Enhanced activation of motor execution networks using action observation combined with imagination of lower limb movements

Michael Villiger, Natalia Estévez, Marie-Claude Hepp-Reymond, Daniel Kiper, Spyros S Kollias, Kynan Eng, Sabina Hotz-Boendermaker, Michael Villiger, Natalia Estévez, Marie-Claude Hepp-Reymond, Daniel Kiper, Spyros S Kollias, Kynan Eng, Sabina Hotz-Boendermaker

Abstract

The combination of first-person observation and motor imagery, i.e. first-person observation of limbs with online motor imagination, is commonly used in interactive 3D computer gaming and in some movie scenes. These scenarios are designed to induce a cognitive process in which a subject imagines himself/herself acting as the agent in the displayed movement situation. Despite the ubiquity of this type of interaction and its therapeutic potential, its relationship to passive observation and imitation during observation has not been directly studied using an interactive paradigm. In the present study we show activation resulting from observation, coupled with online imagination and with online imitation of a goal-directed lower limb movement using functional MRI (fMRI) in a mixed block/event-related design. Healthy volunteers viewed a video (first-person perspective) of a foot kicking a ball. They were instructed to observe-only the action (O), observe and simultaneously imagine performing the action (O-MI), or imitate the action (O-IMIT). We found that when O-MI was compared to O, activation was enhanced in the ventralpremotor cortex bilaterally, left inferior parietal lobule and left insula. The O-MI and O-IMIT conditions shared many activation foci in motor relevant areas as confirmed by conjunction analysis. These results show that (i) combining observation with motor imagery (O-MI) enhances activation compared to observation-only (O) in the relevant foot motor network and in regions responsible for attention, for control of goal-directed movements and for the awareness of causing an action, and (ii) it is possible to extensively activate the motor execution network using O-MI, even in the absence of overt movement. Our results may have implications for the development of novel virtual reality interactions for neurorehabilitation interventions and other applications involving training of motor tasks.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. fMRI design.
Figure 1. fMRI design.
The session consisted of 2 runs containing a total of 7 blocks of each of the 4 conditions. Each block contained 6 trials of the same condition. Each block was preceded by the presentation (1.5 sec) of an instruction. Within a run the blocks were presented in pseudo-random order. Each trial consisted of a 5 s video clip followed by an inter-stimulus interval (ISI) with a duration jittered between 3.5 and 6.5 s. In the first run only the O and SCR conditions were included. The second run included blocks of O-MI, O-IMIT and SCR. The protocol was conceived to yield the same number of trials in each condition (42).
Figure 2. Activation patterns during right foot…
Figure 2. Activation patterns during right foot movements in healthy subjects from the contrast O-MI>O.
The results are superimposed on the MNI template and the regions are listed in Table 3. Numbers in the color bar correspond to t-values. Abbreviations: PMv: ventral premotor cortex; IPL: inferior parietal lobe; INS: insula.
Figure 3. Conjunction (shared activations) and percent…
Figure 3. Conjunction (shared activations) and percent signal changes.
Conjunction (shared activations) of O-MI and O-IMIT are displayed in the left two columns. The results are superimposed on the MNI template and regions are listed in Table 4. Numbers in the color bar on the left side correspond to t-values. In the right column, percent signal changes of the BOLD responses (± SEM across subjects) for the group local maximum in left PMv, right IPL, and right OTC are shown in each condition (O, O-MI and O-IMIT). Abbreviations: same as Figure 2; OTC: occipitotemporal cortex.
Figure 4. Head motion – Translation/Rotation.
Figure 4. Head motion – Translation/Rotation.
Left: Translation in x-, y- and z-direction of 14 subjects among 205 (1st run - above) and 369 scans (2nd run - below). Right: Rotations (roll, pitch, yaw) of 14 subjects among 205 (1st run - above) and 369 scans (2nd run - below). Regarding pitch rotation, the rotation is around the right-left-axis, moving the head up and down like shaking the head “yes”. Roll rotation is around the inferior-superior-axis, like shaking the head “no”. Yaw is rotation around the anterior-posterior-axis, like shaking the head “maybe”.

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