Increased shoulder abduction loading potentiated elbow flexor stretch reflexes via flexion synergy expression in the paretic arm. Compared with stretch reflexes in individuals without neurologic injury, paretic reflexes were larger at rest but were approximately equal to control muscles at matched levels of preactivation.


      Because flexion synergy expression modifies stretch reflexes in involved muscles, interventions that reduce flexion synergy expression may confer the added benefit of reducing spasticity during functional use of the arm.


      List of abbreviations:

      BIC (biceps), EE (elbow extension), EF (elbow flexion), LLR (long-latency reflex), MVT (maximum voluntary torque), SABD (shoulder abduction), SLR (short-latency reflex)
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        • Lance J.W.
        The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture.
        Neurology. 1980; 30: 1303-1313
        • Brunnstrom S.
        Movement therapy in hemiplegia.
        Harper & Row, New York1970
        • Twitchell T.E.
        The restoration of motor function following hemiplegia in man.
        Brain. 1951; 74: 443-480
        • Dewald J.P.
        • Pope P.S.
        • Given J.D.
        • Buchanan T.S.
        • Rymer W.Z.
        Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects.
        Brain. 1995; 118: 495-510
        • Sukal T.M.
        • Ellis M.D.
        • Dewald J.P.
        Shoulder abduction-induced reductions in reachins work area following hemiparetic stroke: neuroscientific implications.
        Exp Brain Res. 2007; 183: 215-223
        • Miller L.C.
        • Dewald J.P.
        Involuntary paretic wrist/finger flexion forces and EMG increase with shoulder abduction load in individuals with chronic stroke.
        Clin Neurophysiol. 2012; 123: 1216-1225
        • McPherson J.G.
        • Stienen A.H.
        • Drogos J.M.
        • Dewald J.P.
        The relationship between the flexion synergy and stretch reflexes in individuals with chronic hemiparetic stroke.
        IEEE Int Conf Rehabil Robot. 2011; 2011: 5975516
        • Ellis M.D.
        • Sukal T.
        • DeMott T.
        • Dewald J.P.
        Augmenting clinical evaluation of hemiparetic arm movement with a laboratory-based quantitative measurement of kinematics as a function of limb loading.
        Neurorehabil Neural Repair. 2008; 22: 321-329
        • Burne J.
        • Carleton V.
        • O'Dwyer N.
        The spasticity paradox: movement disorder or disorder of resting limbs?.
        J Neurol Neurosurg Psychiatry. 2005; 76: 47-54
        • Sunnerhagen K.S.
        • Olver J.
        • Francisco G.E.
        Assessing and treating functional impairment in poststroke spasticity.
        Neurology. 2013; 80: S35-S44
        • Mandon L.
        • Boudarham J.
        • Robertson J.
        • Bensmail D.
        • Roche N.
        • Roby-Brami A.
        Faster reaching in chronic spastic stroke patients comes at the expense of arm-trunk coordination.
        Neurorehabil Neural Repair. 2016; 30: 209-220
        • Lee W.A.
        • Boughton A.
        • Rymer W.Z.
        Absence of stretch reflex gain enhancement in voluntarily activated spastic muscle.
        Exp Neurol. 1987; 98: 317-335
        • Powers R.K.
        • Campbell D.
        • Rymer W.Z.
        Stretch reflex dynamics in spastic elbow flexor muscles.
        Ann Neurol. 1989; 25: 32-42
        • Thilmann A.F.
        • Fellows S.J.
        • Garms E.
        The mechanism of spastic muscle hypertonus. Variation in reflex gain over the time course of spasticity.
        Brain. 1991; 114: 233-244
        • Hu X.
        • Suresh N.L.
        • Chardon M.K.
        • Rymer W.Z.
        Contributions of motoneuron hyperexcitability to clinical spasticity in hemispheric stroke survivors.
        Clin Neurophysiol. 2015; 126: 1599-1606
        • Musampa N.K.
        • Mathieu P.A.
        • Levin M.F.
        Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity.
        Exp Brain Res. 2007; 181: 579-593
        • Lorentzen J.
        • Grey M.J.
        • Crone C.
        • Mazevet D.
        • Biering-Sorensen F.
        • Nielsen J.B.
        Distinguishing active from passive components of ankle plantar flexor stiffness in stroke, spinal cord injury and multiple sclerosis.
        Clin Neurophysiol. 2010; 121: 1939-1951
        • Zhang L.Q.
        • Chung S.G.
        • Ren Y.
        • Liu L.
        • Roth E.J.
        • Rymer W.Z.
        Simultaneous characterizations of reflex and nonreflex dynamic and static changes in spastic hemiparesis.
        J Neurophysiol. 2013; 110: 418-430
        • Ibrahim I.K.
        • Berger W.
        • Trippel M.
        • Dietz V.
        Stretch-induced electromyographic activity and torque in spastic elbow muscles. Differential modulation of reflex activity in passive and active motor tasks.
        Brain. 1993; 116: 971-989
        • Ellis M.D.
        • Holubar B.G.
        • Acosta A.M.
        • Beer R.F.
        • Dewald J.P.
        Modifiability of abnormal isometric elbow and shoulder joint torque coupling after stroke.
        Muscle Nerve. 2005; 32: 170-178
        • Ellis M.D.
        • Acosta A.M.
        • Yao J.
        • Dewald J.P.
        Position-dependent torque coupling and associated muscle activation in the hemiparetic upper extremity.
        Exp Brain Res. 2007; 176: 594-602
        • Ellis M.D.
        • Drogos J.M.
        • Carmona C.
        • Keller T.
        • Dewald J.P.
        Neck rotation modulates flexion synergy torques, indicating an ipsilateral reticulospinal source for impairment in stroke.
        J Neurophysiol. 2012; 108: 3096-3104
        • Stienen A.H.
        • McPherson J.G.
        • Schouten A.C.
        • Dewald J.P.
        The ACT-4D: a novel rehabilitation robot for the quantification of upper limb motor impairments following brain injury.
        IEEE Int Conf Rehabil Robot. 2011; 2011: 5975460
        • Schmit B.D.
        • Dewald J.P.
        • Rymer W.Z.
        Stretch reflex adaptation in elbow flexors during repeated passive movements in unilateral brain-injured patients.
        Arch Phys Med Rehabil. 2000; 81: 269-278
        • Trumbower R.D.
        • Ravichandran V.J.
        • Krutky M.A.
        • Perreault E.J.
        Contributions of altered stretch reflex coordination to arm impairments following stroke.
        J Neurophysiol. 2010; 104: 3612-3624
        • Perreault E.J.
        • Chen K.
        • Trumbower R.D.
        • Lewis G.
        Interactions with compliant loads alter stretch reflex gains but not intermuscular coordination.
        J Neurophysiol. 2008; 99: 2101-2113
        • Kuypers H.G.
        The descending pathways to the spinal cord, their anatomy and function.
        Prog Brain Res. 1964; 11: 178-202
        • Davidson A.G.
        • Buford J.A.
        Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging.
        Exp Brain Res. 2006; 173: 25-39
        • Riddle C.N.
        • Edgley S.A.
        • Baker S.N.
        Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract.
        J Neurosci. 2009; 29: 4993-4999
        • Zaaimi B.
        • Edgley S.A.
        • Soteropoulos D.S.
        • Baker S.N.
        Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey.
        Brain. 2012; 135: 2277-2289
        • Fedirchuk B.
        • Dai Y.
        Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production.
        J Physiol. 2004; 557: 355-361
        • Heckman C.J.
        • Johnson M.D.
        • Mottram C.J.
        • Schuster J.
        Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns.
        Neuroscientist. 2008; 14: 264-275
        • Johnson M.D.
        • Heckman C.J.
        Gain control mechanisms in spinal motoneurons.
        Front Neural Circuits. 2014; 8: 81
        • McPherson J.G.
        • Ellis M.D.
        • Heckman C.J.
        • Dewald J.P.
        Evidence for increased activation of persistent inward currents in individuals with chronic hemiparetic stroke.
        J Neurophysiol. 2008; 100: 3236-3243
        • Johnson M.D.
        • Thompson C.K.
        • Tysseling V.M.
        • Powers R.K.
        • Heckman C.J.
        The potential for understanding the synaptic organization of human motor commands via the firing patterns of motoneurons.
        J Neurophysiol. 2017; 118: 520-531
        • Powers R.K.
        • Heckman C.J.
        Synaptic control of the shape of the motoneuron pool input-output function.
        J Neurophysiol. 2017; 117: 1171-1184
        • Ellis M.D.
        • Schut I.
        • Dewald J.P.
        Flexion synergy overshadows flexor spasticity during reaching in chronic moderate to severe hemiparetic stroke.
        Clin Neurophysiol. 2017; 128: 1308-1314
        • Calota A.
        • Levin M.F.
        Tonic stretch reflex threshold as a measure of spasticity: implications for clinical practice.
        Top Stroke Rehabil. 2009; 16: 177-188
        • Heckmann C.J.
        • Gorassini M.A.
        • Bennett D.J.
        Persistent inward currents in motoneuron dendrites: implications for motor output.
        Muscle Nerve. 2005; 31: 135-156
        • Beer R.F.
        • Dewald J.P.
        • Rymer W.Z.
        Deficits in the coordination of multijoint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics.
        Exp Brain Res. 2000; 131: 305-319
        • Feldman A.G.
        Once more on the equilibrium-point hypothesis (lambda model) for motor control.
        J Mot Behav. 1986; 18: 17-54
        • Bhagchandani N.
        • Schindler-Ivens S.
        Reciprocal inhibition post-stroke is related to reflex excitability and movement ability.
        Clin Neurophysiol. 2012; 123: 2239-2246
        • Nielsen J.B.
        • Petersen N.T.
        • Crone C.
        • Sinkjaer T.
        Stretch reflex regulation in healthy subjects and patients with spasticity.
        Neuromodulation. 2005; 8: 49-57
        • Blanchette A.K.
        • Mullick A.A.
        • Moin-Darbari K.
        • Levin M.F.
        Tonic stretch reflex threshold as a measure of ankle plantar-flexor spasticity after stroke.
        Phys Ther. 2016; 96: 687-695
        • Powers R.K.
        • Marder-Meyer J.
        • Rymer W.Z.
        Quantitative relations between hypertonia and stretch reflex threshold in spastic hemiparesis.
        Ann Neurol. 1988; 23: 115-124
        • Meskers C.G.
        • Schouten A.C.
        • de Groot J.H.
        • et al.
        Muscle weakness and lack of reflex gain adaptation predominate during post-stroke posture control of the wrist.
        J Neuroeng Rehabil. 2009; 6: 29