Adjustments of prehension synergies in response to self-triggered and experimenter-triggered load and torque perturbations

Abstract

Humans are known to show anticipatory adjustments in the grip force prior to a self-generated or predictable action or perturbation applied to a hand-held object. We investigated whether humans can also adjust covariation of individual finger forces (multi-finger synergies) prior to self-triggered perturbations. To address this issue, we studied adjustments in multi-digit synergies associated with applied load/torque perturbations while the subjects held a customized handle steadily. The main hypothesis was that the subjects would be able to demonstrate the phenomenon of anticipatory covariation, that is changes in covariation patterns among digit forces and moments of force in anticipation of a perturbation, but only when the perturbation was triggered by the subjects themselves. Based on the principle of superposition (decoupled grasping force and resultant torque control), we also expected to see different adjustments in indices of multi-digit synergies stabilizing the total gripping force and the total moment of force. The task for the subjects (n = 8) was to return the initial handle position as quickly as possible after a perturbation, which consisted of removing one of three loads hanging from the handle. There were six experimental conditions: two types of perturbations (self-triggered and experimenter-triggered) by three positions of the load (left, center, and right). Three-dimensional forces and moments of force recorded from each digit contact were used for the analysis. Indices of covariation among digit forces and among moments of force, previously employed for studying motor synergies, were computed across trials. Positive values of the indices reflected negative covariations of individual digit forces and moments of force (their inter-compensatory changes) to stabilize the total force and moment acting on the handle. In steady-state conditions, subjects showed strong positive indices for both digit forces and digit moments. Under the self-triggered conditions, changes in the indices of digit force and moment covariation were seen about 150 ms prior to the perturbation, while such changes were observed only after the perturbation under the experimenter-triggered conditions. Immediately following a perturbation, the indices of force and moment covariation rapidly changed to negative revealing the lack of inter-compensation among the individual digit forces and moments. Later, both indices showed a recovery to positive values; the recovery was faster in the self-triggered conditions than in the experimenter-triggered ones. During the steady-state phase after the perturbation, the indices of force and moment covariation decreased and increased, respectively, as compared to their values during the steady-state phase prior to the perturbation. We conclude that humans are able to adjust multi-digit synergies involved in prehensile tasks in anticipation of a self-triggered perturbation. These conclusions speak against hypotheses on the organization of multi-element actions based on optimal control principles. Different changes in the indices of force and moment covariation after a perturbation corroborate the principle of superposition. We discuss relations of anticipatory covariation to anticipatory postural adjustments.

Fig. 1

a The customized handle; the force-moment sensors shown as white cylinders were attached to two vertical aluminum bars. Three loads of 0.30 kg each are shown as black cylinders. The loads were attached to the long horizontal aluminum beam; one of them was attached with a cotton thread and the other two with bolt–nut structures. A force sensor was attached to the bottom of the load on the thread. The transmitter of a magnetic position-angle sensor shown as a small black cube was attached to the plastic base affixed to the top of the handle. M_X, M_Y, and M_Z are moments produced by the digits about X-, Y-, and Z-axes. b The subject held the handle while monitoring its angular position about X- and Z-axes, θ_X and θ_Z, respectively. The right wrist and forearm were housed in a wrist–forearm brace and secured with Velcro straps. The left hand could either rest on the knee or positioned just under a load for trials with self-triggered perturbations

Fig. 2

Individual digit a normal and c tangential forces during experimenter-triggered unloading and b normal and d tangential forces during self-triggered unloading. T, I, M, R, and L stand for thumb, index, middle, ring, and little fingers, respectively. The perturbation started at time t = 0 s (t₀). The data are from single trials performed by a representative subject performing a load lifting at the left location. The magnitudes of normal and tangential forces are shown in the figure. Note that thumb normal force direction is opposite to the finger normal forces while all tangential force directions are the same

Fig. 3

Linear positions of the magnetic sensor along Y-axis during a experimenter-triggered unloading and b self-triggered unloading. Angular positions of the sensor about X-axis during c experimenter-triggered unloading and d self-triggered unloading. The perturbation started at time t = 0 s (t₀). The data are from single trials performed by a representative subject. Different lines show data during lifting the loads at different locations, left (thin solid line), center (dashed line), and right (thick solid line)

Fig. 4

Peak linear and angular displacements of the handle under the experimenter-triggered (gray bars) and self-triggered (white bars) conditions. The data were averaged over all 12 trials for each subject and further averaged across all subjects. Mean values are shown with standard error bars

Fig. 5

Indices of finger force covariation, ΔV_F(t) for a experimenter-triggered and b self-triggered conditions and indices of finger moment covariation, ΔV_M(t) for c experimenter-triggered and d self-triggered conditions. The load was removed at time t₀ = 0 s (t₀). The data for a representative subject is shown. Different lines show data during lifting the loads at different locations, left (thin solid line), center (dashed line), and right (thick solid line). Note the early shifts in ΔV indices for self-triggered conditions

Fig. 6

The times of initiation of a decrease in ΔV_F(t) and ΔV_M(t) with respect to the time of unloading, t₀; negative and positive values represent the times of initiation before and after t₀, respectively. Data averaged across subjects is shown with standard error bars

Fig. 7

Changes in ΔV_F(t) and ΔV_M(t) indices between the steady-state value 1,000 ms prior to t₀ and the minimum value over the 2,000 ms after t₀. The data is shown as averages over subjects with standard error bars

Fig. 8

Averaged values of a ΔV_F(t) and b ΔV_M(t) over the 100 ms, 1,000 ms before and 2,500 ms after the time of perturbation. The data was averaged over subjects and presented as means ± SE

Fig. 9

Critical times (t_CR) of ΔV_F(t) and ΔV_M(t). The perturbation was given at time 0 s. The data was averaged over subjects and presented as means ± SE