Acquisition of a simple motor skill: task-dependent adaptation plus long-term change in the human soleus H-reflex

Abstract

Activity-dependent plasticity occurs throughout the CNS. However, investigations of skill acquisition usually focus on cortex. To expand the focus, we analyzed in humans the development of operantly conditioned H-reflex change, a simple motor skill that develops gradually and involves plasticity in both the brain and the spinal cord. Each person completed 6 baseline and 24 conditioning sessions over 10 weeks. In each conditioning session, the soleus H-reflex was measured while the subject was or was not asked to increase (HRup subjects) or decrease (HRdown subjects) it. When the subject was asked to change H-reflex size, immediate visual feedback indicated whether a size criterion had been satisfied. Over the 24 conditioning sessions, H-reflex size gradually increased in six of eight HRup subjects and decreased in eight of nine HRdown subjects, resulting in final sizes of 140 +/- 12 and 69 +/- 6% of baseline size, respectively. The final H-reflex change was the sum of within-session (i.e., task-dependent) adaptation and across-session (i.e., long-term) change. Task-dependent adaptation appeared within four to six sessions and persisted thereafter, averaging +13% in HRup subjects and -15% in HRdown subjects. In contrast, long-term change began after 10 sessions and increased gradually thereafter, reaching +27% in HRup subjects and -16% in HRdown subjects. Thus, the acquisition of H-reflex conditioning consists of two phenomena, task-dependent adaptation and long-term change, that together constitute the new motor skill. In combination with previous data, this new finding further elucidates the interaction of plasticity in brain and spinal cord that underlies the acquisition and maintenance of motor skills.

Figures

Figure 1.

The study protocol. A, Left, Subject with electrodes on right leg faces monitor in standard study posture. Right top, Six baseline and 24 conditioning sessions occur at a rate of three per week and are followed by four follow-up sessions over the next 3 months. Right middle, At the beginning and end of each session, H–M recruitment curves (i.e., Hmax and Mmax) are obtained. In between, each baseline session has three 75 trial blocks of control H-reflexes, and each conditioning session has (as shown) a 20 trial block of control reflexes followed by three 75 trial blocks of conditioned H-reflexes. Right bottom, Soleus EMG recorded in a single representative trial. B, Visual feedback presented to the subject on the monitor. In all trials, the number of the current trial within its block and the running success rate for the current block are displayed, and the background EMG panel shows the correct range (shaded) and the current value (green vertical bar). If the EMG stays in the correct range for at least 2 s, an H-reflex is elicited. In control trials, the H-reflex panel is entirely shaded (indicating that every H-reflex is a success) and the green vertical bar is the H-reflex size for the most recent trial. In conditioned trials, the shading in the H-reflex panel indicates the rewarded H-reflex range for HRup (i.e., above a given value) or HRdown (i.e., below a given value) conditioning, the dark horizontal line is the average H-reflex size of the baseline sessions, and the vertical bar is the H-reflex size for the most recent trial. If that H-reflex size falls within the shaded area, the bar is green and the trial is a success. If it falls outside the shaded area, the bar is red and the trial is a failure. (For details, see Materials and Methods.)

Figure 2.

Final conditioned H-reflex sizes for individual subjects. The filled symbols represent the 14 successful subjects [i.e., subjects whose average conditioned H-reflexes for conditioning sessions 19–24 were significantly greater (for an HRup subject) or significantly less (for an HRdown subject) than the average H-reflexes of the six baseline sessions (p < 0.05, two-tailed t test)]. The open symbols represent the three subjects in whom conditioning was unsuccessful.

Figure 3.

Average (±SE) H-reflex measures for all successful HRup (upward triangle) and HRdown (downward triangle) subjects over the baseline, conditioning, and follow-up sessions. A, Average conditioned H-reflex size. B, Average control H-reflex size. C, Average of conditioned H-reflex size minus control H-reflex size. (For details, see Results.)

Figure 4.

Average conditioned (A) and control (B) H-reflexes from two representative subjects for a baseline session (solid) and the last conditioning session (dashed). Both conditioned and control H-reflexes are larger after 24 conditioning sessions in the HRup subject (left) and smaller in the HRdown subject (right). Background EMG and M-wave size do not change.

Figure 5.

Average control (solid) and conditioned (dashed) H-reflexes for a representative conditioning session of an HRup (left) and an HRdown subject (right). In each subject, task-dependent reflex change is evident: the conditioned H-reflex is larger than the control H-reflex in the HRup subject and smaller in the HRdown subject. Background EMG and M-wave size do not change.