Representation of goal and movements without overt motor behavior in the human motor cortex: a transcranial magnetic stimulation study

Abstract

We recorded motor-evoked potentials (MEPs) to transcranial magnetic stimulation from the right opponens pollicis (OP) muscle while participants observed an experimenter operating two types of pliers: pliers opened by the extension of the fingers and closed by their flexion ("normal pliers") and pliers opened by the flexion of the fingers and closed by their extension ("reverse pliers"). In one experimental condition, the experimenter merely opened and closed the pliers; in the other, he grasped an object with them. In a further condition, the participants imagined themselves operating the normal and reverse pliers. During the observation of actions devoid of a goal, the MEP amplitudes, regardless of pliers used, reflected the muscular pattern involved in the execution of the observed action. In contrast, during the observation of goal-directed actions, the MEPs from OP were modulated by the action goal, increasing during goal achievement despite the opposite hand movements necessary to obtain it. During motor imagery, the MEPs recorded from OP reflected the muscular pattern required to perform the imagined action. We propose that covert activity in the human motor cortex may reflect different aspects of motor behavior. Imagining oneself performing tool actions or observing tool actions devoid of a goal activates the representation of the hand movements that correspond to the observed ones. In contrast, the observation of tool actions with a goal incorporates the distal part of the tool in the observer's body schema, resulting in a higher-order representation of the meaning of the motor act.

Figure 1.

Diagram of experimental conditions in experiments 1, 2, and 3. Two tools (normal and reverse pliers) were used in two action types (no-goal and goal). Normal pliers (left) are opened by extension of the thumb and index fingers and closed by their flexion. Reverse pliers (right) are opened by flexion of the thumb and index fingers and closed by their extension. In the no-goal condition (top), tools were first opened and then closed repetitively without any object to grasp. In the goal condition (bottom), the same movements were performed to grasp small objects. Magnetic stimuli were delivered for each condition just before the moment of maximal aperture and maximal closure of the tool's arms, as signaled by built-in potentiometers. The tasks were to observe the actions in experiment 1 and in experiment 3 and to imagine doing the actions in experiment 2.

Figure 2.

Modulation of MEPs during action observation. Mean MEP amplitudes recorded from the right opponens pollicis during the observation of the experimenter operating the normal and reverse tools, in both the goal and no-goal conditions. “Extend” and “flex” refer to the movements of the experimenter's thumb. Values from individual participants are represented as line–symbol, whereas mean values of the group are represented as gray columns. p values from the relevant post hoc comparisons are given.

Figure 3.

Modulation of MEPs during motor imagery. Mean MEP amplitudes recorded from the right opponens pollicis during the imagination of motor behaviors using the normal and reverse tools in both the goal and no-goal conditions. “Extend” and “flex” refer to the imagined movements of the participants' thumb. Values from individual participants are represented as line–symbol, whereas mean values of the group are represented as gray columns. p values from the relevant post hoc comparisons are given.

Figure 4.

Modulation of MEPs during action observation after motor training. Mean MEP amplitudes recorded from the right opponens pollicis during observation of the extension and flexion phases of the experimenter's fingers, with the reverse pliers, in both the goal and no-goal conditions. Values from individual participants are represented as line–symbol, whereas mean values of the group are represented as gray columns. p values from the relevant post hoc comparisons are given.