Acquisition of a simple motor skill: task-dependent adaptation and long-term changes in the human soleus stretch reflex

Abstract

Changing the H reflex through operant conditioning leads to CNS multisite plasticity and can affect previously learned skills. To further understand the mechanisms of this plasticity, we operantly conditioned the initial component (M1) of the soleus stretch reflex. Unlike the H reflex, the stretch reflex is affected by fusimotor control, comprises several bursts of activity resulting from temporally dispersed afferent inputs, and may activate spinal motoneurons via several different spinal and supraspinal pathways. Neurologically normal participants completed 6 baseline sessions and 24 operant conditioning sessions in which they were encouraged to increase (M1up) or decrease (M1down) M1 size. Five of eight M1up participants significantly increased M1; the final M1 size of those five participants was 143 ± 15% (mean ± SE) of the baseline value. All eight M1down participants significantly decreased M1; their final M1 size was 62 ± 6% of baseline. Similar to the previous H-reflex conditioning studies, conditioned reflex change consisted of within-session task-dependent adaptation and across-session long-term change. Task-dependent adaptation was evident in conditioning session 1 with M1up and by session 4 with M1down. Long-term change was evident by session 10 with M1up and by session 16 with M1down. Task-dependent adaptation was greater with M1up than with the previous H-reflex upconditioning. This may reflect adaptive changes in muscle spindle sensitivity, which affects the stretch reflex but not the H reflex. Because the stretch reflex is related to motor function more directly than the H reflex, M1 conditioning may provide a valuable tool for exploring the functional impact of reflex conditioning and its potential therapeutic applications. NEW & NOTEWORTHY Since the activity of stretch reflex pathways contributes to locomotion, changing it through training may improve locomotor rehabilitation in people with CNS disorders. Here we show for the first time that people can change the size of the soleus spinal stretch reflex through operant conditioning. Conditioned stretch reflex change is the sum of task-dependent adaptation and long-term change, consistent with H-reflex conditioning yet different from it in the composition and amount of the two components.

Keywords: humans; operant conditioning; plasticity; stretch reflex.

Conflict of interest statement

No conflicts of interest, financial or otherwise, are declared by the authors.

Figures

Fig. 1.

A: study session schedule: 6 baseline sessions are followed by 24 conditioning sessions, all at a pace of 3 sessions/wk. B: the stretch reflex pedal. Participants are seated comfortably with both feet on separate foot plates. C: the change in ankle angle (top) and the activity of the soleus muscle (SOL) (bottom) following a single imposed dorsiflexion perturbation. Peaks M1 and M2 are shown. Gray shaded area visualizes the time window for the M1 for which the participants received feedback during the conditioning sessions. D: visual feedback. The feedback on the screen comprises 2 parts, the background EMG and the stretch reflex size, both shown as bars. Shaded area in left panel represents the preset range for the SOL background activity, which must be maintained for at least 2 s by the participant for a stretch reflex trial to occur. Shaded area in right panel represents the targeted range for the size of the M1 component. During control trials, this shaded area is set as large as possible since the participant is not training to modify the M1 size. During M1up conditioning trials, this shaded area appears in the upper half (i.e., at criterion level and above), based on the baseline sessions. In contrast, during M1down conditioning trials, this area appears in the lower half (i.e., at criterion level and below). Immediately after a stretch reflex trial occurs (i.e., 200 ms after perturbation onset), a vertical bar reflecting M1 size is displayed. When the bar height falls within the shaded area, the participant had a successful conditioning trial and the bar is green. If the bar height falls out of the shaded area, the bar becomes red and the trial is registered as an unsuccessful trial. This provides immediate feedback on M1 size to the participant for each single trial performed. Abs., absolute; M1down, conditioning to decrease M1 size; M1up, conditioning to increase M1 size.

Fig. 2.

Soleus and tibialis anterior (TA) background EMG and the soleus maximum M-wave amplitude (Mmax) and maximum H-reflex amplitude (Hmax) values for all baseline and conditioning sessions in M1up (A) and M1down (B) participants in whom conditioning was successful. Each set of a symbol and error bars represents the average (±SE) value for successfully conditioned participants. n = 5 for M1up (A), and n = 8 for M1down (B). M1down, conditioning to decrease M1 size; M1up, conditioning to increase M1 size; ○, Soleus background EMG amplitude; □, TA background EMG; ◇, Mmax; ×, Hmax.

Fig. 3.

A: the final conditioned M1 size for individual participants. Filled symbols represent successful participants in whom the average conditioned M1 for conditioning sessions 19–24 was significantly increased (5 of 8 M1up participants, ▲) or decreased (8 of 8 M1down participants, ▼) compared with the average baseline M1. B: the final conditioned M2 size for individual participants. As for A, filled symbols represented the successful participants in whom the average conditioned M1 for conditioning sessions 19–24 was significantly increased (5 of 8 M1up participants, ▲) or decreased (8 of 8 M1down participants, ▼) compared with the average baseline M1. Open symbols show the 3 unsuccessful participants (i.e., 3 of 8 M1up participants). M1down, conditioning to decrease M1 size; M1up, conditioning to increase M1 size.

Fig. 4.

Average conditioned and control stretch reflexes for a representative participant of each of the M1up (A) and M1down (B) groups. Top: the change in ankle angle. Bottom: the average rectified soleus (SOL) EMG data of the three 75-trial blocks for 1 baseline session and the last conditioning session in single participants. Dashed black traces represent data from a single baseline session, and red (M1up) and blue (M1down) traces represent data from the last conditioning session. The gray shaded area indicates the M1 response window. M1down, conditioning to decrease M1 size; M1up, conditioning to increase M1 size.

Fig. 5.

Average (±SE) M1 sizes and H-reflex sizes (from Thompson et al. 2009) for all successful M1up/HRup (red) and M1down/HRdown (blue) participants for all baseline and conditioning sessions. A, top: average conditioned M1 size. Middle: average control M1 size. Bottom: within-sessions change (average conditioned minus control M1 size). B, top: average conditioned H-reflex size. Middle: average control H-reflex size. Bottom: within-sessions change (average conditioned minus control H-reflex size). Vertical dashed line separates the baseline sessions from the conditioning sessions. M1down, conditioning to decrease M1 size; M1up, conditioning to increase M1 size. *Significant difference (P < 0.05) between the two conditioning protocols in the amount of within-session reflex change.

Fig. 6.

Control M1 change with M1down conditioning: control soleus (SOL) EMG during 1 baseline session and the final conditioning session for n = 1. Each trace is the average of 20 trials. The gray shaded area indicates the M1 response window. M1down, conditioning to decrease M1 size.

Fig. 7.

Within-session task dependent adaptation with M1up conditioning: control soleus (SOL) EMG during the control trials (the first 20 trials where no visual feedback is provided) and the conditioning trials (the 3 blocks of 75 trials where feedback is provided in relation to the size of the M1 response) for n = 1. The gray shaded area indicates the M1 response window. M1up, conditioning to increase M1 size.