Learning effects on muscle modes and multi-mode postural synergies

Abstract

We used the framework of the uncontrolled manifold hypothesis to explore the effects of practice on the composition of muscle groups (M-modes) and multi-M-mode synergies stabilizing the location of the center of pressure (COP). In particular, we tested a hypothesis that practice could lead to a transition from co-contraction muscle activation patterns to reciprocal patterns. We also tested a hypothesis that new sets of M-modes would form stronger synergies stabilizing COP location. Subjects practiced load release tasks for five days while standing on a board with a narrow support surface (unstable board). Their M-modes and indices of multi-M-mode synergies were computed during standing without instability and during standing on an unstable board before practice, in the middle of practice, and at the end of practice. During standing without instability, subjects showed two consistent M-modes uniting dorsal and ventral muscles of the body respectively (reciprocal modes). While standing on an unstable board, prior to practice, subjects commonly showed M-modes uniting muscle pairs with opposing actions at major leg joints-co-contraction modes. Such sets of M-modes failed to stabilize the COP location in the anterior-posterior direction. Practice led to better task performance reflected in fewer incidences of lost balance. This was accompanied by a drop in the occurrence of co-contraction M-modes and the emergence of multi-mode synergies stabilizing the COP location. We conclude that the central nervous system uses flexible sets of elemental variables (modes) to ensure stable trajectories of important performance variables (such as COP location). Practice can lead to adjustments in both the composition of M-modes and M-mode co-variation patterns resulting in stronger synergies stabilizing COP location.

Figure 1

The experimental setup: The subjects stood on the force platform (the “stable condition”) or on a specially constructed wooden board (the “unstable condition”). The board was fitted with a narrow beam on the undersurface. This board was placed over the force platform such that its narrow dimension was in the anterior-posterior (AP) direction. For the load release task, the subject held a load suspended behind the body through the pulley system and then released the load quickly. Location of some of the EMG electrodes is also shown (TA tibialis anterior, GL lateral head of gastrocnemius, GM medial head of gastrocnemius, SOL soleus, RF rectus femoris, VL vastus lateralis, BF biceps femoris, ST semitendinosus, RA rectus abdominis, and ES erector spinae); acc - accelerometer.

Figure 2

Changes in performance errors with practice: The percentage of the number of error trials for the consecutive five practice days for the two tasks (A: load release task, B: arm movement task). The filled circles and open circles show the data for Board-A and Board-B, respectively. When the percentage of errors dropped under 10% (the horizontal dashed lines), Board-A was replaced wih Board-B on the next day.

Figure 3

Displacement of the center of pressure in the anterior-posterior direction (COP_AP) and normalized EMG patterns for a representative subject who performed the load release task with the load of 4 kg (A) and the arm movement task (B) in the three test sessions: Pre-practice (PRE: thin line), mid-practice (MID: thick dashed line) and post-practice (POST: thick line) while standing on Board-1. The time of the action initiation is shown as time zero (t₀) with vertical lines. Averages across nine trials (load release) and 50 trials (arm movement) are shown. COP_AP displacement in the anterior direction is shown as positive (Fig.3a, b). The scales have been selected for better visualization.

Figure 3

Displacement of the center of pressure in the anterior-posterior direction (COP_AP) and normalized EMG patterns for a representative subject who performed the load release task with the load of 4 kg (A) and the arm movement task (B) in the three test sessions: Pre-practice (PRE: thin line), mid-practice (MID: thick dashed line) and post-practice (POST: thick line) while standing on Board-1. The time of the action initiation is shown as time zero (t₀) with vertical lines. Averages across nine trials (load release) and 50 trials (arm movement) are shown. COP_AP displacement in the anterior direction is shown as positive (Fig.3a, b). The scales have been selected for better visualization.

Figure 4

The diagram of classification of muscle modes (M-modes) based on results of the PCA. There were two types of “reciprocal modes”, three types of “co-contraction modes”, and five types of “mixed modes”. The muscles indicated in italics did not show up consistently in the PC indicated. TA tibialis anterior, GL lateral head of gastrocnemius, GM medial head of gastrocnemius, SOL soleus, RF rectus femoris, VL vastus lateralis, BF biceps femoris, ST semitendinosus, RA rectus abdominis, and ES erector spinae.

Figure 5

The total range (min - max), the 25-75% range, and the median for the number of times the reciprocal M-modes and the total of the co-contraction and mixed M-modes were seen across subjects. STABLE - stable condition, PRE - pre-practice under unstable condition, MID - mid-practice under unstable condition, POST - post-practice under unstable condition. Note that the co-contraction and mixed M-modes occurred more frequently at the PRE test as compared to the STABLE test. Then, their number dropped with practice. * p < 0.05

Figure 6

Typical changes of the index of multi-mode synergy, ΔV during quick arm extension movements by a representative subject in the three test sessions, pre-practice (thin line), mid-practice (thick dashed line) and post-practice (thick line) while standing on Board-1 (unstable condition). The time of action initiation is shown as time zero (t₀, the vertical dashed line). The data are shown for 15 ms time intervals. Before practice, the subject showed consistently negative values of ΔV; these values turned positive during the other two sessions. No drop in ΔV after the action initiation can be seen in the post-practice session.

Figure 7

The two variance components (V_UCM: black bars and V_ORT: open bars) averaged across subjects for the arm movement task in the three test sessions (PRE, MID and POST) with standard error bars. The data were averaged over three 150 ms time intervals (T1: from -300 to -150 ms prior to t₀, T2: from -150 ms prior to t₀ to t₀ and T3: from t₀ to +150 ms after t₀). * p < 0.05

Figure 8

The ΔV indices averaged across subjects for the arm movement task in the three test sessions (PRE, MID and POST) with standard error bars. The ΔV indices were averaged over three 150 ms time intervals. The open, striped and black bars correspond to the time interval from -300 to -150 ms prior to t₀ (T1), from -150 ms prior to t₀ to t₀ (T2) and from t₀ to +150 ms after t₀ (T3), respectively. Note that ΔV after practice was significantly larger than that before practice. * p < 0.05.

Figure 9

An illustration of the two features of synergies using an example of producing a value of the total force with two fingers. Clouds of data points are shown in the finger mode space. The solid slanted line corresponds to perfect task performance. The three clouds correspond to different sharing patterns reflected in different average locations (black dot). The spherical distribution of data points (D₁) shows no co-variation between the modes that would stabilize the total force. The ellipse elongated along the solid slanted line (D₂) shows mode co-variation that is beneficial for F_TOT stabilization - a force stabilizing synergy. The ellipse elongated orthogonal to that line (D₃) corresponds to mode co-variation that destabilizes F_TOT.