Operant Conditioning of a Spinal Reflex Can Improve Locomotion after Spinal Cord Injury in Humans

Operant Conditioning of a Spinal Reflex Can Improve Locomotion after Spinal Cord Injury in Humans Aiko K. Thompson Ferne Pomerantz Jonathan R. Wolpaw

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Operant Conditioning of a Spinal Reflex Can Improve Locomotion after Spinal Cord Injury in Humans 2013 Journal of Neuroscience 10.1523/jneurosci.3968-12.2013 thompson2013-operant-conditioning-of-a-spinal-r thompson2013-operant-conditioning-of-a-spinal-r.txt, the project's staged copy b4b8df982d92d7713b3acbefd08a6d1a15f93def open-access rehabilitation-neuroscience

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0 spans located by searching the stored text for the quote's exact words, allowing any whitespace between them The soleus H-reflex, and whether operantly down-conditioning it improves locomotion in people with chronic incomplete spinal cord injury. Quotation withheld because this record is not cleared for redistribution. Can people with chronic incomplete spinal cord injury down-condition the soleus H-reflex operantly, and if so is the reflex decrease accompanied by improved locomotion? Quotation withheld because this record is not cleared for redistribution. method Quotation withheld because this record is not cleared for redistribution. operant down-conditioning of the soleus H-reflex Quotation withheld because this record is not cleared for redistribution. behavioural-experiment behavioural-experiment Quotation withheld because this record is not cleared for redistribution. mechanisms Acquiring the new smaller-reflex behaviour disturbs the post-injury spinal equilibrium and thereby triggers widespread adaptive plasticity that settles into a new equilibrium serving both the new reflex and locomotion Quotation withheld because this record is not cleared for redistribution. mechanisms In neurologically normal people, compensatory plasticity protecting already-satisfactory behaviours works against the long-term spinal change, which is why long-term change is smaller in them than in SCI subjects Quotation withheld because this record is not cleared for redistribution. mechanisms Injury to the corticospinal tract, the descending pathway that conditioning depends on, weakens the immediate cortical (task-dependent) component of the reflex change in SCI subjects status: the paper's own words: may reflect Quotation withheld because this record is not cleared for redistribution. mechanisms Better bilateral modulation of ankle muscle activity yields more effective weight bearing and push-off, which in turn raises walking speed Quotation withheld because this record is not cleared for redistribution. Conditioned H-reflex change decomposes into a within-session task-dependent adaptation, read as cortical influence, plus an across-session long-term change, read as spinal cord plasticity Quotation withheld because this record is not cleared for redistribution. The two components split differently after injury: less task-dependent adaptation, more long-term change, summing to the same total decrease as in normal subjects Quotation withheld because this record is not cleared for redistribution. Reduced task-dependent adaptation after injury is attributed to damage to the corticospinal tract, on which reflex conditioning depends Quotation withheld because this record is not cleared for redistribution. In an uninjured cord, compensatory plasticity protects behaviours that are already satisfactory and thereby limits the long-term reflex change; after injury there is nothing to protect, so the change proceeds further Quotation withheld because this record is not cleared for redistribution. Acquiring the new reflex disturbs the equilibrium the injured cord had settled into, triggering wider plasticity that changes locomotion as a whole rather than one pathway Quotation withheld because this record is not cleared for redistribution. After injury the long-term change is doubly rewarded - it satisfies the conditioning criterion and it improves walking - which is offered as why it goes further than in normal subjects Quotation withheld because this record is not cleared for redistribution. The success rate, though not significantly below that of normal subjects, was lower, and applicability to more severe impairment is unknown. what this limits: the transfer of the method to more impaired patients: THEIR SUCCESS RATE WAS NOT SIGNIFICANTLY DIFFERENT FROM THAT OF NORMAL SUBJECTS ... IT WAS LOWER Quotation withheld because this record is not cleared for redistribution. The small H-reflex increase seen in the unconditioned control group may be a nonspecific effect of repeated exposure to the measurement protocol. what this limits: the control-group baseline drift: THIS MAY HAVE BEEN A NONSPECIFIC EFFECT OF CONTINUED EXPOSURE OVER 30 SESSIONS TO THE BASELINE PROTOCOL Quotation withheld because this record is not cleared for redistribution. Thirteen subjects, of whom only six showed the effect, and the comparison group has four what this limits: every group-level statistic: 13 AMBULATORY SUBJECTS, of whom only six showed the effect, against a comparison group of four Quotation withheld because this record is not cleared for redistribution. All subjects were AIS grade C or D, so the protocol is untested in more severe injury and requires surviving supraspinal input what this limits: any extension to more severe injury: THE NEED FOR SUPRASPINAL INPUT WILL REMAIN, and all subjects here retained it Quotation withheld because this record is not cleared for redistribution. The subjects who improved are the same subjects in whom conditioning worked, so improvement and successful conditioning cannot be separated from subject-level differences what this limits: the walking-improvement result, which is not independent of the conditioning result: THE IMPROVEMENT ... DID NOT OCCUR IN PEOPLE IN WHOM THE H-REFLEX DID NOT DECREASE, WHETHER THEY WERE UC SUBJECTS OR UNSUCCESSFUL DC SUBJECTS Quotation withheld because this record is not cleared for redistribution. The breadth of the effect exceeds what the manipulated pathway can explain, and the wider plasticity invoked to cover the gap is inferred rather than measured what this limits: the proposed mechanism's sufficiency: IT IS UNLIKELY THAT THE PLASTICITY UNDERLYING A SMALLER SOLEUS H-REFLEX IN ONE LEG COULD ITSELF HAVE SUCH BROAD BENEFICIAL EFFECTS ON WALKING Quotation withheld because this record is not cleared for redistribution. The normal-subject comparison values are drawn from an earlier study rather than a concurrent control group what this limits: every comparison against normal values: THE DATA FOR NORMAL DC SUBJECTS ARE FROM THOMPSON ET AL. (2009), not from a concurrent control group Quotation withheld because this record is not cleared for redistribution. The subject comments are unsolicited and unblinded, and the subjects knew which protocol they were on what this limits: the subjects' own reports of benefit: OVER THE 3 MONTHS OF THE STUDY, THE SUBJECTS WERE NOT ASKED ABOUT THE CURRENT STATE OF THEIR MOTOR FUNCTION - unsolicited and unblinded Quotation withheld because this record is not cleared for redistribution. The comparison group's reflex drifted upward over the same period, which the authors attribute to nonspecific exposure rather than measure duplicate of: limitations[1] · what this limits: the same scope as limitations[1] - the control group's reflex drifted upward over the same period, attributed to nonspecific exposure to the baseline procedure rather than to conditioning Quotation withheld because this record is not cleared for redistribution. control trials in which the visual feedback shows only background EMG and nothing about H-reflex size - the weakest entry in this sample, carried by the word SIMPLY eliminates: prestimulus background EMG differing between control and conditioning trials, so a change in the reflex cannot be a posture or muscle-activation effect · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. H-reflex - conditioned: the average over the 225 feedback trials, the reflex the subject was actively trying to change Quotation withheld because this record is not cleared for redistribution. H-reflex - control: the average over 20 trials with no feedback and no instruction, which is what shows whether the change persists when the subject is not trying Quotation withheld because this record is not cleared for redistribution. H-reflex - locomotor: the average across 12 step-cycle bins during walking, a different behavioural context from the standing measurement Quotation withheld because this record is not cleared for redistribution. H-reflex - maximum (H max): the peak of the recruitment curve, a property of the pathway rather than of a trial Quotation withheld because this record is not cleared for redistribution. success - within a trial: the reflex fell below the current criterion value, shown to the subject as a green bar Quotation withheld because this record is not cleared for redistribution. success - across the study: the last six conditioning sessions differed significantly from baseline, which is the sense in which two-thirds of subjects succeeded Quotation withheld because this record is not cleared for redistribution. modulation - of EMG across the step cycle: how much a muscle varies its own activity, captured by the modulation index Quotation withheld because this record is not cleared for redistribution. modulation - of the reflex across the step cycle: how reflex size varies by phase, which should be lowest in swing and becomes so after conditioning Quotation withheld because this record is not cleared for redistribution. change - task-dependent adaptation: the within-session difference between control and conditioned reflex, produced immediately on being asked Quotation withheld because this record is not cleared for redistribution. claim_type: method a second reading reaching the same value. Recorded: method — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. method: behavioural-experiment a second reading reaching the same value. Recorded: behavioural-experiment — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. phenomenon: operant down-conditioning of the soleus H-reflex a second reading reaching the same value. Recorded: operant down-conditioning of the soleus H-reflex — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. builds-on → Thompson et al. (2009) human soleus H-reflex conditioning protocol in neurologically normal subjects Quotation withheld because this record is not cleared for redistribution. extends → Chen et al. (2006b) soleus H-reflex conditioning in spinal cord-injured rats Quotation withheld because this record is not cleared for redistribution. replicates → Chen et al. (2006b) and Segal and Wolf (1994) Quotation withheld because this record is not cleared for redistribution. extends → Thompson et al. 2009, the same conditioning protocol in neurologically normal subjects Quotation withheld because this record is not cleared for redistribution. extends → Chen et al. 2006b, H-reflex conditioning in spinal cord-injured rats Quotation withheld because this record is not cleared for redistribution. supports → Wolpaw 2010, the negotiated equilibrium hypothesis Quotation withheld because this record is not cleared for redistribution. supports → Segal and Wolf 1994, spinal stretch reflex conditioning in people with SCI Quotation withheld because this record is not cleared for redistribution. task-dependent adaptation —part-of→ H-reflex task-dependent adaptation H-reflex strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. long-term change —part-of→ H-reflex long-term change H-reflex strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. task-dependent adaptation —contrasted-with→ long-term change task-dependent adaptation long-term change strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. step-cycle symmetry —operationalised-as→ step cycle step-cycle symmetry step cycle strength of the relation: 1 Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span defines symmetry as a RATIO of intervals within the step cycle; operationalised-as is loose. Quotation withheld because this record is not cleared for redistribution. spasticity —causes→ swing phase spasticity swing phase strength of the relation: 0.9 Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span says spasticity PROLONGED the swing phase; the direction is not on the edge. Quotation withheld because this record is not cleared for redistribution. hyperreflexia —causes→ locomotion hyperreflexia locomotion strength of the relation: 0.9 Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span says locomotion was impaired by hyperreflexia; the edge carries no direction. Quotation withheld because this record is not cleared for redistribution. corticospinal tract —causes→ task-dependent adaptation corticospinal tract task-dependent adaptation strength of the relation: 0.6 — the record marks this weak Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span says the lesser adaptation MAY reflect damage to the CST; hedged. Quotation withheld because this record is not cleared for redistribution. soleus —contrasted-with→ tibialis anterior soleus tibialis anterior strength of the relation: 1 Audit 2026-09-28: DOUBTFUL - read against its span and kept, but soleus and its antagonist were both recorded; contrasted-with is loose. Quotation withheld because this record is not cleared for redistribution. t-test t-test Quotation withheld because this record is not cleared for redistribution. t-test t-test Quotation withheld because this record is not cleared for redistribution. ANOVA ANOVA Quotation withheld because this record is not cleared for redistribution. Mann-Whitney U test Mann-Whitney U test Quotation withheld because this record is not cleared for redistribution. p-value p-value Quotation withheld because this record is not cleared for redistribution. standard deviation standard deviation Quotation withheld because this record is not cleared for redistribution. standard error standard error Quotation withheld because this record is not cleared for redistribution. t-test t-test Quotation withheld because this record is not cleared for redistribution. t-test t-test Quotation withheld because this record is not cleared for redistribution. Mann-Whitney U test Mann-Whitney U test Quotation withheld because this record is not cleared for redistribution. repeated-measures ANOVA repeated-measures ANOVA Quotation withheld because this record is not cleared for redistribution. repeated-measures ANOVA repeated-measures ANOVA Quotation withheld because this record is not cleared for redistribution. standard error standard error Quotation withheld because this record is not cleared for redistribution. standard deviation standard deviation Quotation withheld because this record is not cleared for redistribution. p-value p-value Quotation withheld because this record is not cleared for redistribution. p-value p-value Quotation withheld because this record is not cleared for redistribution. Six of the nine people with spinal cord injury successfully down-conditioned the soleus H-reflex, a 67% success rate not significantly below the 89% seen in neurologically normal subjects. Quotation withheld because this record is not cleared for redistribution. The H-reflex decrease was specific to the conditioning protocol: no unconditioned subject's reflex fell, and the two groups' final reflex sizes differed significantly. Quotation withheld because this record is not cleared for redistribution. Ten-metre walking speed rose by an average of 59% in the six subjects whose H-reflex decreased. Quotation withheld because this record is not cleared for redistribution. Gait symmetry moved toward the ideal ratio of 1 in every subject whose H-reflex decreased. Quotation withheld because this record is not cleared for redistribution. In subjects whose H-reflex did not decrease, gait actually became less symmetrical over the same 30 sessions. Quotation withheld because this record is not cleared for redistribution. Successful down-conditioning of one leg's soleus reflex increased step-cycle EMG modulation in ankle and knee flexors and extensors of both legs, not just the conditioned leg. Quotation withheld because this record is not cleared for redistribution. Although the total reflex decrease matched that of normal subjects, its composition differed: SCI subjects showed less immediate task-dependent adaptation (-7% vs -15%) and more long-term across-session change (-24% vs -16%). Quotation withheld because this record is not cleared for redistribution. Unprompted positive reports of improved walking clustered almost entirely in the six successfully conditioned subjects (25 of 30 comments). Quotation withheld because this record is not cleared for redistribution. The reflex decrease persisted after training stopped, averaging 65% of baseline at one month and 58% at three months. Quotation withheld because this record is not cleared for redistribution. The reflex reduction carried over into walking itself: the H-reflex elicited during locomotion fell to 59% of its baseline size. Quotation withheld because this record is not cleared for redistribution. the conditioned H-reflex fell to the same 69% of baseline in SCI subjects as in normal subjects, but by a different mix of components Quotation withheld because this record is not cleared for redistribution. task-dependent adaptation was smaller and long-term change larger after injury Quotation withheld because this record is not cleared for redistribution. reflex decrease was specific to the down-conditioning protocol and absent in the unconditioned group Quotation withheld because this record is not cleared for redistribution. the unconditioned group's reflex rose slightly but significantly over the same period Quotation withheld because this record is not cleared for redistribution. walking speed rose 59% on average in the six subjects whose reflex decreased Quotation withheld because this record is not cleared for redistribution. gait symmetry improved in every subject whose reflex decreased and worsened in every subject whose did not Quotation withheld because this record is not cleared for redistribution. EMG modulation improved bilaterally, not only in the conditioned leg Quotation withheld because this record is not cleared for redistribution. the reflex decrease persisted at one and three months in every subject Quotation withheld because this record is not cleared for redistribution. unsolicited positive comments appeared only after the conditioned reflex had decreased substantially, from the 12th session on Quotation withheld because this record is not cleared for redistribution. two subjects reduced their reliance on a walking aid Quotation withheld because this record is not cleared for redistribution. the success rate in SCI subjects was 67%, not significantly below the 89% seen in normal subjects Quotation withheld because this record is not cleared for redistribution. stimulus and recording conditions were stable across all sessions, ruling out measurement drift as the source of the reflex change Quotation withheld because this record is not cleared for redistribution. H-reflex size H-reflex size Quotation withheld because this record is not cleared for redistribution. conditioned H-reflex size conditioned H-reflex size Quotation withheld because this record is not cleared for redistribution. modulation index (MI) modulation index (MI) Quotation withheld because this record is not cleared for redistribution. step-cycle symmetry step-cycle symmetry Quotation withheld because this record is not cleared for redistribution. task-dependent adaptation task-dependent adaptation Quotation withheld because this record is not cleared for redistribution. negotiated equilibrium negotiated equilibrium Quotation withheld because this record is not cleared for redistribution. control H-reflex size control H-reflex size Quotation withheld because this record is not cleared for redistribution. modulation index modulation index Quotation withheld because this record is not cleared for redistribution. negotiated equilibrium negotiated equilibrium Quotation withheld because this record is not cleared for redistribution. successful down-conditioning successful down-conditioning Quotation withheld because this record is not cleared for redistribution. soleus H-reflex size soleus H-reflex size Quotation withheld because this record is not cleared for redistribution. walking time walking time Quotation withheld because this record is not cleared for redistribution. step-cycle symmetry step-cycle symmetry Quotation withheld because this record is not cleared for redistribution. MI MI Quotation withheld because this record is not cleared for redistribution. conditioned H-reflex size conditioned H-reflex size Quotation withheld because this record is not cleared for redistribution. control H-reflex size control H-reflex size Quotation withheld because this record is not cleared for redistribution. 10 m walking speed 10 m walking speed Quotation withheld because this record is not cleared for redistribution. modulation index modulation index Quotation withheld because this record is not cleared for redistribution. soleus and TA background EMG level soleus and TA background EMG level Quotation withheld because this record is not cleared for redistribution. M-wave size M-wave size Quotation withheld because this record is not cleared for redistribution. 6/9 or 67% — proportion of SCI subjects in whom down-conditioning succeeded Quotation withheld because this record is not cleared for redistribution. 69 ± 11% and 69 ± 6% — final conditioned H-reflex as a percentage of baseline in SCI subjects and in normal subjects — identical values Quotation withheld because this record is not cleared for redistribution. +59 ± 19% — mean increase in 10 m walking speed among successfully conditioned subjects Quotation withheld because this record is not cleared for redistribution. 74 ±17% to 80 ± 11% — average locomotor EMG modulation index before and after successful down-conditioning Quotation withheld because this record is not cleared for redistribution. 20 control and 225 conditioned — number of H-reflexes elicited per conditioning session for the down-conditioning subjects Quotation withheld because this record is not cleared for redistribution. −7% vs −15% — task-dependent adaptation in SCI subjects compared with neurologically normal subjects Quotation withheld because this record is not cleared for redistribution. 25 of the 30 — positive spontaneous comments contributed by the six successfully conditioned subjects Quotation withheld because this record is not cleared for redistribution. n = 13 — total number of ambulatory subjects with spinal cord injury enrolled Quotation withheld because this record is not cleared for redistribution. 13 subjects — the whole sample, split 9 conditioned and 4 unconditioned Quotation withheld because this record is not cleared for redistribution. 2:1 — the randomisation ratio favouring the conditioned group Quotation withheld because this record is not cleared for redistribution. 30 sessions — the length of the conditioning phase, six more than the 24 needed in normal subjects Quotation withheld because this record is not cleared for redistribution. 225 conditioned H-reflexes — trials per session carrying feedback, against 20 without Quotation withheld because this record is not cleared for redistribution. 50–60% — the success rate the criterion was tuned to produce, keeping the task neither trivial nor hopeless Quotation withheld because this record is not cleared for redistribution. 69 ± 11% — final conditioned H-reflex as a share of baseline in SCI subjects, identical to normals Quotation withheld because this record is not cleared for redistribution. +59 ± 19% — walking speed gain in the subjects whose reflex decreased Quotation withheld because this record is not cleared for redistribution. 0–123% — the full spread of walking speed change across all subjects Quotation withheld because this record is not cleared for redistribution. 30 positive comments and no negative comments — the unsolicited subject reports, 25 of them from the six successful subjects Quotation withheld because this record is not cleared for redistribution. 0.59 to 0.80 m/s — one subject's walking speed before and after, given as the concrete case behind the group mean Quotation withheld because this record is not cleared for redistribution. 8 months to 50 years — time since injury across the sample, a very wide chronicity range for 13 people Quotation withheld because this record is not cleared for redistribution.

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