Neural processes mediating the preparation and release of focal motor output are suppressed or absent during imagined movement

Abstract

Movements that are executed or imagined activate a similar subset of cortical regions, but the extent to which this activity represents functionally equivalent neural processes is unclear. During preparation for an executed movement, presentation of a startling acoustic stimulus (SAS) evokes a premature release of the planned movement with the spatial and temporal features of the tasks essentially intact. If imagined movement incorporates the same preparatory processes as executed movement, then a SAS should release the planned movement during preparation. This hypothesis was tested using an instructed-delay cueing paradigm during which subjects were required to rapidly release a handheld weight while maintaining the posture of the arm or to perform first-person imagery of the same task while holding the weight. In a subset of trials, a SAS was presented at 1500, 500, or 200 ms prior to the release cue. Task-appropriate preparation during executed and imagined movements was confirmed by electroencephalographic recording of a contingent negative variation waveform. During preparation for executed movement, a SAS often resulted in premature release of the weight with the probability of release progressively increasing from 24 % at -1500 ms to 80 % at -200 ms. In contrast, the SAS rarely (<2 % of trials) triggered a release of the weight during imagined movement. However, the SAS frequently evoked the planned postural response (suppression of bicep brachii muscle activity) irrespective of the task or timing of stimulation (even during periods of postural hold without preparation). These findings provide evidence that neural processes mediating the preparation and release of the focal motor task (release of the weight) are markedly attenuated or absent during imagined movement and that postural and focal components of the task are prepared independently.

Fig. 1

a Summary of the timing of the stimuli for the instructed-delay paradigm. A warning tone (100 ms, 1000 Hz, 80 dB) was presented 3000 ms before an imperative release tone (100 ms, 1000 Hz, 80 dB). In a subset of trials, a SAS (40 ms, 1000 Hz, 123 dB) was presented at either 1500, 500, or 200 ms prior to the release cue. b Grand average-rectified EMG responses in the finger extensors

Fig. 2

Examples of EMG activity in the elbow flexors (biceps brachii, BB), finger extensors (extensor digitorum communis, EDC), and sternocleidomastoid (SCM) muscles during the different trial conditions. The left panel shows responses during imagined movements (IM), and the right panel shows executed movements (EM). During EM control trials (no SAS) (bottom right plot), movement release was preceded by a suppression of EMG activity in BB (shaded gray box) and activation of EDC. Mental imagery of the same task (bottom left plot) was associated with tonic BB activity to maintain the elbow posture, but there was no suppression of BB or activation of EDC. The presentation of a SAS at −1500, −500, or −200 ms during the preparation phase for EMs evoked a rapid release of the weight that was accompanied by a burst of activity in the SCM muscle, suppression of BB activity, followed by the activation of the EDC muscle. During IMs, the activation of EDC is absent, but the SAS consistently produced a suppression of BB activity. Similarly, the presentation of a SAS alone (i.e., no warning or release tone) also produced BB EMG suppression and a SCM burst, but no EDC activity

Fig. 3

Average incidence of SAS-triggered release of the weight across subjects for both the executed and imagined movement tasks. Note the progressive increase in incidence for the executed task and the lack of movement release for the imagined task. Error bars are one standard error

Fig. 4

Average incidence of suppression of biceps brachii (BB) EMG across subjects for both the executed and imagined movement tasks. Note that BB suppression was observed for all SAS timings, including the SAS control condition (SAS at −3000 ms). CON = control trials without a SAS. Error bars are one standard error

Fig. 5

a Grand average CNV waveforms at each scalp surface electrode for the executed (black lines) and imagined (red lines) movement tasks. The zero point on the time axis is the onset of the release tone. b Expansion of the waveform at electrode Cz. The gray bars indicate the 100 ms windows used to calculate areas under the CNV waveform centered on the −3800, −1500, −500, and −200 time points. Asterisk (*) indicates a significant difference between tasks (p < 0.05) at the marked time point