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115138verIIRobotic-assisted locomotor training enhances ankle performance in adults with incomplete spinal cord injuryVennila Krishnan1, Matthew Kindig2, Mehdi Mirbagheri2,31Department of Physical Therapy, California State University at Long Beach, CA 90840, United States2Sensory Motor Performance Program, Rehabilitation Institute of Chicago, IL 60611, United States3Department of Physical Medicine and Rehabilitation, Northwestern University, Chicago, IL 60611. United StatesCorresponding AuthorVennila Krishnan, PT, PhDAssociate ProfessorDepartment of Physical Therapy, ET 1181250 Bellflower BlvdCalifornia State UniversityLong Beach, CA 90840Phone: 562-985-4155Fax: 562-985-4069Email: vennila.krishnan@csulb.eduRunning title: Robotic-assisted locomotor training enhances ankle performance in iSCIKey words: ankle motor control, co-activation, electromyography, SCI, robotic intervention, MVCABSTRACTPurpose: Ankle joint control plays an important role in independent walking. We investigated the effects of robotic assisted locomotor training (RALT) on impaired ankle joint control in individuals with chronic incomplete spinal cord injury (iSCI). Method: Sixteen individuals with iSCI underwent twelve 1-hour sessions of RALT for 4-weeks, while sixteen individuals with iSCI served as controls. We evaluated changes in ankle control measures, torque and co-activation during maximal voluntary contractions (MVC) in dorsi- and plantar-flexion. We also evaluated changes in the walking performance measures using Timed Up and Go (TUG), 10-meter walk (10MWT) and 6-minute walk (6MWT) tests at two time points: baseline and after 4-weeks. Results: The RALT group markedly improved in MVC torque during both dorsi- and plantar-flexion contractions. Furthermore, co-activation during the dorsi-flexion MVC decreased in the RALT group compared to the controls after the training. Regarding walking performance, the RALT group significantly improved in walking mobility (TUG) and speed (10MWT). Finally, correlation analysis indicated a significant linear relationship between MVC torques and walking performance measures. Conclusion: Our findings provide evidence that RALT improves ankle joint control, which may translate into enhanced walking performance in individuals with chronic iSCI. Key words: ankle motor control, co-activation, electromyography, SCI, robotic intervention, MVC, torqueINTRODUCTIONIn individuals after incomplete spinal cord injury (iSCI), independent walking is negatively influenced by, in part, decreased strength ADDIN EN.CITE <EndNote><Cite><Author>Waters</Author><Year>1994</Year><RecNum>5</RecNum><DisplayText>(1)</DisplayText><record><rec-number>5</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">5</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Waters, R. L.</author><author>Adkins, R. H.</author><author>Yakura, J. S.</author><author>Sie, I.</author></authors></contributors><auth-address>Regional Spinal Cord Injury Care System of Southern California, Rancho Los Amigos Medical Center, Downey 90242.</auth-address><titles><title>Motor and sensory recovery following incomplete paraplegia</title><secondary-title>Arch Phys Med Rehabil</secondary-title><alt-title>Archives of physical medicine and rehabilitation</alt-title></titles><periodical><full-title>Arch Phys Med Rehabil</full-title></periodical><pages>67-72</pages><volume>75</volume><number>1</number><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Motor Neurons/physiology</keyword><keyword>Neurologic Examination</keyword><keyword>Neurons, Afferent/physiology</keyword><keyword>Paraplegia/*physiopathology/*rehabilitation</keyword><keyword>Psychomotor Performance/*physiology</keyword><keyword>Spinal Cord Injuries/*physiopathology/*rehabilitation</keyword><keyword>Time Factors</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>1994</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0003-9993 (Print)&#xD;0003-9993 (Linking)</isbn><accession-num>8291966</accession-num><urls><related-urls><url>;(1) and increased co-activation ADDIN EN.CITE <EndNote><Cite><Author>Lim</Author><Year>2005</Year><RecNum>35</RecNum><DisplayText>(2)</DisplayText><record><rec-number>35</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">35</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Lim, H. K.</author><author>Lee, D. C.</author><author>McKay, W. B.</author><author>Priebe, M. M.</author><author>Holmes, S. A.</author><author>Sherwood, A. M.</author></authors></contributors><auth-address>Baylor College of Medicine, Houston, TX 77030, USA.</auth-address><titles><title>Neurophysiological assessment of lower-limb voluntary control in incomplete spinal cord injury</title><secondary-title>Spinal Cord</secondary-title><alt-title>Spinal cord</alt-title></titles><pages>283-90</pages><volume>43</volume><number>5</number><keywords><keyword>Adult</keyword><keyword>Cross-Sectional Studies</keyword><keyword>Disability Evaluation</keyword><keyword>Electromyography/methods</keyword><keyword>Female</keyword><keyword>Functional Laterality/physiology</keyword><keyword>Humans</keyword><keyword>Lower Extremity/*physiopathology</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Muscle, Skeletal/*physiopathology</keyword><keyword>Neurophysiology</keyword><keyword>Psychomotor Performance/*physiology</keyword><keyword>ROC Curve</keyword><keyword>Reproducibility of Results</keyword><keyword>Retrospective Studies</keyword><keyword>Sensitivity and Specificity</keyword><keyword>Spinal Cord Injuries/*physiopathology</keyword></keywords><dates><year>2005</year><pub-dates><date>May</date></pub-dates></dates><isbn>1362-4393 (Print)&#xD;1362-4393 (Linking)</isbn><accession-num>15672098</accession-num><urls><related-urls><url>;(2) of the muscles around ankle joint ADDIN EN.CITE <EndNote><Cite><Author>Dietz</Author><Year>1995</Year><RecNum>19</RecNum><DisplayText>(3)</DisplayText><record><rec-number>19</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">19</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Dietz, V.</author><author>Colombo, G.</author><author>Jensen, L.</author><author>Baumgartner, L.</author></authors></contributors><auth-address>Paraplegic Centre, University Hospital Balgrist, Zurich, Switzerland.</auth-address><titles><title>Locomotor capacity of spinal cord in paraplegic patients</title><secondary-title>Ann Neurol</secondary-title><alt-title>Annals of neurology</alt-title></titles><pages>574-82</pages><volume>37</volume><number>5</number><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Electromyography</keyword><keyword>Exercise Therapy</keyword><keyword>Humans</keyword><keyword>Locomotion/drug effects/*physiology</keyword><keyword>Middle Aged</keyword><keyword>Paraplegia/etiology/*physiopathology/rehabilitation</keyword><keyword>Spinal Cord/*physiopathology</keyword><keyword>Spinal Cord Injuries/complications/physiopathology/rehabilitation</keyword></keywords><dates><year>1995</year><pub-dates><date>May</date></pub-dates></dates><isbn>0364-5134 (Print)&#xD;0364-5134 (Linking)</isbn><accession-num>7755351</accession-num><urls><related-urls><url>;(3). Appropriate ankle joint control plays an important role in independent walking, as it is crucial to maintain body weight support during gait ADDIN EN.CITE <EndNote><Cite><Author>Gottschall</Author><Year>2003</Year><RecNum>12</RecNum><DisplayText>(4)</DisplayText><record><rec-number>12</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">12</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Gottschall, J. S.</author><author>Kram, R.</author></authors></contributors><auth-address>Department of Kinesiology and Applied Physiology, University of Colorado, Boulder, Colorado 80309, USA. gottscha@ucsu.colorado.edu</auth-address><titles><title>Energy cost and muscular activity required for propulsion during walking</title><secondary-title>J Appl Physiol</secondary-title><alt-title>Journal of applied physiology</alt-title></titles><pages>1766-72</pages><volume>94</volume><number>5</number><keywords><keyword>Adult</keyword><keyword>Ankle/physiology</keyword><keyword>Biomechanics</keyword><keyword>Body Weight/physiology</keyword><keyword>Electromyography</keyword><keyword>Energy Metabolism/*physiology</keyword><keyword>Female</keyword><keyword>Gait/physiology</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Muscle, Skeletal/*physiology</keyword><keyword>Oxygen Consumption/physiology</keyword><keyword>Walking/*physiology</keyword></keywords><dates><year>2003</year><pub-dates><date>May</date></pub-dates></dates><isbn>8750-7587 (Print)&#xD;0161-7567 (Linking)</isbn><accession-num>12506042</accession-num><urls><related-urls><url>;(4). In particular, the dorsi-flexor (DF) muscles that act around the ankle joint play a crucial role in controlling the foot trajectory during the swing phase to ensure adequate foot clearance ADDIN EN.CITE <EndNote><Cite><Author>Donelan</Author><Year>2002</Year><RecNum>13</RecNum><DisplayText>(5)</DisplayText><record><rec-number>13</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">13</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Donelan, J. M.</author><author>Kram, R.</author><author>Kuo, A. D.</author></authors></contributors><auth-address>Department of Integrative Biology, University of California, Berkeley, CA 94720-3140, USA.</auth-address><titles><title>Mechanical work for step-to-step transitions is a major determinant of the metabolic cost of human walking</title><secondary-title>J Exp Biol</secondary-title><alt-title>The Journal of experimental biology</alt-title></titles><pages>3717-27</pages><volume>205</volume><number>Pt 23</number><keywords><keyword>Biomechanics</keyword><keyword>Calorimetry, Indirect</keyword><keyword>Energy Metabolism</keyword><keyword>Humans</keyword><keyword>Kinetics</keyword><keyword>Linear Models</keyword><keyword>Mathematics</keyword><keyword>Models, Biological</keyword><keyword>Oxygen Consumption</keyword><keyword>Physical Exertion/physiology</keyword><keyword>Regression Analysis</keyword><keyword>Walking/*physiology</keyword></keywords><dates><year>2002</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>0022-0949 (Print)&#xD;0022-0949 (Linking)</isbn><accession-num>12409498</accession-num><urls><related-urls><url>;(5), and the plantar-flexor (PF) muscles are critical for propulsive force generation at the end of the stance phasePEVuZE5vdGU+PENpdGU+PEF1dGhvcj5OZXB0dW5lPC9BdXRob3I+PFllYXI+MjAwMTwvWWVhcj48

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ADDIN EN.CITE.DATA (7, 8). Given the mechanical power deficits during gait in chronic iSCI subjects ADDIN EN.CITE <EndNote><Cite><Author>Dietz</Author><Year>1995</Year><RecNum>19</RecNum><DisplayText>(3)</DisplayText><record><rec-number>19</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">19</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Dietz, V.</author><author>Colombo, G.</author><author>Jensen, L.</author><author>Baumgartner, L.</author></authors></contributors><auth-address>Paraplegic Centre, University Hospital Balgrist, Zurich, Switzerland.</auth-address><titles><title>Locomotor capacity of spinal cord in paraplegic patients</title><secondary-title>Ann Neurol</secondary-title><alt-title>Annals of neurology</alt-title></titles><pages>574-82</pages><volume>37</volume><number>5</number><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Electromyography</keyword><keyword>Exercise Therapy</keyword><keyword>Humans</keyword><keyword>Locomotion/drug effects/*physiology</keyword><keyword>Middle Aged</keyword><keyword>Paraplegia/etiology/*physiopathology/rehabilitation</keyword><keyword>Spinal Cord/*physiopathology</keyword><keyword>Spinal Cord Injuries/complications/physiopathology/rehabilitation</keyword></keywords><dates><year>1995</year><pub-dates><date>May</date></pub-dates></dates><isbn>0364-5134 (Print)&#xD;0364-5134 (Linking)</isbn><accession-num>7755351</accession-num><urls><related-urls><url>;(3), improving paretic ankle control may considerably improve walking performance.Several studies have shown that robotic-assisted body weight supported treadmill training (BWSTT) using the Lokomat (Hocoma Inc., Zurich, Switzerland) – a motorized exoskeleton that drives the patient’s legs over a treadmill –can improve over-ground walking ability in individuals with chronic iSCI PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Nb3Jhd2lldHo8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFy

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ADDIN EN.CITE.DATA (9-11). Fundamentally, the motorized exoskeleton replaces the manual assistance provided by therapists with repetitive, guided and task-specific stepping ADDIN EN.CITE <EndNote><Cite><Author>Patritti</Author><Year>2010</Year><RecNum>25</RecNum><DisplayText>(12)</DisplayText><record><rec-number>25</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">25</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Patritti, B.</author><author>Sicari, M.</author><author>Deming, L.</author><author>Romaguera, F.</author><author>Pelliccio, M.</author><author>Benedetti, M. G.</author><author>Nimec, D.</author><author>Bonato, P.</author></authors></contributors><auth-address>Department of Physical Medicine and Rehabilitation, Harvard Medical School, Spaulding Rehabilitation Hospital, Boston, MA 02114, USA. bpatritti@srh-</auth-address><titles><title>Enhancing robotic gait training via augmented feedback</title><secondary-title>Conf Proc IEEE Eng Med Biol Soc</secondary-title><alt-title>Conference proceedings : ... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Conference</alt-title></titles><pages>2271-4</pages><volume>2010</volume><keywords><keyword>Biomechanics</keyword><keyword>Biomedical Engineering/methods</keyword><keyword>Cerebral Palsy/*rehabilitation</keyword><keyword>Child</keyword><keyword>Exercise Therapy/methods</keyword><keyword>*Feedback</keyword><keyword>*Gait</keyword><keyword>Humans</keyword><keyword>Monitoring, Physiologic/*instrumentation/methods</keyword><keyword>Motion</keyword><keyword>Motor Skills</keyword><keyword>*Robotics</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2010</year></dates><isbn>1557-170X (Print)&#xD;1557-170X (Linking)</isbn><accession-num>21097013</accession-num><urls><related-urls><url>;(12), by moving the individuals’ legs in a pre-programmed, physiological gait pattern. The advantages of using such systems include providing training for a longer duration with more physiological and reproducible gait patterns, and quantification of walking performance over the course of recovery ADDIN EN.CITE <EndNote><Cite><Author>Schwartz</Author><Year>2011</Year><RecNum>26</RecNum><DisplayText>(13)</DisplayText><record><rec-number>26</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">26</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Schwartz, I.</author><author>Sajina, A.</author><author>Neeb, M.</author><author>Fisher, I.</author><author>Katz-Luerer, M.</author><author>Meiner, Z.</author></authors></contributors><auth-address>Department of Physical Medicine and Rehabilitation, Hadassah University Hospital, Jerusalem, Israel.</auth-address><titles><title>Locomotor training using a robotic device in patients with subacute spinal cord injury</title><secondary-title>Spinal Cord</secondary-title><alt-title>Spinal cord</alt-title></titles><pages>1062-7</pages><volume>49</volume><number>10</number><keywords><keyword>Acute Disease</keyword><keyword>Adult</keyword><keyword>Case-Control Studies</keyword><keyword>Exercise Therapy/instrumentation/*methods</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Motor Activity/*physiology</keyword><keyword>Paraplegia/etiology/physiopathology/*rehabilitation</keyword><keyword>Quadriplegia/etiology/physiopathology/*rehabilitation</keyword><keyword>Robotics/*methods</keyword><keyword>Spinal Cord Injuries/physiopathology/*rehabilitation</keyword><keyword>Young Adult</keyword></keywords><dates><year>2011</year><pub-dates><date>Oct</date></pub-dates></dates><isbn>1476-5624 (Electronic)&#xD;1362-4393 (Linking)</isbn><accession-num>21625239</accession-num><urls><related-urls><url>;(13). To date, the effectiveness of a robotic-assisted locomotor training (RALT) protocol has mostly been quantified using clinical walking performance measures such as walking speed ADDIN EN.CITE <EndNote><Cite><Author>Niu</Author><Year>2012</Year><RecNum>39</RecNum><DisplayText>(14)</DisplayText><record><rec-number>39</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">39</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Niu, X.</author><author>Varoqui, D.</author><author>Kindig, M.</author><author>Mirbagheri, M. M.</author></authors></contributors><auth-address>Deptartment of Physical Medicine and Rehabilitation, Northwestern University.</auth-address><titles><title>The effect of robot-assisted locomotor training on walking speed</title><secondary-title>Conf Proc IEEE Eng Med Biol Soc</secondary-title><alt-title>Conference proceedings : ... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Conference</alt-title></titles><pages>3858-61</pages><volume>2012</volume><dates><year>2012</year></dates><isbn>1557-170X (Print)&#xD;1557-170X (Linking)</isbn><accession-num>23366770</accession-num><urls><related-urls><url>;(14), endurance, and functional independence ADDIN EN.CITE <EndNote><Cite><Author>Wirz</Author><Year>2005</Year><RecNum>33</RecNum><DisplayText>(15)</DisplayText><record><rec-number>33</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">33</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Wirz, M.</author><author>Zemon, D. H.</author><author>Rupp, R.</author><author>Scheel, A.</author><author>Colombo, G.</author><author>Dietz, V.</author><author>Hornby, T. G.</author></authors></contributors><auth-address>Spinal Cord Injury Center, Balgrist University Hospital, Zurich, Switzerland.</auth-address><titles><title>Effectiveness of automated locomotor training in patients with chronic incomplete spinal cord injury: a multicenter trial</title><secondary-title>Arch Phys Med Rehabil</secondary-title><alt-title>Archives of physical medicine and rehabilitation</alt-title></titles><periodical><full-title>Arch Phys Med Rehabil</full-title></periodical><pages>672-80</pages><volume>86</volume><number>4</number><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Chronic Disease</keyword><keyword>Female</keyword><keyword>Gait</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>*Orthotic Devices</keyword><keyword>Robotics</keyword><keyword>Spinal Cord Injuries/*rehabilitation</keyword><keyword>Task Performance and Analysis</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2005</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>0003-9993 (Print)&#xD;0003-9993 (Linking)</isbn><accession-num>15827916</accession-num><urls><related-urls><url>;(15). 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ADDIN EN.CITE.DATA (11, 16). Consequently, the purpose of this study was to quantify the effects of a 4-week RALT protocol on ankle motor control during MVC contraction (as assessed by the net joint torque and muscular co-activation), and on overall walking performance measures (as assessed by clinical walking assessments) in chronic iSCI. We hypothesized that, when compared to a matched- control group, the RALT group would show improved torque, reduced co-activation of the ankle joint, and enhanced walking performance. We also expected that there would be a positive correlation between the ankle control measures and the walking performance measures, in general. METHODSThirty two ambulatory chronic iSCI participants with incomplete motor function loss were recruited to participate in this study. Half of the participants underwent a 4-week RALT protocol (50.81 ± 7.93 years) and the other half were assigned to the Control group (49.4 ± 11.28 years). The groups were matched by age, time since injury, muscle tone at the ankle plantar-flexors (as assessed by Modified Ashworth Scale (MAS) ADDIN EN.CITE <EndNote><Cite><Author>Ashworth</Author><Year>1964</Year><RecNum>44</RecNum><DisplayText>(17)</DisplayText><record><rec-number>44</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">44</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ashworth, B.</author></authors></contributors><titles><title>Preliminary Trial of Carisoprodol in Multiple Sclerosis</title><secondary-title>Practitioner</secondary-title><alt-title>The Practitioner</alt-title></titles><pages>540-2</pages><volume>192</volume><keywords><keyword>*Biomedical Research</keyword><keyword>*Carisoprodol</keyword><keyword>*Multiple Sclerosis</keyword></keywords><dates><year>1964</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>0032-6518 (Print)&#xD;0032-6518 (Linking)</isbn><accession-num>14143329</accession-num><urls><related-urls><url>;(17)) and walking ability (Walking Index for Spinal Cord Injury II (WISCI II)PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EaXR1bm5vPC9BdXRob3I+PFllYXI+MjAwMDwvWWVhcj48

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ADDIN EN.CITE.DATA (18, 19)). Detailed demographic characteristics for both groups are presented in Table 1. The following inclusion criteria were met by the participants: (a) motor-incomplete SCI with an American Spinal Injury Association impairment scale (AIS) classification of C or D, (b) level of injury above T10, (c) partial to full ambulatory capacity (i.e., the ability to take at least two steps independently), (d) passive range of motion of the lower extremity within functional limits for ambulation, and (e) medical clearance to participate in the experiment. Subjects were recruited from the outpatient service of the Rehabilitation Institute of Chicago. The experimental procedure was approved by the Northwestern University Institutional Review Board and the participants provided their informed consent. RALT protocolThe RALT group participated in locomotor training using the Lokomat three times a week over four weeks, for a total of twelve training sessions ADDIN EN.CITE <EndNote><Cite><Author>Mirbagheri</Author><Year>2012</Year><RecNum>38</RecNum><DisplayText>(11)</DisplayText><record><rec-number>38</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">38</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Mirbagheri, M. M.</author><author>Niu, X.</author><author>Kindig, M.</author><author>Varoqui, D.</author></authors></contributors><auth-address>Rehabilitation Institute of Chicago, IL, USA. mehdi@northwestern.edu</auth-address><titles><title>The effects of locomotor training with a robotic-gait orthosis (Lokomat) on neuromuscular properties in persons with chronic SCI</title><secondary-title>Conf Proc IEEE Eng Med Biol Soc</secondary-title><alt-title>Conference proceedings : ... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Conference</alt-title></titles><pages>3854-7</pages><volume>2012</volume><dates><year>2012</year></dates><isbn>1557-170X (Print)&#xD;1557-170X (Linking)</isbn><accession-num>23366769</accession-num><urls><related-urls><url>;(11). Each session lasted one hour, including set-up time, with 30 to 45 minutes of training. < Figure 1 is about here>For the RALT protocol, in accordance to the individual’s tolerance, the treadmill speed was increased from 1.5 km/h to 3.0 km/h, over the course of training. In addition, the guidance force was progressively reduced during the training (from full to 20% assistance), as tolerated by the subject. During the training session, the ankle was held in a neutral position (90? angle between the leg and foot) by spring-supported stirrups that supported the plantar surface of the foot and connected to the knee orthosis of the exoskeleton. The upright weight bearing position on the neutral foot with a slight closed kinematic tibial tilt provided a stimulation to both dorsi- and plantar-flexors to activate while walking. A mirror was placed before the patient to allow for self-monitoring of his/her leg movements during the training, and the physical therapist provided encouraging verbal feedback throughout the training.Experimental setup and Instrumentation The participants’ ankle motor control was evaluated using MVC assessments on the first day of training and on the last day of training. Each participant was seated in an experimental chair with the thigh strapped to the chair base (Figure 2). The bare-foot was secured to a rigid footrest attached to the rotational axis of a servomotor. The seat, footrest, and motor were adjusted such that the ankle was kept in the neutral position, while the knee joint was flexed at 60?. A 6-axis torque transducer recorded net joint torque of the ankle. Torque data were sampled at 1 kHz by a 16 bit A/D converter (National Instruments, Austin TX), and passed through a 230 Hz anti-aliasing filter on-line. The isometric testing procedure from the experimental setup is valid and the results have been well published PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NaXJiYWdoZXJpPC9BdXRob3I+PFllYXI+MjAxMjwvWWVh

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ADDIN EN.CITE.DATA (11, 14). Surface electromyography (EMG) was recorded from the tibialis anterior (DF muscle) and gastrocnemius (PF muscle) via bipolar surface electrodes [DE 2.1 Single Differential Surface EMG Sensor, Delsys, Inc., Boston MA, USA]. Prior to the experiment, the skin area was cleaned by isopropyl alcohol. EMG signals were sampled at 1 kHz, and amplified (gain 10,000) and low-pass filtered at 230 Hz.< Figure 2 is about here>ProcedureParticipants were instructed to perform a 5-second MVC ‘as hard as possible’ in each direction by lifting their toes up (DF) or by pushing down with their toes onto the footrest (PF). The MVC during the dorsi- flexion contraction determined the isometric torque for the DF (TDF) while MVC during the plantar-flexion contraction determined the isometric torque for the PF (TPF). We did not assess the EMG activation of DF and PF muscles during the training. Data analysisData analysis was carried out using Matlab (The Mathworks, Natick, USA). Prior to further analyses, torque signals were low-pass filtered with a cut-off frequency of 5 Hz. Isometric torque was calculated as the average torque during the middle 3-s window for each contraction direction (TDF and TPF). EMG signals of both DF and PF muscles were full wave rectified and low-pass filtered using a 4th order, zero-lag Butterworth filter at 10 Hz. Baseline noise of the initial 1-s, when the subject was relaxed, was subtracted from the respective filtered EMG signals. To facilitate comparisons across subjects, EMG values for each muscle were normalized to the peak activity of the respective muscles for each subject. Finally, the co-activation for dorsi-flexion (CADF) and plantar-flexion (CAPF) during MVC was calculated based on previous literature ADDIN EN.CITE <EndNote><Cite><Author>Kellis</Author><Year>2003</Year><RecNum>47</RecNum><DisplayText>(20)</DisplayText><record><rec-number>47</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">47</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Kellis, E.</author><author>Arabatzi, F.</author><author>Papadopoulos, C.</author></authors></contributors><auth-address>Department of Physical Education and Sport Sciences at Serres, Aristotle University of Thessaloniki, Serres, Greece. ekellis@phed-sr.auth.gr</auth-address><titles><title>Muscle co-activation around the knee in drop jumping using the co-contraction index</title><secondary-title>J Electromyogr Kinesiol</secondary-title><alt-title>Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology</alt-title></titles><pages>229-38</pages><volume>13</volume><number>3</number><keywords><keyword>Adult</keyword><keyword>Humans</keyword><keyword>*Knee</keyword><keyword>Male</keyword><keyword>*Muscle Contraction</keyword><keyword>Muscle, Skeletal/*physiology</keyword><keyword>Track and Field/*physiology</keyword></keywords><dates><year>2003</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>1050-6411 (Print)&#xD;1050-6411 (Linking)</isbn><accession-num>12706603</accession-num><urls><related-urls><url>;(20). To assess the participants’ functional ambulation capacity, a total of three clinical evaluations were performed pre- and post-training: the Timed Up and Go test (TUG) ADDIN EN.CITE <EndNote><Cite><Author>Bohannon</Author><Year>2006</Year><RecNum>82</RecNum><DisplayText>(21)</DisplayText><record><rec-number>82</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">82</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bohannon, R. W.</author></authors></contributors><auth-address>Neag School of Education, University of Connecticut, Storrs, CT, USA. ptconsultant@</auth-address><titles><title>Reference values for the timed up and go test: a descriptive meta-analysis</title><secondary-title>J Geriatr Phys Ther</secondary-title><alt-title>Journal of geriatric physical therapy</alt-title></titles><pages>64-8</pages><volume>29</volume><number>2</number><keywords><keyword>Aged</keyword><keyword>Aged, 80 and over</keyword><keyword>*Geriatric Assessment</keyword><keyword>Humans</keyword><keyword>*Locomotion</keyword><keyword>Reference Values</keyword></keywords><dates><year>2006</year></dates><isbn>1539-8412 (Print)&#xD;1539-8412 (Linking)</isbn><accession-num>16914068</accession-num><urls><related-urls><url>;(21), the 10-meter walk test (10MWT) ADDIN EN.CITE <EndNote><Cite><Author>Jackson</Author><Year>2008</Year><RecNum>83</RecNum><DisplayText>(22)</DisplayText><record><rec-number>83</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">83</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Jackson, A. B.</author><author>Carnel, C. T.</author><author>Ditunno, J. F.</author><author>Read, M. S.</author><author>Boninger, M. L.</author><author>Schmeler, M. R.</author><author>Williams, S. R.</author><author>Donovan, W. H.</author><author>Gait,</author><author>Ambulation, Subcommittee</author></authors></contributors><auth-address>Department of Physical Medicine and Rehabilitation, University of Alabama, Birmingham, AL 35213, USA.</auth-address><titles><title>Outcome measures for gait and ambulation in the spinal cord injury population</title><secondary-title>J Spinal Cord Med</secondary-title><alt-title>The journal of spinal cord medicine</alt-title></titles><pages>487-99</pages><volume>31</volume><number>5</number><keywords><keyword>Disability Evaluation</keyword><keyword>Gait/*physiology</keyword><keyword>Humans</keyword><keyword>*Outcome Assessment (Health Care)</keyword><keyword>Reproducibility of Results</keyword><keyword>Sensitivity and Specificity</keyword><keyword>Severity of Illness Index</keyword><keyword>*Spinal Cord Injuries/epidemiology/physiopathology/therapy</keyword><keyword>Walking/*physiology</keyword></keywords><dates><year>2008</year></dates><isbn>1079-0268 (Print)&#xD;1079-0268 (Linking)</isbn><accession-num>19086706</accession-num><urls><related-urls><url>;(22), and the 6-minute walk test (6MWT) ADDIN EN.CITE <EndNote><Cite><Author>Bellet</Author><Year>2012</Year><RecNum>85</RecNum><DisplayText>(23)</DisplayText><record><rec-number>85</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="1452274598">85</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bellet, R. N.</author><author>Adams, L.</author><author>Morris, N. R.</author></authors></contributors><auth-address>Physiotherapy Department, The Prince Charles Hospital, Metro North Health Service District, Brisbane, Queensland, Australia. Nicole_Bellet@health..au</auth-address><titles><title>The 6-minute walk test in outpatient cardiac rehabilitation: validity, reliability and responsiveness--a systematic review</title><secondary-title>Physiotherapy</secondary-title></titles><periodical><full-title>Physiotherapy</full-title></periodical><pages>277-86</pages><volume>98</volume><number>4</number><keywords><keyword>Ambulatory Care/*standards</keyword><keyword>Coronary Artery Disease/*rehabilitation</keyword><keyword>Exercise Test/*standards</keyword><keyword>Humans</keyword><keyword>Physical Therapy Modalities/*standards</keyword><keyword>Reproducibility of Results</keyword><keyword>*Walking</keyword></keywords><dates><year>2012</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>1873-1465 (Electronic)&#xD;0031-9406 (Linking)</isbn><accession-num>23122432</accession-num><urls><related-urls><url>;(23). The participants walked with their usual walking aids. The isometric torques (TDF and TPF), co-activations (CADF and CAPF) and the clinical evaluations were performed at the same two time points as the MVC, i.e., before training (baseline) and after 4-weeks. Baseline scores for both RALT and control groups are presented in Table 1. Statistical analysisData were presented as mean and standard errors within each group. Kolmogorov-Smirnov tests of normality were used to test the normality of the data. Wherever the normality was violated, non-parametric tests were used in the analysis. To test the homogeneity between the control and RALT groups at the time of inclusion, we used Mann-Whitney tests on the following continuous variables: age, lesion duration, WISCI II, TUG, 10MWT and 6MWT. Chi-square tests were performed on the categorical (level of lesion) and ordinal variables (MAS).We performed paired sample t-tests to compare the values at baseline and at 4-weeks for both the RALT and the control groups separately. Effect size was assessed with standardized response mean (SRM) ADDIN EN.CITE <EndNote><Cite><Author>Liang</Author><Year>1990</Year><RecNum>20</RecNum><DisplayText>(24)</DisplayText><record><rec-number>20</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">20</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Liang, M. H.</author><author>Fossel, A. H.</author><author>Larson, M. G.</author></authors></contributors><auth-address>Department of Medicine, Harvard Medical School, Boston, MA.</auth-address><titles><title>Comparisons of five health status instruments for orthopedic evaluation</title><secondary-title>Med Care</secondary-title><alt-title>Medical care</alt-title></titles><pages>632-42</pages><volume>28</volume><number>7</number><keywords><keyword>Aged</keyword><keyword>Aged, 80 and over</keyword><keyword>Boston</keyword><keyword>Evaluation Studies as Topic</keyword><keyword>Female</keyword><keyword>Follow-Up Studies</keyword><keyword>*Health Status Indicators</keyword><keyword>*Hip Prosthesis/adverse effects</keyword><keyword>Hospital Bed Capacity, 500 and over</keyword><keyword>Humans</keyword><keyword>*Knee Prosthesis/adverse effects</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Outcome and Process Assessment (Health Care)/*methods/statistics &amp; numerical data</keyword><keyword>Pain/etiology</keyword><keyword>Questionnaires</keyword></keywords><dates><year>1990</year><pub-dates><date>Jul</date></pub-dates></dates><isbn>0025-7079 (Print)&#xD;0025-7079 (Linking)</isbn><accession-num>2366602</accession-num><urls><related-urls><url>;(24) for torque and co-activation data, where the mean pre-post RALT training change was divided by the standard deviation of the change. Based on Cohen’s criteria, SRM values of 0.20, 0.50 and 0.80 indicate small, moderate and large effects, respectively ADDIN EN.CITE <EndNote><Cite><Author>Liang</Author><Year>1990</Year><RecNum>20</RecNum><DisplayText>(24)</DisplayText><record><rec-number>20</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">20</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Liang, M. H.</author><author>Fossel, A. H.</author><author>Larson, M. G.</author></authors></contributors><auth-address>Department of Medicine, Harvard Medical School, Boston, MA.</auth-address><titles><title>Comparisons of five health status instruments for orthopedic evaluation</title><secondary-title>Med Care</secondary-title><alt-title>Medical care</alt-title></titles><pages>632-42</pages><volume>28</volume><number>7</number><keywords><keyword>Aged</keyword><keyword>Aged, 80 and over</keyword><keyword>Boston</keyword><keyword>Evaluation Studies as Topic</keyword><keyword>Female</keyword><keyword>Follow-Up Studies</keyword><keyword>*Health Status Indicators</keyword><keyword>*Hip Prosthesis/adverse effects</keyword><keyword>Hospital Bed Capacity, 500 and over</keyword><keyword>Humans</keyword><keyword>*Knee Prosthesis/adverse effects</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Outcome and Process Assessment (Health Care)/*methods/statistics &amp; numerical data</keyword><keyword>Pain/etiology</keyword><keyword>Questionnaires</keyword></keywords><dates><year>1990</year><pub-dates><date>Jul</date></pub-dates></dates><isbn>0025-7079 (Print)&#xD;0025-7079 (Linking)</isbn><accession-num>2366602</accession-num><urls><related-urls><url>;(24). The pre-post RALT training change was determined by subtracting the baseline from the 4-week measure. To determine the effect of the RALT on the walking performance (second hypothesis), Wilcoxon signed-rank tests were performed on baseline and 4-week data independently for each group for each of the walking assessments (TUG, 10MWT and 6MWT) as they were non-normally distributed. We also used Spearman rank correlation analysis to determine the relationships between the three walking capacity measures (i.e., TUG, 10MWT and 6MWT) and the ankle’s isometric and co-activation measures at baseline. All statistical tests were performed using SPSS v.21 (SPSS Inc., Chicago, USA) with a significance (alpha) level of 0.05. RESULTSDemographic characteristicsBoth the RALT and the control groups were similar in demographic and clinical measures at the baseline evaluation. There was no difference between the groups in age (p=0.73), duration of lesion (p=0.42), level of lesion (χ2 = 0.1, p=0.72), walking capacity as measured by WISCI II (p=.70), plantar muscle tone as assessed by MAS (χ2 = 7.7, p=0.10), TUG (p=0.14), 10MWT (p=0.59), and 6MWT (p=0.34). <Table. 1 is about here>Isometric Torque, Co-activations and Clinical MeasuresThe RALT group (Figure 3) showed an average increase of 20.7 ± 8.2% in TDF (p<0.05), and an average increase of 22.4 ± 9.4% in TPF (p<0.05), with a moderate training effect size (SRM=0.57) for both. In contrast, for the control group, no statistically significant difference was found between the baseline and 4-weeks for both TDF (p=0.86) and TPF (p=0.14). The RALT group showed a reduction in the co-activation of the PF muscle after one month of RALT training; this training effect was moderate (SRM=0.53). We did not see any statistically significant reduction between the baseline and 4-weeks for the control CADF (p=0.64) and CADF (p=0.31) as well as for the RALT CAPF (p=0.62). < Figure 3 is about here>The TUG showed a significant reduction of 13.9 ± 3.2% (Figure 4) in the time needed to perform the task (p < 0.05) with a moderate effect size (SRM=0.54) for the RALT group. The 10MWT exhibited a significant increase in the mean over-ground gait speed (0.08 ± 0.02 m/s) after training (p < 0.05). This change corresponded to an improvement of 13.0 ± 2.6%, with a moderate effect size (SRM=0.71). However, no significant change (p = 0.33) was observed in walking endurance (6MWT). For the Control group, no statistically significant differences were found between the pre- and post-tests for TUG (p = 0.54), 10MWT (p = 0.45), and 6MWT (p = 0.34).< Figure 4 is about here>Relationship between ankle control measures and walking performanceIn order to show the important role of ankle control measures in walking performance, we combined both the baseline measures of intervention and control group together to do a correlation between the ankle control measures (torque and co-activation) and the walking performance (TUG, 10 MWT and 6 MWT). The correlation coefficients are presented in Table 2. All of the walking performance tests (walking mobility assessed by the TUG, over-ground walking speed measured by the 10MWT, and walking endurance assessed by the 6MWT) showed significant linear correlations with TDF and TPF (p < 0.05 for all). The correlation test implied that the muscle strength of the ankle is related to the clinical measures of walking. However, the walking performance measures did not show any correlations with the co-activation tests. < Table 2 is about here>DISCUSSIONIn this study, we evaluated changes in ankle control measures (torque and co-activation) during MVCs, along with walking performance in individuals with chronic incomplete SCI with and without RALT. For both the groups, clinical gait and ankle control measures were assessed at baseline and after 4 weeks to evaluate ankle impairment and walking performance. The RALT group who underwent twelve training sessions showed increased maximal torque during both dorsi- (TDF) and plantar-flexion (TPF) contractions. Moreover, co-activation during dorsiflexion decreased in the RALT group after training, whereas there were no changes in co-activation seen in plantarflexion. Regarding the clinical walking performance measures, RALT significantly improved walking mobility (TUG) and over-ground walking speed (10MWT) with no change in walking endurance. 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ADDIN EN.CITE.DATA (25). Our study extends that result by finding that RALT can improve voluntary torque for both the DF and PF muscle groups. Spinal cord injury causes a reduction in skeletal muscle fiber size ADDIN EN.CITE <EndNote><Cite><Author>Castro</Author><Year>1999</Year><RecNum>53</RecNum><DisplayText>(26)</DisplayText><record><rec-number>53</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">53</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Castro, M. J.</author><author>Apple, D. F., Jr.</author><author>Hillegass, E. A.</author><author>Dudley, G. A.</author></authors></contributors><auth-address>Department of Exercise Science, The University of Georgia, Athens 30602, USA.</auth-address><titles><title>Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury</title><secondary-title>Eur J Appl Physiol Occup Physiol</secondary-title><alt-title>European journal of applied physiology and occupational physiology</alt-title></titles><pages>373-8</pages><volume>80</volume><number>4</number><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Atrophy/pathology</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Leg/pathology</keyword><keyword>Magnetic Resonance Imaging</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Muscle, Skeletal/*pathology</keyword><keyword>Spinal Cord Injuries/*pathology</keyword><keyword>Thigh/pathology</keyword><keyword>Time Factors</keyword></keywords><dates><year>1999</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>0301-5548 (Print)&#xD;0301-5548 (Linking)</isbn><accession-num>10483809</accession-num><urls><related-urls><url>;(26) that is characterized by reduced strength due to lack of neural drive in individuals with iSCI ADDIN EN.CITE <EndNote><Cite><Author>Hillegass</Author><Year>1999</Year><RecNum>55</RecNum><DisplayText>(27)</DisplayText><record><rec-number>55</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">55</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Hillegass, E. A.</author><author>Dudley, G. A.</author></authors></contributors><auth-address>Department of Physical Therapy, Georgia State University, Atlanta 30303, USA.</auth-address><titles><title>Surface electrical stimulation of skeletal muscle after spinal cord injury</title><secondary-title>Spinal Cord</secondary-title><alt-title>Spinal cord</alt-title></titles><pages>251-7</pages><volume>37</volume><number>4</number><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Electric Stimulation</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Isometric Contraction/physiology</keyword><keyword>Leg/pathology/physiology</keyword><keyword>Magnetic Resonance Imaging</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Muscle Contraction/physiology</keyword><keyword>Muscle Fatigue/physiology</keyword><keyword>Muscle, Skeletal/pathology/*physiopathology</keyword><keyword>Spinal Cord Injuries/pathology/*physiopathology</keyword></keywords><dates><year>1999</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>1362-4393 (Print)&#xD;1362-4393 (Linking)</isbn><accession-num>10338344</accession-num><urls><related-urls><url>;(27). Specifically in the ankle joint, a deficit in cortico-spinal voluntary activation of the DF musclePEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IYW5zZW48L0F1dGhvcj48WWVhcj4yMDA1PC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (7, 28), along with a specific increase in reciprocal inhibition from spastic triceps surae muscles ADDIN EN.CITE <EndNote><Cite><Author>Yanagisawa</Author><Year>1978</Year><RecNum>16</RecNum><DisplayText>(29)</DisplayText><record><rec-number>16</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">16</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Yanagisawa, N.</author><author>Tanaka, R.</author></authors></contributors><titles><title>Reciprocal Ia inhibition in spastic paralysis in man</title><secondary-title>Electroencephalogr Clin Neurophysiol Suppl</secondary-title><alt-title>Electroencephalography and clinical neurophysiology. Supplement</alt-title></titles><pages>521-6</pages><number>34</number><keywords><keyword>Brain/physiopathology</keyword><keyword>*H-Reflex</keyword><keyword>Hemiplegia/physiopathology</keyword><keyword>Humans</keyword><keyword>Motor Neurons/physiology</keyword><keyword>Muscle Spasticity/*physiopathology</keyword><keyword>*Neural Inhibition</keyword><keyword>Paralysis/*physiopathology</keyword><keyword>*Reflex, Monosynaptic</keyword><keyword>Reflex, Stretch</keyword><keyword>Spinal Cord Diseases/physiopathology</keyword></keywords><dates><year>1978</year></dates><isbn>0424-8155 (Print)&#xD;0424-8155 (Linking)</isbn><accession-num>285852</accession-num><urls><related-urls><url>;(29), could lead to weakness, reduced ability to produce torque and possibly reduced DF muscle fiber size ADDIN EN.CITE <EndNote><Cite><Author>Rochester</Author><Year>1995</Year><RecNum>52</RecNum><DisplayText>(30)</DisplayText><record><rec-number>52</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">52</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rochester, L.</author><author>Barron, M. J.</author><author>Chandler, C. S.</author><author>Sutton, R. A.</author><author>Miller, S.</author><author>Johnson, M. A.</author></authors></contributors><auth-address>Institute of Health Sciences, University of Northumbria at Newcastle, UK.</auth-address><titles><title>Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 2. Morphological and histochemical properties</title><secondary-title>Paraplegia</secondary-title><alt-title>Paraplegia</alt-title></titles><pages>514-22</pages><volume>33</volume><number>9</number><keywords><keyword>Adenosine Triphosphatases/metabolism</keyword><keyword>Adult</keyword><keyword>Capillaries/physiology</keyword><keyword>Creatine Kinase/metabolism</keyword><keyword>Electric Stimulation</keyword><keyword>Histocytochemistry</keyword><keyword>Humans</keyword><keyword>Muscle Fibers, Skeletal/enzymology/ultrastructure</keyword><keyword>Muscle, Skeletal/enzymology/pathology/*physiology</keyword><keyword>Myofibrils/enzymology</keyword><keyword>Oxidation-Reduction</keyword><keyword>Paraplegia/pathology/*physiopathology</keyword><keyword>Succinate Dehydrogenase/metabolism</keyword></keywords><dates><year>1995</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>0031-1758 (Print)&#xD;0031-1758 (Linking)</isbn><accession-num>8524604</accession-num><urls><related-urls><url>;(30). Nevertheless, we know that exercise training is beneficial in chronic iSCI, which improves skeletal muscle strength ADDIN EN.CITE <EndNote><Cite><Author>Hicks</Author><Year>2003</Year><RecNum>67</RecNum><DisplayText>(31)</DisplayText><record><rec-number>67</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">67</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Hicks, A. L.</author><author>Martin, K. A.</author><author>Ditor, D. S.</author><author>Latimer, A. E.</author><author>Craven, C.</author><author>Bugaresti, J.</author><author>McCartney, N.</author></authors></contributors><auth-address>Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada.</auth-address><titles><title>Long-term exercise training in persons with spinal cord injury: effects on strength, arm ergometry performance and psychological well-being</title><secondary-title>Spinal Cord</secondary-title><alt-title>Spinal cord</alt-title></titles><pages>34-43</pages><volume>41</volume><number>1</number><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Analysis of Variance</keyword><keyword>Arm/physiology</keyword><keyword>*Exercise Therapy</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Muscle, Skeletal/physiology</keyword><keyword>Pain Measurement</keyword><keyword>Physical Endurance</keyword><keyword>Quality of Life</keyword><keyword>Self Concept</keyword><keyword>Spinal Cord Injuries/*psychology/*rehabilitation</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2003</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>1362-4393 (Print)&#xD;1362-4393 (Linking)</isbn><accession-num>12494319</accession-num><urls><related-urls><url>;(31). By guiding the lower limb in a physiological step pattern and allowing upright weight bearing on the neutral positioned foot with a closed kinematic tibial tilt would have provided a stimulation to both dorsi- and plantar-flexors to activate while walking, a condition known to promote the best recovery of function ADDIN EN.CITE <EndNote><Cite><Author>Ada</Author><Year>2003</Year><RecNum>75</RecNum><DisplayText>(32)</DisplayText><record><rec-number>75</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">75</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ada, L.</author><author>Canning, C. G.</author><author>Low, S. L.</author></authors></contributors><auth-address>School of Physiotherapy, University of Sydney, Australia. l.ada@cchs.usyd.edu.au</auth-address><titles><title>Stroke patients have selective muscle weakness in shortened range</title><secondary-title>Brain</secondary-title><alt-title>Brain : a journal of neurology</alt-title></titles><pages>724-31</pages><volume>126</volume><number>Pt 3</number><keywords><keyword>Aged</keyword><keyword>Case-Control Studies</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>*Muscle Contraction</keyword><keyword>Muscle Weakness/*etiology</keyword><keyword>Stroke/*complications/physiopathology</keyword><keyword>Torque</keyword></keywords><dates><year>2003</year><pub-dates><date>Mar</date></pub-dates></dates><isbn>0006-8950 (Print)&#xD;0006-8950 (Linking)</isbn><accession-num>12566292</accession-num><urls><related-urls><url>;(32). RALT effects on co-activation at the ankle jointThe level of co-activation of the PF muscle decreased in RALT when compared to the controls after training. Increased antagonist co-activation in the ankle joint is prevalent in individuals with iSCI during dynamic controlled movement ADDIN EN.CITE <EndNote><Cite><Author>Knutsson</Author><Year>1997</Year><RecNum>71</RecNum><DisplayText>(33)</DisplayText><record><rec-number>71</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">71</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Knutsson, E.</author><author>Martensson, A.</author><author>Gransberg, L.</author></authors></contributors><auth-address>Department of Clinical Neurophysiology, Karolinska Hospital, Stockholm, Sweden.</auth-address><titles><title>Influences of muscle stretch reflexes on voluntary, velocity-controlled movements in spastic paraparesis</title><secondary-title>Brain</secondary-title><alt-title>Brain : a journal of neurology</alt-title></titles><pages>1621-33</pages><volume>120 ( Pt 9)</volume><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Electromyography</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Knee</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Movement/physiology</keyword><keyword>Multivariate Analysis</keyword><keyword>Muscle Contraction</keyword><keyword>Muscle, Skeletal/*physiopathology</keyword><keyword>Paraparesis, Tropical Spastic/*physiopathology</keyword><keyword>Reflex, Stretch/*physiology</keyword><keyword>Reproducibility of Results</keyword><keyword>Time Factors</keyword><keyword>Torque</keyword><keyword>Volition</keyword></keywords><dates><year>1997</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>0006-8950 (Print)&#xD;0006-8950 (Linking)</isbn><accession-num>9313644</accession-num><urls><related-urls><url>;(33) as well as in isometric contractions. During maximal isometric contractions, antagonist co-activation tends to reduce the efficiency of the agonist, increase the metabolic cost, and reduce the maximal net torque available to the joint ADDIN EN.CITE <EndNote><Cite><Author>Gomez-Soriano</Author><Year>2010</Year><RecNum>77</RecNum><DisplayText>(34)</DisplayText><record><rec-number>77</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">77</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Gomez-Soriano, J.</author><author>Castellote, J. M.</author><author>Perez-Rizo, E.</author><author>Esclarin, A.</author><author>Taylor, J. S.</author></authors></contributors><auth-address>Grupo Funcion Sensitivomotora, Hospital Nacional de Paraplejicos, SESCAM, Finca La Peraleda s/n, 45071 Toledo, Spain.</auth-address><titles><title>Voluntary ankle flexor activity and adaptive coactivation gain is decreased by spasticity during subacute spinal cord injury</title><secondary-title>Exp Neurol</secondary-title><alt-title>Experimental neurology</alt-title></titles><pages>507-16</pages><volume>224</volume><number>2</number><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Ankle/*physiopathology</keyword><keyword>Ankle Joint/*physiopathology</keyword><keyword>Electromyography</keyword><keyword>Humans</keyword><keyword>Longitudinal Studies</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>*Movement</keyword><keyword>Muscle Contraction</keyword><keyword>Muscle Spasticity/etiology/*physiopathology</keyword><keyword>Muscle Tonus</keyword><keyword>Muscle, Skeletal/*physiopathology</keyword><keyword>Pilot Projects</keyword><keyword>Recovery of Function</keyword><keyword>Spinal Cord Injuries/complications/*physiopathology</keyword><keyword>Torque</keyword><keyword>Young Adult</keyword></keywords><dates><year>2010</year><pub-dates><date>Aug</date></pub-dates></dates><isbn>1090-2430 (Electronic)&#xD;0014-4886 (Linking)</isbn><accession-num>20580713</accession-num><urls><related-urls><url>;(34). It has also been known that specific agonist training would be a source of improvement in performance and skill ADDIN EN.CITE <EndNote><Cite><Author>Basmajian.</Author><Year>1985</Year><RecNum>62</RecNum><DisplayText>(35)</DisplayText><record><rec-number>62</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">62</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>J Basmajian.</author><author>C DeLuca.</author></authors></contributors><titles><title>Muscles Alive: Their Functions Revealed by Electromyography</title></titles><edition>5th Edition</edition><section>pp 154, 223-244</section><dates><year>1985</year></dates><pub-location>Baltimore, MD</pub-location><publisher>Williams and Wilkins</publisher><urls></urls></record></Cite></EndNote>(35). We believe that through the RALT protocol’s weight bearing training, the level of PF co-activation could have decreased that in turn might have improved the efficiency of agonist. RALT effects on walking performanceFour weeks of RALT showed an improvement in the walking speed (10MWT) and walking mobility (TUG) in chronic iSCI individuals. This is in line with the observations seen with robotic-assisted gait devices that show a beneficial effect on walking capacity PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XaXJ6PC9BdXRob3I+PFllYXI+MjAwNTwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (15, 36). Of particular importance is the change seen in walking speed in our study after RALT training. The average increase in speed in 10MWT was around 0.08 m/s in the RALT group after four weeks, which was larger than the minimally important difference of 0.05 m/s reported by Musselman after BWSTT ADDIN EN.CITE <EndNote><Cite><Author>E</Author><Year>2007</Year><RecNum>79</RecNum><DisplayText>(37)</DisplayText><record><rec-number>79</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">79</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Kristin Musselman.</author></authors></contributors><titles><title>Clinical significance testing in rehabilitation research: what, why, and how?</title><secondary-title>Physical Therapy Reviews</secondary-title></titles><pages>287-296</pages><volume>12</volume><number>4</number><dates><year>2007</year></dates><urls></urls></record></Cite></EndNote>(37). The key factors that could have contributed to this notable improvement in walking speed and mobility could be (i) increased DF torque because of increased DF strength and decreased PF co-activation allowing for adequate foot clearance during the swing phase ADDIN EN.CITE <EndNote><Cite><Author>Barbeau</Author><Year>1987</Year><RecNum>27</RecNum><DisplayText>(38)</DisplayText><record><rec-number>27</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">27</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Barbeau, H.</author><author>Rossignol, S.</author></authors></contributors><titles><title>Recovery of locomotion after chronic spinalization in the adult cat</title><secondary-title>Brain Res</secondary-title><alt-title>Brain research</alt-title></titles><pages>84-95</pages><volume>412</volume><number>1</number><keywords><keyword>Adaptation, Physiological</keyword><keyword>Animals</keyword><keyword>Back</keyword><keyword>Cats</keyword><keyword>*Decerebrate State</keyword><keyword>Electromyography</keyword><keyword>Extremities</keyword><keyword>Gait</keyword><keyword>*Locomotion</keyword><keyword>Male</keyword><keyword>Muscles/physiology</keyword></keywords><dates><year>1987</year><pub-dates><date>May 26</date></pub-dates></dates><isbn>0006-8993 (Print)&#xD;0006-8993 (Linking)</isbn><accession-num>3607464</accession-num><urls><related-urls><url>;(38), and (ii) increased PF torque due to the strengthened ankle PF muscle that provides most of the energy required for body propulsion ADDIN EN.CITE <EndNote><Cite><Author>Neptune</Author><Year>2001</Year><RecNum>11</RecNum><DisplayText>(6)</DisplayText><record><rec-number>11</rec-number><foreign-keys><key app="EN" db-id="vs9e0d2spfe5axe5a0h5s22udvwwx9se0p5r" timestamp="0">11</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Neptune, R. R.</author><author>Kautz, S. A.</author><author>Zajac, F. E.</author></authors></contributors><auth-address>Rehabilitation R &amp; D Center (153), VA Palo Alto Health Care System, 3801 Miranda Avenue, Palo Alto, CA 94304, USA. rneptune@mail.utexas.edu</auth-address><titles><title>Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking</title><secondary-title>J Biomech</secondary-title><alt-title>Journal of biomechanics</alt-title></titles><pages>1387-98</pages><volume>34</volume><number>11</number><keywords><keyword>Adult</keyword><keyword>Ankle/anatomy &amp; histology/*physiology</keyword><keyword>Ankle Joint/physiology</keyword><keyword>Biomechanics</keyword><keyword>Computer Simulation</keyword><keyword>Gait/physiology</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Models, Biological</keyword><keyword>Muscle, Skeletal/*physiology</keyword><keyword>Walking/*physiology</keyword></keywords><dates><year>2001</year><pub-dates><date>Nov</date></pub-dates></dates><isbn>0021-9290 (Print)&#xD;0021-9290 (Linking)</isbn><accession-num>11672713</accession-num><urls><related-urls><url>;(6). The failure to see changes in the 6MWT may be explained by the nature of the test itself as it is an endurance based test. In addition, the short duration of training in our study would have also contributed in not seeing any changes. Especially in RALT studies, a substantial gain in walking endurance is seen with training durations that were twice as long as in our studyPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XaXJ6PC9BdXRob3I+PFllYXI+MjAwNTwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (15, 39). Study LimitationsOur study had a few limitations. Our control group was inactive and therefore the increase in function we saw in the RALT group could have been due to doing more activity in the intervention group. We also focused on only the ankle joint, which can play a significant role in gait impairment. Future work could be aimed at studying other relevant joints involved in ambulation, such as the knee and the hip joints. ConclusionIn this study of individuals with chronic iSCI, 12 training sessions of RALT resulted in ~20% increases in the net joint torque, decreased co-activation in the ankle joint, and increased walking mobility (assessed by TUG) and speed (assessed by 10MWT). These improvements in the ankle joint after RALT are clinically meaningful given the ankle’s purported role in a functional task such as walking. The relationship seen between ankle torque and the walking measures is a noteworthy observation that positively emphasizes the importance of the ankle muscles in gait. Finally, we propose that rehabilitation therapies in individuals with chronic iSCI should be directed at strengthening the agonist in order to improve joint torque and the associated functional ability in these subjects.Declaration of InterestThe authors report no conflict of interest.AcknowledgementWe would like to thank Niu.X and Varoqui.D for their assistance with running the experiments and operating the RALT. The National Institute of Health [5R01HD059895] supported this study.REFERENCES ADDIN EN.REFLIST 1.Waters RL, Adkins RH, Yakura JS, Sie I. Motor and sensory recovery following incomplete paraplegia. Arch Phys Med Rehabil 1994; 75: 67-72.2.Lim HK, Lee DC, McKay WB, Priebe MM, Holmes SA, Sherwood AM. Neurophysiological assessment of lower-limb voluntary control in incomplete spinal cord injury. 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Muscles Alive: Their Functions Revealed by Electromyography. 5th Edition ed. Baltimore, MD: Williams and Wilkins, 1985.36.Swinnen E, Duerinck S, Baeyens JP, Meeusen R, Kerckhofs E. Effectiveness of robot-assisted gait training in persons with spinal cord injury: a systematic review. J Rehabil Med 2010; 42: 520-526.37.Musselman. K. Clinical significance testing in rehabilitation research: what, why, and how? Physical Therapy Reviews 2007; 12: 287-296.38.Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 1987; 412: 84-95.39.Hornby TG, Zemon DH, Campbell D. Robotic-assisted, body-weight-supported treadmill training in individuals following motor incomplete spinal cord injury. Phys Ther 2005; 85: 52-66.Figure 1Robotic assisted locomotor training (RALT) device.Figure 2Experimental apparatus used to evaluate ankle isometric maximal voluntary contractions.Figure 3Baseline and 4-weeks average in the isometric MVC torque and the co-activation of the ankle measures for the RALT and the control group is shown. Bars represent the standard deviation of the group mean. Asterisks * indicate significance at P < 0.05 between pre- and post-tests. Figure 4Baseline and 4-weeks average in the clinical measures for the RALT and the control group. Bars represent the standard deviation of the group mean. Asterisks * indicate significance at P < 0.05 between pre- and post-tests. TUG= Timed Up and Go test; 10MWT=10-meter walk test; 6MWT = Six minute walk test. Table 1 – Baseline demographic characteristics and clinical scores of the RALT and control groups.Baseline DemographyRALT Group (n=16)Control Group (n=16)Mean ± SDRangeMean ± SDRangeSigAge (y)50.81 ± 7.9337 – 7050.02 ± 9.5728-68p=0.73Lesion duration (y)11.38 ± 9.652 – 3610.35 ± 9.791 – 36p=0.42WISCI II (range, 0-20)15.31 ± 4.179 – 2014.50 ± 4.319 – 20p=0.70TUG (s)33.4 ± 34.759.7 – 126.146.5 ± 31.198.7 – 115.0p=0.1410MWT (s)44.6 ± 57.660.05 – 1.0647.27 ± 47.610.06 – 1.49p=0.596MWT (m)204.7 ± 102.7625.5 – 346.0177.6 ± 143.6120.7 – 501.2p=0.34Sex? (F-M)8 (50%) – 8 (50%)4 (25%) – 12 (75%)Level of Lesion? (C-T)9C (56%), 7T (44%)9C (56%), 7T (44%)p=0.72Ankle flexors MAS? (range, 0-4)2 (IQR = 1)2 (IQR = 1)p=0.10Continuous data are expressed as mean ± standard deviation [range], categorical variables (?) are expressed as a number (%) and nominal variables (?) are expressed as the median (InterQuartile Range). Abbreviations: F = female; M = male; C = cervical; T = thoracic; MAS = Modified Ashworth Scale; WISCI II = Walking Index for Spinal Cord Injury II; TUG = Timed Up and Go; 10MWT = 10-meter walk; 6MWT = 6-minute walk.Table 2 - Correlations (r values) show a linear relationship between clinical walking performance measures and torques at baseline for both groups combined. TDFTPFTUG-0.51*-0.42*10MWT-0.62*-0.53*6MWT0.57*0.46*Abbreviations: TUG = Timed Up and Go; 10MWT = 10-meter walk test; 6MWT = 6-minute walk test. TDF and TPF = isometric torque in dorsi- and plantar-flexion directions. *represents significant correlations (p < 0.05). ................
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