Neural Correlates of Online Action Preparation

Abstract

When performing movements in rapid succession, the brain needs to coordinate ongoing execution with the preparation of an upcoming action. Here we identify the processes and brain areas involved in this ability of online preparation. Human participants (both male and female) performed pairs of single-finger presses or three-finger chords in rapid succession, while 7T fMRI was recorded. In the overlap condition, they could prepare the second movement during the first response and in the nonoverlap condition only after the first response was completed. Despite matched perceptual and movement requirements, fMRI revealed increased brain activity in the overlap condition in regions along the intraparietal sulcus and ventral visual stream. Multivariate analyses suggested that these areas are involved in stimulus identification and action selection. In contrast, the dorsal premotor cortex, known to be involved in planning upcoming movements, showed no discernible signs of heightened activity. This observation suggests that the bottleneck during simultaneous action execution and preparation arises at the level of stimulus identification and action selection, whereas movement planning in the premotor cortex can unfold concurrently with the execution of a current action without requiring additional neural activity.

Keywords: MVPA; action selection; fMRI; hand control; motor planning; sequential movements.

Figure 1.

Task design for Experiment 1. A, The cascade of processes constituting action preparation starts with stimulus-related processes (identical for chord and single-finger conditions; early) and ends with movement-related processes (more complex for chords and single-finger movements; late). B, Association between arbitrary cues and actions (single-finger presses and chords). Participants were divided into two groups, and for the second group, the symbol–response assignment was switched across press types. C, Visual stimulus and trial timeline in Experiment 1. Participants needed to produce the action indicated in the box simultaneously with high-pitch tones (black note). The symbol was on the screen during a variable preparation time before the tone (yellow box). Five small lines on the top represented the applied force on each key, with a press threshold of 0.8 N indicated by the red line. D, Example of two produced force trajectories (black dotted lines) with either large (left) or small mean deviations (right) from the ideal force trajectory (purple line). Trials are illustrated in a three-dimensional finger force space consisting of two active fingers (index and ring) and one passive digit (middle).

Figure 2.

Task design for Experiment 2. A, Visual display. Participants were instructed to produce the action indicated by the symbol in the bottom box. The content of the top box indicated the next action. Participants were instructed to fixate the cross between the two boxes, such that each symbol (∼1° from fixation) could be identified without shifting gaze. B, Time course of the continuous paradigm. One low-pitch tone (gray note) alternated with two high-pitch tones (black note). Participants had to produce actions indicated in the bottom box synchronously with high-pitch tones with ±200 ms (red intervals). The symbol displayed in the top and bottom box over time is indicated by the top and bottom yellow strip, respectively. In the overlap condition, the second symbol (&) was visible in the top box during the preparation phase of the first response. C, In the nonoverlap SS condition, the second response cue appeared together with the first tone, preventing online preparation. D, In the nonoverlap LS condition, the first response had a long preparation time.

Figure 3.

Three-finger chords take longer to prepare. A, Solid lines indicate the group-averaged accuracy as a function of available preparation time for single (blue) and chord (orange). The dotted lines are the model fit average across subjects. The vertical lines indicate the median time when the fitted curves for chord (orange) or single finger (blue) reach 80%. B, Similar to A but for mean deviation. Significant pairwise differences are indicated with ***p < 0.001, ns (not significant), p > 0.05, in a two-sided one–sample t test.

Figure 4.

Online preparation benefits execution. A, Accuracy for the first (left) and the second response (right) separate for single-finger and chord and overlap and nonoverlap conditions. B, Mean deviation from a straight-line force trajectory within correct trials for the first response (left) and second response (right) separate for single-finger and chord and overlap and nonoverlap conditions. Error bars indicate the SEM across participants. ***p < 0.001, **p < 0.01, *p < 0.05, using two-sided paired t test.

Figure 5.

Online preparation activates superior parietal and occipitotemporal regions. The inset shows the inflated cortical surface of the contralateral (left) hemisphere, highlighting the area of interest (A–C, purple). A, Flat representation of the neocortex with major sulci indicated by black dotted lines and ROIs by white borders. B, Group-averaged percent signal change for task versus resting baseline averaged across overlap and nonoverlap conditions and press types (single, chord). C, The difference in percent signal change between overlap and nonoverlap LS conditions, averaged across single finger and chord. Black dashed boundaries represent significant clusters. D, The activity difference between chord and single-finger conditions. The dashed outline is the same as in C. E, ROI-based analysis of percent signal change across overlap (purple)/nonoverlap (green) LS conditions for chords (dark) and single-finger presses (light). Error bars denote SEM across participants. Bars at the bottom of this panel show the significance of overlap versus nonoverlap LS effect and chord versus single effect within each region (dark gray, ***p < 0.001; light gray, **p < 0.005). ROIs: early auditory cortex (EAC), ventral stream visual cortex (VSVC), MT+ complex and neighboring visual areas (MT+), posterior superior parietal lobule (SPLp), anterior superior parietal lobule (SPLa), primary somatosensory cortex (S1), primary motor cortex (M1), dorsal premotor cortex (PMd), ventral premotor cortex (PMv), secondary motor area (SMA). Sulci: superior frontal sulcus (SFS), inferior frontal sulcus (IFS), precentral sulcus (PrCS), central sulcus (CS), postcentral sulcus (PoCS), intraparietal sulcus (IPS), parieto-occipital sulcus (POS), lateral occipital sulcus (LOS), lunate sulcus (LnS), superior temporal sulcus (STS), inferior temporal sulcus (ITS), collateral sulcus (CoS), sylvian fissure (SF).

Figure 6.

No evidence for extra online preparation activation in chord conditions. A, The contrast between the overlap and nonoverlap condition for single fingers and (B) for chords.

Figure 7.

Involvement of task-related network in cue-related and action-related processes. A, The average RDM for of group 1 was compared with the average RDM of Group 2 for actions with the same press type (left) or with the same set of cues (right). For M1, the similarity was high when the actions were matched. B, In MT+ region, the similarity was higher when the cues were matched. C,D, Group maps for the log Bayes factor for the action model (C) and cue model (D). Darker colors represent stronger evidence for encoding. Each map was thresholded with PXP >0.75 and log Bayes factor (logBF) >1. Black dashed outline is the same as in Figure 5C.