Elsevier

NeuroImage

Volume 45, Issue 2, 1 April 2009, Pages 512-521
NeuroImage

Judgment of actions in experts: A high-resolution EEG study in elite athletes

https://doi.org/10.1016/j.neuroimage.2008.11.035Get rights and content

Abstract

The present study tested the two following hypotheses: (i) compared to non-athletes, elite athletes are characterized by a reduced cortical activation during the judgment of sporting observed actions; (ii) in elite athletes, a good judgment of observed sporting actions is related to a low cortical activation. To address these issues, electroencephalographic (EEG) data were recorded in 15 elite rhythmic gymnasts and 13 non-gymnasts. They observed a series of 120 rhythmic gymnastic videos. At the end of each video, the subjects had to judge the artistic/athletic level of the exercise by a scale from 0 to 10. The mismatch between their judgment and that of the coach indexed the degree of action judgment. The EEG cortical sources were estimated by sLORETA. With reference to a pre-stimulus period, the power decrease of alpha (8–12 Hz) rhythms during the videos indexed the cortical activation (event related desynchronization, ERD). Regarding the hypothesis (i), low- and high-frequency alpha ERD was lower in amplitude in the elite rhythmic gymnasts compared to the non-gymnasts in occipital and temporal areas (ventral pathway) and in dorsal pathway. Regarding the hypothesis (ii), in the elite rhythmic gymnasts high-frequency alpha ERD was higher in amplitude with the videos characterized by a high judgment error than those characterized by a low judgment error; this was true in inferior posterior parietal and ventral premotor areas (“mirror” pathway). These results globally suggest that the judgment of observed sporting actions is related to low amplitude of alpha ERD, as a possible index of spatially selective cortical activation (“neural efficiency”).

Introduction

Previous neuroimaging studies using positron emission tomography (PET), single photon emission computed tomography (SPECT), and functional magnetic resonance imaging (fMRI) have shown that subjects with highest score to tests probing intelligent quotient, word fluency, spatial skills, and working memory have weakest fronto-parietal activation during cognitive tasks (Haier et al., 1988, Haier et al., 1992, Haier et al., 2004, Charlot et al., 1992, Parks et al., 1988; Rypma and D'Rypma and D'Esposito, 1999, Rypma et al., 2002, Rypma et al., 2005, Ruff et al., 2003). These results support the so called “neural efficiency” hypothesis, which postulates a more efficient cortical function in brighter as compared to individuals with poor performance to test probing cognitive functions. However, the “neural efficiency” hypothesis has been challenged by other neuroimaging evidence showing that fronto-parietal cortical activation was stronger in subjects with high cognitive performance (Newman et al., 2003, Gray et al., 2003).

To enlighten the physiological mechanism at the basis of the “neural efficiency”, cortical activity has been indexed by an event-related power decrease of resting electroencephalographic (EEG) alpha rhythms at about 8–12 Hz (alpha event-related desynchronization, ERD). It has been shown that people with high intelligent quotient (IQ) present low-amplitude alpha ERD during several cognitive tasks such as sentence–picture verification test (Neubauer et al., 1995), Posner's letter matching test (Neubauer et al., 1999), forward digit span task (Grabner et al., 2004), attention-switching task (Grabner et al., 2004), working memory task (Grabner et al., 2004), and Stankov's triplet numbers test (Neubauer and Fink 2003) as well as mental speed, short-term memory and reasoning tasks (Grabner et al., 2006). On the whole, these results have indicated a reduced (selective) event-related cortical activation in line with the “neural efficiency” hypothesis (Grabner et al., 2004).

In the last years, several lines of evidence have extended the “neural efficiency” hypothesis to cortical motor systems of “experts”. Firstly, compared to amateur rifle shooters, professionals showed a greater increase of occipital alpha power during pre-shot period (Haufler et al., 2000 Janelle et al., 2000). Secondly, occipital alpha power increased during the phases preceding the best shots and decreased during the phases preceding the worst shots in expert pistol shooters (Loze et al., 2001). Thirdly, amplitude of fMRI-BOLD activity was lower in professional piano players compared to control subjects, during complex finger movements (Krings et al., 2000). Fourthly, averaged scalp potentials related to the preparation of right voluntary wrist extension (readiness potential, RP) were lower in amplitude over supplementary motor and bilateral sensorimotor areas in elite kendo and gymnastic athletes compared to non-athletes (Kita et al., 2001). Fifthly, the RP overlying contralateral sensorimotor area was lower in amplitude in elite rifle and gun shooters compared to amateurs during the preparation of self-paced finger movements (Fattapposta et al., 1996, Di Russo et al., 2005).

To our knowledge, the “neural efficiency” hypothesis has not been explored during understanding of actions performed by others, an implicit grasp of what other people do or feel. To this regard, it has been shown that specialized fronto-parietal systems (mirror systems) allow us to directly understand the meaning of the actions of others and to sub-serve imitation and observational learning (Gallese et al., 2004, Rizzolatti and Craighero, 2004, Vogt and Thomaschke, 2007). These systems would be selectively active not only when one executes a given motor act (e.g. grasping), but also during the observation of motor acts. Some mirror neurons also show selective activation as a function of peculiar purpose of a certain action (e.g. grasping for eating, but not grasping for placing), so that they may represent the understanding of agent's intention (Rizzolatti et al., 2006). Activation of mirror systems during voluntary and observed movements is associated with alpha ERD over sensorimotor cortex in normal subjects (Babiloni et al., 2002, Ulloa and Pineda, 2007) but not in subjects with autism (Oberman et al., 2005).

The present study tested the two following hypotheses: (i) compared to non-athletes, elite athletes are characterized by a reduced cortical activation during the judgment of observed sporting actions; (ii) in elite athletes, a good judgment of observed sporting actions is related to a low cortical activation. To address these hypotheses, EEG data were recorded in elite rhythmic gymnasts and non-gymnasts. They observed a series of rhythmic gymnastic videos. At the end of each video, the subjects had to judge the artistic/athletic level of the exercise. The mismatch between their judgment and that of the coach indexed the degree of action judgment. Amplitude of alpha ERD was used as an index of spatially selective cortical activation (“neural efficiency”). Statistical EEG source analysis focused on 3 main brain circuits theoretically involved in the judgment of videos with sporting actions involving athletes and objects in movement. A first ventral cortical visual pathway was considered as it is typically involved in the recognition of objects (Braddick and Atkinson, 2007). A second dorsal cortical visual pathway was considered as it is typically involved in the analysis of visual space (Rolls and Stringer, 2006). A third fronto-parietal “mirror system” pathway was considered as it is typically involved in the understanding of actions performed by others (Gallese et al., 2004, Rizzolatti and Craighero, 2004, Vogt and Thomaschke, 2007).

Section snippets

Subjects and ethical approval

We recruited 15 elite rhythmic gymnasts (15 women) and 13 non gymnasts (10 women). The elite rhythmic gymnasts had been practicing rhythmic gymnastics for more than 8 years at least five times a week. They also regularly compete in national and international tournaments. The non-gymnasts did not play rhythmic gymnastics at competitive or amateur level. The mean subjects' age was 21.4 years in elite rhythmic gymnasts (± 1 standard error, SE; range: 16 to 27 years) and 20.8 years in the

Behavioral data (judgment error)

For illustrative purpose, Fig. 2 shows the distribution of judgment error for each rhythmic gymnastic video for the two groups (elite rhythmic gymnasts and non-gymnasts). The mean judgment error (± SE) was 1.14 (± 0.04 SE) for the elite rhythmic gymnasts and 1.67 (± 0.04 SE) for the non-gymnasts. As expected, the ANOVA showed a main effect for the factor Group (F(1,24) = 101.7; p < 0.00001), confirming the hypothesis of a lower judgment error for the elite rhythmic gymnasts compared to the

Discussion

In line with the “neural efficiency” hypothesis in experts, we tested the hypothesis that compared to non-gymnasts, elite rhythmic gymnasts are characterized by a reduced cortical activation (alpha ERD) in visuomotor systems during the judgment of observed actions. Furthermore, we predicted that in elite rhythmic gymnasts, a good judgment of videos with rhythmic gymnastic performances is associated with low cortical activation (alpha ERD) in visuomotor systems. As a methodological novelty, the

Acknowledgments

The research was granted by Sport Medicine School - University of Rome Sapienza, Tosinvest Sanità, and Federazione Ginnastica d'Italia (FGI).

Dr. Francesco Infarinato and Dr. Roberta Lizio participated to this study in the framework of their Ph.D. program at the Doctoral School in Neurophysiology, Department of Physiology and Pharmacology, University of Rome “Sapienza”.

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