Nonlinear engagement of action observation network underlying action anticipation in players with different levels of expertise

Abstract

The goal of this study was to reconcile inconsistency of neural engagement underlying action anticipation between experts and nonexperts, as well as between correct and incorrect anticipations. Therefore, we asked novice, intermediate, and skilled baseball batters (N, IB, and SB) to anticipate their swing decisions in response to pitching videos of a strike or ball, using functional magnetic resonance imaging. Behavioral results confirmed the effect of expertise that is generally shown in a linear fashion. Imaging results instead revealed a nonlinear relationship between expertise level and the evoked response amplitude of nodes within the action observation network. The relationship was best captured by an inverted U-shaped quadratic response profile across the three groups such that IB exhibited higher activation than did both SB and N. These empirical findings extend the framework of predictive coding as well as of neural efficiency in anticipating the action of others, and they might be associated with the underlying process to interpret the goal of the observed action and prepare one's own response. Furthermore, the right anterior cerebellum showed different levels of activation for correct and incorrect anticipations in all groups, adding novel evidence of its subtle involvement in anticipation processes irrespective of expertise status.

Decoding motor expertise from fine‐tuned oscillatory network organization

“…From mirror neurons to extended action observation networks (AONs), it is well‐known that executing and observing others' actions activates similar brain regions (Caspers, Zilles, Laird, & Eickhoff, 2010; Hardwick, Caspers, Eickhoff, & Swinnen, 2018; Rizzolatti & Craighero, 2004). Such sensorimotor activations are stronger for actions within the observer's expert motor repertoire (Calvo‐Merino, Glaser, Grezes, Passingham, & Haggard, 2005; Calvo‐Merino, Grezes, Glaser, Passingham, & Haggard, 2006), likely reflecting anticipatory resonant mechanisms rather than passive responses to visual stimuli (Aglioti, Cesari, Romani, & Urgesi, 2008; Chen, Chang, Huang, & Yen, 2020; Tomeo, Cesari, Aglioti, & Urgesi, 2013). This aligns with current predictive accounts of action processing (Avenanti, Paracampo, Annella, Tidoni, & Aglioti, 2018; Kilner, Friston, & Frith, 2007; Paracampo, Montemurro, de Vega, & Avenanti, 2018; Urgen & Saygin, 2020; Urgesi et al, 2010; Wilson & Knoblich, 2005), suggesting that we use our sensorimotor system to predict other's forthcoming actions.…”

The influence of pitcher handedness on pitch‐calling behavior: Insights from fMRI study on baseball umpires

“…pitch would be a strike or ball owing to their greater visual/perceptual experience with pitching actions and (at least partially) their motor experience in pitching (Chen et al, 2017(Chen et al, , 2020(Chen et al, , 2023Paull & Glencross, 1997;Ranganathan & Carlton, 2007).…”

“…Thus, these nodes are associated with the internal simulation of observed pitching action (Chen et al, 2023). Apart from its mirror property, the PMC is involved in predicting ongoing dynamic events ranging from human actions to non-biological actions such as ocean waves (Schubotz, 2007;Wolfensteller et al, 2007), reinforcing its role in action anticipation (Chen et al, 2020(Chen et al, , 2023.…”

“…The other AON node, the posterior middle temporal gyrus/superior temporal sulcus, is also activated when observing the action of a biological motion (Grossman et al, 2000;Grossman et al, 2010;Herrington et al, 2011;Pelphrey et al, 2005;Saygin, 2007), implying that pitching action can be processed using the structural and kinematic information of joints (Chen et al, 2020(Chen et al, , 2023. Furthermore, when viewing strike versus ball pitches, batters show different brain activation intensities within the AON nodes (Chen et al, 2020), particularly in the left ventral extrastriate cortex (Chen et al, 2020(Chen et al, , 2023. This activation is possibly associated with the processing of the relevant visual information conveyed by the pitching action and baseball trajectory.…”

“…At the neural level, we expected that umpires might engage the AON and subcortical motor regions during pitch-calling, as found in players and nonplayers during action anticipation (Chen et al, 2020(Chen et al, , 2023Karlinsky et al, 2017;Smith, 2016). Furthermore, the pitch effect may be found within the AON, specifically in the left ventral extrastriate cortex as batters process strikes and balls differently (Chen et al, 2020(Chen et al, , 2023. For the effect of pitcher handedness, activation in the ipsilateral aSPL and visual cortices was expected (Fiave & Nelissen, 2021;Shmuelof & Zohary, 2008), that is, left-handed pitchers would induce greater activation in the left aSPL and visual cortices than right-handed pitchers, and vice versa.…”