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.
Highlights
Our environment is filled with sensory cues that influence the timing and expression of voluntary actions
Predicted movements are preceded by preparatory cortical activity In contrast to task performance, the time course of cortical preparation was markedly different between conditions (Figure 2)
The PREDICT condition was associated with a Contingent Negative Variation (CNV) waveform characterized by an initial auditory-evoked potential in response to the warning tone at 23500 ms, a subsequent period of sustained activity with a slow developing negative slope, followed by a more rapid-rising negative potential beginning an average of 1459 6 320 ms prior to the onset of wrist extensor muscle activity (Figures 2B and 2C)
Summary
Our environment is filled with sensory cues that influence the timing and expression of voluntary actions. Relevant cues often require a reaction to the stimulus (reactive movements) or provide advance information that can be used to proactively plan the timing and content of the forthcoming actions (predictive movements) In the latter context, movements are often preceded by a slow-rising increase in cortical activity beginning as much as 2–3 seconds before movement onset [1,2,3]. It has been proposed that preparatory activity reflects the initial state of a dynamical system in which the early neuronal population activity does not represent the forthcoming movement parameters [12] Resolution of this problem is greatly limited by the inability to decode the function of movementrelated preparatory activity, whether obtained from single-, multiunit or local field potential recordings of neuronal activity in behaving non-human primates or scalp surface recordings from humans, and its relationship to the eventual motor output
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