Prediction of human actions: expertise and task-related effects on neural activation of the action observation network

Abstract

The action observation network (AON) is supposed to play a crucial role when athletes anticipate the effect of others' actions in sports such as tennis. We used functional magnetic resonance imaging to explore whether motor expertise leads to a differential activation pattern within the AON during effect anticipation and whether spatial and motor anticipation tasks are associated with a differential activation pattern within the AON depending on participant expertise level. Expert (N=16) and novice (N=16) tennis players observed video clips depicting forehand strokes with the instruction to either indicate the predicted direction of ball flight (spatial anticipation) or to decide on an appropriate response to the observed action (motor anticipation). The experts performed better than novices on both tennis anticipation tasks, with the experts showing stronger neural activation in areas of the AON, namely, the superior parietal lobe, the intraparietal sulcus, the inferior frontal gyrus, and the cerebellum. When novices were contrasted with experts, motor anticipation resulted in stronger activation of the ventral premotor cortex, the supplementary motor area, and the superior parietal lobe than spatial anticipation task did. In experts, the comparison of motor and spatial anticipation revealed no increased activation. We suggest that the stronger activation of areas in the AON during the anticipation of action effects in experts reflects their use of the more fine-tuned motor representations they have acquired and improved during years of training. Furthermore, results suggest that the neural processing of different anticipation tasks depends on the expertise level.

Keywords: action anticipation; action observation; cerebellum; instructions; motor expertise.

Figure 1

Examples of all experimental conditions. Each of the 144 video clips lasted 2–3 s. (A) Male player performing a forehand stroke. The tennis stroke sequences were stopped at ball–racket contact and shown in both tennis anticipation conditions (motor anticipation, spatial anticipation). (B) Female player bouncing the ball with her racket (observation only condition). (C) Yellow ball moving down the screen on a vertical sinusoidal trajectory, disappearing at a random point in time (dashed line) (ball only condition). Please note that participants did not see the gray trajectory in the ball only condition.

Figure 2

Configuration and procedure for the 24 miniblocks. Each miniblock started with an instruction followed by six trials of one of the four experimental conditions. Each trial began with a fixation cross, followed by one of the 144 video clips and a subsequent response. The order of the miniblocks as well as the distribution of the videos was randomized for each participant.

Figure 3

Significant brain activation in all 32 participants for the comparison tennis anticipation > observation only. T maps were thresholded at t = 5.81 (P < 0.05, FWE‐corrected). Activation is rendered on a high‐resolution T1 template (“colin brain”).

Figure 4

Significantly stronger activation in the tennis experts compared to the novices for the comparison tennis anticipation > observation only. The blue vertical lines indicate the slice positions. T maps were thresholded at t = 2.50 (P < 0.05, FWE‐corrected). Activation is rendered on a high‐resolution T1 template (“colin brain”) as well as on the cerebellar SUIT template [Diedrichsen, 2006].

Figure 5

(A) Stronger activation in the novices in a between‐subject comparison of both groups for the contrast motor anticipation > spatial anticipation (blue marks). (B) Higher activation within the expert tennis players for the contrasts motor anticipation > spatial anticipation (red marks) and spatial anticipation > motor anticipation (blue marks). (C) Stronger activation within the novices for the contrast motor anticipation > spatial anticipation (red marks).T maps were thresholded at t = 3.00 (P < 0.05, FWE‐corrected). Activation is rendered on a high‐resolution T1 template (“colin brain”).