Early and unintentional release of planned motor actions during motor cortical preparation

Abstract

Voluntary movements are often preceded by a movement-related potential beginning as much as two seconds prior to the onset of movement. In light of evidence that motor actions can be prepared and initiated in less than 200 ms, the function of this early activity has remained enigmatic. We hypothesized that the movement-related potential reflects the state of preparation of the planned movement. This was tested by delivering a startling acoustic stimulus during the preparation phase of a load-release task. The cue to release the load was presented either 3.5 seconds after a warning cue (PREDICT condition) or randomly between 4-12 seconds (REACT condition). Electroencephalographic, electromyographic and limb and load kinematic signals were recorded. In a subset of trials, a startle stimulus was delivered at -1500, -1000, -500, -250, -100 or 0 ms before the release cue. A contingent-negative variation (CNV) waveform, with a late phase of slow-rising negativity beginning an average of 1459 ms prior to movement, was observed for the PREDICT condition but not the REACT condition. For both conditions, the startle stimulus frequently evoked the early and unintentional release of the load-release sequence. The incidence of release was significantly (p<0.001) correlated with the late phase of the CNV for the PREDICT condition but not the REACT condition. For the REACT condition, the incidence of movement release was subject-specific, constant across the preparation interval, and uncorrelated with cortical activity. The onset of movement release by the startle stimulus was significantly shorter (p<0.001) for the PREDICT compared to the REACT condition. These findings provide evidence that the late phase of the CNV reflects cortical activity mediating the progressive preparation and storage of the forthcoming movement and that during this phase an intense sensory stimulus can evoke early and unintentional release of the planned action.

Figure 1. Summary of the stimulus timing conditions and muscle activation patterns.

A load release task was tested using two cueing conditions: PREDICT and REACT. A. Summary of the timing of the cues and presentation of the startle stimuli. For the PREDICT condition, subjects were presented with a warning tone 3500 ms prior to an imperative cue release tone. Subjects were trained to release the load within 1 simple reaction time in 50% of trials. For the REACT condition, there was no warning cue and the release tone was presented randomly between 4–12 s. For both conditions, a 40 ms, 124 dB startling acoustic stimulus (SAS) was presented in 22% of all trials at 7 time points over the preparation interval. B. Average rectified EMG data from a single subject showing responses in the biceps brachii (BB) and extensor digitorum communis (EDC) muscles during the PREDICT and REACT conditions. EMG responses were time-locked to the onset of activity in the EDC muscle (0 ms).

Figure 2. Movement-related potentials (MRPs) were affected by the predictability of the imperative release cue.

A. Grand average movement-related potentials derived from control trials at each of the nine EEG electrodes for both the PREDICT (black) and REACT (red) conditions. The cartoon to the right shows the locations of the electrodes on the scalp. B. Average integrated EEG calculated over 100 ms time bins at 8 time points centered on −4500, −2500, −1500, −1000, −500, −250, −100, 0 ms. Differences between conditions were significant (p<0.007) at all time points except at baseline (−4500 ms). C. Average slope of the movement-related potentials over three time intervals. The slopes were significantly different between conditions during movement preparation but not baseline (PRE) (p<0.007).

Figure 3. Movement-related oscillations were affected by the predictability of the imperative release cue.

The upper plots show the grand average time-frequency spectrograms at the C3 electrode overlying the contralateral sensorimotor region for the PREDICT (A) and REACT (B) conditions. Magnitudes have been normalized to the power over the pre-warning cue interval (−5 to −4.25 s). Note the marked suppression of oscillations in the alpha band (8–12 Hz) immediately following the warning cue and in the beta-band (15–30 Hz) during the 1500 ms time period immediately preceding the onset of wrist extensor (EDC) muscle activity (0 ms) for the PREDICT task. In contrast, the suppression of MRCOs occurred immediately prior to EMG onset for the REACT task and was confined to the beta-band. Plots C and D show the results of the statistical analysis of the normalized time-frequency spectrograms at the C3 electrode for the PREDICT (C) and REACT (D) conditions. Significant (p<0.05) increases (red) and decreases (blue) in MRCOs relative to baseline activity are shown.

Figure 4. Summary of the effects of a startling acoustic stimulus (SAS) on the release of movement.

A. Single trial examples of the elbow joint displacement and rectified EMG activity in biceps brachii (BB) and extensor digitorum communis (EDC) muscles when movement was initiated in response to the imperative tone (control trial, black line) or in response to a SAS presented 500 ms before the release tone (red line). Note that the kinematics and muscle activation patterns (the BB EMG suppression is highlighted with a grey bar) for the SAS-evoked movement were unchanged from control trials but the sequence was initiated less than 100 ms after the startle stimulus. B. The incidence of release of the movement sequence by a SAS was significantly affected by the temporal probability of imperative cue. For the PREDICT condition, the average incidence of release progressively increased from 0% of trials at −3500 ms (warning cue) to over 80% at −100 and 0 ms. In contrast, the incidence of release was relatively constant across all stimulus timings for the REACT condition. C. Examples of the incidence of movement release as a function of the timing of the SAS across three subjects (S1, S2, S3). For the PREDICT task, all subjects showed a similar profile of increasing incidence of release. In contrast, the behavior for the REACT task was different across subjects. S1 rarely released, S3 released on nearly every trial and S2 released in approximately 60% of trials, irrespective of timing of the SAS.

Figure 5. Summary of the effects of a startling acoustic stimulus (SAS) on the timing of movement release.

Reaction times relative to the onset of the SAS were sorted into 20 ms bins. The histograms show the percentage of trials within each reaction time bin for both the PREDICT (open rectangles) and REACT (filled rectangles) tasks. The vertical black arrows show the timing of the imperative release tone. The vertical dashed line is drawn at reaction time of 100 ms. The percentage of trials with reaction times less than 100 ms is shown to the right of the histogram distributions. Note that fast reaction times were common for the PREDICT condition when the SAS was presented 250 ms or less before the imperative cue.