Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players

Abstract

The ability to predict the actions of others is quintessential for effective social interactions, particularly in competitive contexts (e.g. in sport) when knowledge about upcoming movements allows anticipating rather than reacting to opponents. Studies suggest that we predict what others are doing by using our own motor system as an internal forward model and that the fronto-parietal action observation network (AON) is fundamental for this ability. However, multiple-duty cells dealing with action perception and execution have been found in a variety of cortical regions. Here we used functional magnetic resonance imaging to explore, in expert basketball athletes and novices, whether the ability to make early predictions about the fate of sport-specific actions (i.e. free throws) is underpinned by neural regions beyond the classical AON. We found that, although involved in action prediction, the fronto-parietal AON was similarly activated in novices and experts. Importantly, athletes exhibited relatively greater activity in the extrastriate body area during the prediction task, probably due to their expert reading of the observed action kinematics. Moreover, experts exhibited higher activation in the bilateral inferior frontal gyrus and in the right anterior insular cortex when producing errors, suggesting that they might become aware of their own errors. Correct action prediction induced higher posterior insular cortex activity in experts and higher orbito-frontal activity in novices, suggesting that body awareness is important for performance monitoring in experts, whereas novices rely more on higher-order decision-making strategies. This functional reorganization highlights the tight relationship between action anticipation, error awareness and motor expertise leading to body-related processing and differences in decision-making processes.

The influence of motor expertise on the brain activity of motor task performance: A meta-analysis of functional magnetic resonance imaging studies

“…Recent research has indicated that motor expertise influences the brain activity of motor execution (e.g., Bernardi et al, 2013;Meister et al, 2005), motor observation (e.g., Kim et al, 2011;Olsson & Lundström, 2013;Pilgramm, Lorey, Stark, Munzert, Vaitl, & Zentgraf, 2010;Stout et al, 2011;, motor imagery or planning (e.g., Chang et al, 2011;Milton, Solodkin, Hlustík, & Small, 2007;Wei & Luo, 2010), motor prediction (e.g., Abreu et al, 2012;Balser et al, 2014;, and even the comprehension of action language (Beilock, Lyons, MattarellaMicke, Nusbaum, & Small, 2008;Lyons et al, 2010;Tomasino, Maieron, Guatto, Fabbro, & Rumiati, 2013). However, the findings are inconsistent.…”

Inferior frontal oscillations reveal visuo-motor matching for actions and speech: evidence from human intracranial recordings

“…The regions belonging to such a broad network for abstract representation of actions include the dorsal and ventral premotor cortex (Calvo-Merino, Glaser, Grezes, Passingham, & Haggard, 2005;Tai, Scherfler, Brooks, Sawamoto, & Castiello, 2004;Wade & Hammond, 2015), superior and inferior parietal lobule (Buccino, et al, 2001;Gardner, Goulden, & Cross, 2015), angular gyrus (Davey, et al, 2015;Farrer, et al, 2008;Lui, et al, 2008), supramarginal gyrus (Abreu, et al, 2012;Pokorny, et al, 2015), and superior temporal sulcus (Alaerts, et al, 2015; see also Cattaneo & Rizzolatti, 2009). …”

A Neurocognitive Approach to Expertise in Visual Object Recognition

“…This visual skill has been associated with activations in a body-selective region in OTC as well as in frontal and parietal areas. Whereas the former reflects expert reading of the observed action kinematics, the latter traditionally has been involved in action observation [47]. Extensive and varied activations have been observed in many additional domains of expertise, including architecture, musical notation reading, archery, taxi driving, and reading (for a review, see [31]).…”