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Behavioural Brain Research 207 (2010) 466–475

Contents lists available at ScienceDirect

Behavioural Brain Research

journa l homepage: www.e lsev ier .com/ locate /bbr

esearch report

Neural efficiency” of experts’ brain during judgment of actions: Aigh-resolution EEG study in elite and amateur karate athletes

laudio Babilonia,b,∗, Nicola Marzanoc, Francesco Infarinatod, Marco Iacobonie, Giulia Rizzae,ierluigi Aschieri f,g, Giuseppe Cibelli a, Andrea Soricelli c,h, Fabrizio Eusebie,i, Claudio Del Percioe

Department of Biomedical Sciences, University of Foggia, Foggia, ItalyCasa di Cura San Raffaele Cassino, ItalyIRCCS SDN Istituto di Ricerca Diagnostica e Nucleare, Napoli, ItalyIRCCS San Raffaele Pisana, Roma, ItalyDipartimento di Fisiologia e Farmacologia, Università “Sapienza”, Roma, ItalyFederazione Italiana Judo Lotta Karate ed Arti Marziali (FIJLKAM), Roma, ItalyFacoltà di Scienze Motorie, Università de L’Aquila, L’Aquila, ItalyUniversità degli Studi di Napoli Parthenope, Napoli, ItalyIRCCS Neuromed, Via Atinense 18, I86077 Pozzilli (Isernia), Italy

r t i c l e i n f o

rticle history:eceived 31 July 2009eceived in revised form 22 October 2009ccepted 26 October 2009vailable online 3 November 2009

eywords:EGlpha event-related desynchronization

ERD)lite karate athletes

a b s t r a c t

Here we tested two working hypotheses on spatially selective cortical activation (“neural efficiency”)in experts: (i) compared to non-athletes, elite karate athletes are characterized by a reduced corticalactivation during the judgment of karate actions; (ii) compared to non-athletes and elite karate athletes,amateur karate athletes are characterized by an intermediate cortical activation during the judgment ofkarate actions. Electroencephalographic (EEG) data were recorded in 16 elite karate athletes, 15 amateurathletes and 17 non-athletes. They observed a series of 120 karate videos. At the end of each video, thesubjects had to judge the technical/athletic level of the exercise by a scale from 0 to 10. The mismatchbetween their judgment and that of the coach indexed the degree of action judgment. The EEG corticalsources were estimated by sLORETA. With reference to a pre-stimulus period, the power decrease of alpha(8–12 Hz) rhythms during the video indexed the cortical activation (event-related desynchronization,

ERD). Regarding the hypothesis of reduced activity in elite karate athletes, low- and high-frequencyalpha ERD was less pronounced in dorsal and “mirror” pathways in the elite karate athletes than inthe non-athletes. Regarding the hypothesis of intermediate cortical activity in amateur karate athletes,low- and high-frequency alpha ERD was less pronounced in dorsal pathways across the non-athletes,the amateur karate athletes, and the elite karate athletes. In conclusion, athletes’ judgment of observedsporting actions is related to less pronounced alpha ERD, as a possible index of “neural efficiency” in

cogn

experts engaged in social

. Introduction

“Neural efficiency” hypothesis posits a more efficient corticalunction in individuals with high performance as compared to thoseith poor performance to test probing cognitive functions, as a

table, trait-like construct that varies between individuals [1–5].The “neural efficiency” hypothesis has been repeatedly tested by

euroimaging studies using positron emission tomography (PET),ingle photon emission computed tomography (SPECT), and func-

∗ Corresponding author at: Department of Biomedical Sciences, University of Fog-ia, Viale Pinto 7, Foggia I-71100, Italy. Tel.: +39 0881 713276;ax: +39 0881 711716.

E-mail addresses: c.babiloni@unifg.it, claudio.babiloni@uniroma1.it (C. Babiloni).

166-4328/$ – see front matter © 2009 Elsevier B.V. All rights reserved.oi:10.1016/j.bbr.2009.10.034

ition.© 2009 Elsevier B.V. All rights reserved.

tional magnetic resonance imaging (fMRI) showing that subjectswith highest score to tests probing intelligent quotient (IQ), wordfluency, spatial skills, and working memory have weakest fronto-parietal activation during cognitive tasks [2–10]. However, thishypothesis has been challenged by other neuroimaging evidenceshowing that fronto-parietal cortical activation is stronger in sub-jects with high cognitive performance [11,12].

To show the physiological mechanism at the basis of the“neural efficiency” hypothesis, cortical activity has been indexedby an event-related power decrease/increase of resting elec-

troencephalographic (EEG) alpha rhythms at 8–12 Hz (alphaevent-related desynchronization/synchronization, ERD/ERS). It hasbeen demonstrated that people with high intelligent quotient (IQ)show low-amplitude alpha ERD during several cognitive tasks[13–16]. The same was true in subjects highly trained for specific

C. Babiloni et al. / Behavioural Brain Research 207 (2010) 466–475 467

Fig. 1. Experimental paradigm. Subjects observed a series of 120 karate videos. The videos showed elite karate athletes performing choreographed actions against imaginaryo o lastew cts hat

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pponents during national or international competitions (Kata specialty). Each videas always present as a target for eyes fixation. At the end of each video, the subje

o 10. The same was done by their coach.

kills (“experts”) during the execution of short-term memory tasks17].

In the last years, several lines of evidence have extended theneural efficiency” hypothesis to cortical motor and visual systemsf “experts” such as elite kendo and gymnastic athletes [18], eliteifle and gun shooters [19–24], elite karate and fencing athletes25,26].

Recently, the “neural efficiency” hypothesis has been confirmedn elite athletes engaged in a task of social cognition [27]. Duringhe judgment of observed sporting actions, alpha ERD was lower inmplitude in elite rhythmic gymnasts than in non-gymnasts [27].his was true in ventral cortical visual pathway typically involved inhe recognition of objects [28] and in dorsal cortical visual pathwayypically involved in the analysis of visual space [29]. Within thelite athletes, the best judgments of the observed sporting actionsere related to low-amplitude alpha ERD in fronto-parietal “mir-

or” pathway typically involved in the understanding of actionserformed by others [30–32], in agreement with previous EEG find-

ngs showing that observation of movements is associated withlpha ERD over sensorimotor cortex in healthy subjects [33,34]ut not in patients with autism [35]. The mentioned patterns ofortical activation were compatible with the fact that the taskequired the recognition of objects (rope, hoop, ball, ribbon, andlubs) and spatial trajectories/relationships, as well as the under-tanding of the meaning of actions performed by others. This isn agreement with previous functional magnetic resonance (fMRI)vidence reporting that expert guitarists showed a reduced cor-ical activation in “mirror” system during the observation of theracticed compared to nonpracticed actions [36]. On the contrary,

t has been shown a greater alpha ERD in professional dancershan in control subjects during the observation of dance videosrom 1 until 2 s after movement onset [37]. Furthermore, previousMRI studies have reported: (i) greater activation in “mirror” sys-em when expert dancers viewed movements that they had beenrained to perform compared to movements they had not [38]; (ii)reater activation in premotor, parietal, and cerebellar areas whenancers viewed moves from their own motor repertoire, comparedo moves that they frequently saw but did not perform [39]; (iii)tronger activation in the “mirror” system when dancers observedancing movements that were part of the individual’s motor reper-oire, compared to observation of nonpracticed movements [40];

iv) stronger activation in the “mirror” system when naïve sub-ects saw a musician playing guitar accords [41]. These differentndings might be related to practice-related increase and decreasef regional activations as a function of brain reorganization andedistribution of cognitive and sensorimotor processes [42], which

d 8 s with a random inter-stimulus interval ranging from 4.5 to 5.5 s. A central crossd to judge the artistic/athletic level of the karate exercise by a scale ranging from 0

would be associated to changes in grey and white matter volumeor in hippocampus [43–45,67].

The present EEG study contributed to the vivid debate on the“neural efficiency” hypothesis in experts. With respect to the men-tioned study by Babiloni and colleagues [25–27], the present EEGstudy evaluated the cortical activation (alpha ERD) accompanyinga social cognition task as a function of athletes’ expertise (elitekarate athletes vs. amateur karate athletes and non-athletes). Fur-thermore, it evaluated the cortical activation accompanying thejudgment of sporting actions with negligible object recognition.Specifically, two novel hypotheses were evaluated: (i) comparedto non-athletes and elite karate athletes, amateur karate athletesare characterized by a intermediate cortical activation during thejudgment of observed karate actions; (ii) compared to non-athletes,elite karate athletes are characterized by a reduced cortical activa-tion in dorsal cortical visual pathway and fronto-parietal “mirror”system during the judgment of karate actions (i.e. no object recog-nition).

2. Methods

2.1. Subjects and ethical approval

We recruited 17 (7 women) elite karate athletes, 15 (8 women) amateurkarate athletes, and 17 (11 women) non-athletes. All subjects were right-handedas revealed by Edinburgh inventory. The elite karate athletes were part of Italiannational karate team. They had been practicing karate for more than 12 years atleast five times a week. They also regularly compete in national and internationaltournaments. The amateur karate athletes practiced karate from 2 to 5 years, andthey usually practiced two times a week. The non-athletes did not play karate orsports similar to karate (i.e. kung fu, etc.) at competitive or amateur level. The meansubjects’ age was 23.8 years in the elite karate athletes (±1 standard error, SE; range:20–33 years), 21.5 years in the amateur karate athletes (±2 SE; range: 17–33 years),and 24.6 years in the non-athletes (±1.4 SE; ranging from 17 to 35 years). Twoanalyses of variance (ANOVA) using the factor Group (elite karate athletes, amateurkarate athletes, non-athletes) were computed to evaluate the presence or absenceof statistically significant differences among the three groups for age and gender.No statistically significant difference was found (age: p > 0.1; gender: p > 0.5). How-ever, the age and gender values were used as covariates in the subsequent statisticalanalysis to exclude that small differences in age and gender could influence the sub-sequent statistical analysis. All subjects gave their informed consent according tothe Declaration of Helsinki. They were free to withdraw from the study at any time.The procedure was approved by the local Institutional Ethics Committee (I MedicalSchool, University of Rome “Sapienza”). The karate subjects were sent to our EEGlab by coworkers of the Karate Italian Federation (FIJLKAM).

2.2. Experimental procedure

The subjects comfortably seated in an armchair in front of a computer mon-itor. The distance between subjects and monitor was of 90 cm. They observed aseries of 120 karate videos (Fig. 1). The videos showed elite karate athletes per-forming choreographed actions against imaginary opponents during national or

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68 C. Babiloni et al. / Behavioural

nternational competitions (Kata speciality). They were taken from a karate federalrchive used for educational purposes. This archive includes videos of high- andow-level karate performances according to the international guidelines for karateeferees. For its educational purpose, the archive does not include videos of ambigu-us karate performances. Each video lasted 8 s (frequency rate: 25 Hz; 200 frames;imension of each frame: 720 × 576 pixels) with a random inter-stimulus intervalanging from 4.5 to 5.5 s. A central cross was always present as a target for eyes fix-tion. At the end of each video, the subjects had to judge the technical/athletic levelf the karate exercise by a scale ranging from 0 to 10. The same was done by theiroach. The judgments of the coach of the Italian karate team were considered as aold standard for the evaluation of action judgment in the present athletes. Such aehavioural analysis was performed for at least two reasons. Firstly, this behaviouralerformance ensured that all subjects paid attention to the videos in line with pre-ious studies investigating action observation [40,27]. Secondly, we could test theontrol hypothesis that the elite karate athletes globally followed the implicit judg-ent rules of their coach, the amateur karate athletes globally gave an approximate

valuation of athletes’ performance, and the non-athletes globally gave an unedu-ated evaluation of athletes’ performance. Of note, the recruited elite athletes hadeceived several months of daily, intense (4–6 h) training under the continuous tech-ical guidance/feed-back of their coach. Along this training, the coach transferred tohem his peculiar technical/athletic criteria for the judgment of a perfect/erroneousarate performance. Noteworthy, the study aim required the definition of the ath-etes’ “peculiar” judgment criteria rather than the definition of “absolute” judgmentriteria. These “peculiar” judgment criteria are much more similar to those of theirersonal coach than to those of any other person, due to the years spent together tohare these criteria. In this line of reasoning, averaging the technical/athletic judg-ents of “external” coaches would have introduced inter-subjects variability in the

gold standard” reference ensured by the judgments of the athletes’ coach.For sake of homogeneity, the judgments of the coach of the Italian karate team

ere considered as a gold standard for the evaluation of action judgment also in themateur athletes and non-athletes. Another reason of this methodological choiceas that the amateur karate athletes had neither a unique coach nor an experience

f intensive training with any coach.

.3. EEG recordings

The EEG data were continuously recorded (bandpass: 0.01–100 Hz, samplingate: 256 Hz; EB-Neuro Be-plus©, Firenze, Italy) from 56 scalp electrodes (cap) posi-ioned over the whole scalp according to the 10–10 system. Electrical reference wasocated between the AFz and Fz electrodes, and the ground electrode was locatedetween the Pz and Oz electrodes. Electrode impedance was kept below 5 k�. In par-llel, the recording of bipolar electrooculographic data (EOG; bandpass: 0.1–100 Hz;ampling rate: 256 Hz) monitored blinking and eye movements. Finally, electromyo-ram (EMG; bandpass: 0–100 Hz; sampling rate: 256 Hz) of first dorsal interosseumuscles of both hands was recorded to monitor involuntary movements or other

nspecific muscle activations.

.4. Preliminary data analysis

The recorded EEG, EOG and EMG data were segmented into single trials lasting0 s, each spanning from −2 to +8 s with reference to the zerotime, defined as thenset of the karate video. For each EEG single trial, the period spanning from −2 so zerotime was considered as baseline and that from +1 to +7 s as event.

Data epochs with instrumental, ocular, and muscular artifacts were identi-ed and automatically eliminated by a computerized procedure using EEG, EOG,nd EMG signals as an input [46]. The EEG data contaminated by ocular artifactsere corrected by an autoregressive method [46]. Finally, two expert electroen-

ephalographists (C.D.P. and F.I.) manually confirmed this automatic selection andorrection, with special attention to residual contaminations of the EEG epochs dueo eye movements and blinking. Therefore, only the EEG epochs totally free from arti-act residuals were accepted for the subsequent analyses. These EEG epochs wereeferred to common average reference for further analyses. The mean number of thertifact-free EEG single trials was of 81 (±6 SE) for the elite karate athletes, 83 (±3E) for the amateur karate athletes, and 92 (±3 SE) for the non-athletes. Of note, anNOVA using the factor Group (elite karate athletes, amateur karate athletes, non-thletes) served to compare the amount of artifact-free EEG single trials betweenhe two groups. No statistically significant difference was found (p > 0.15).

.5. Frequency analysis of alpha rhythms

Power spectrum analysis of the artifact-free EEG data was based on FFT approachsing Welch technique and Hanning windowing function (1 Hz frequency resolu-ion). For the determination of the alpha sub-bands, individual alpha frequency (IAF)eak was identified according to literature guidelines [47–49]. The IAF is defined as

he frequency within the 6–13 Hz range of the EEG spectrum showing the maximumower. With reference to the IAF, the alpha sub-bands of interest were as follows:

ow-frequency alpha band as IAF−2 Hz to IAF, and high-frequency alpha band asAF to IAF+2 Hz. The mean IAF value was 10.5 Hz (±0.3 SE) for the elite karate ath-etes, 10.8 Hz (±0.2 SE) for the amateur karate athletes, and 10.4 Hz (±0.3 SE) forhe non-athletes. There was no significant inter-groups difference in the IAF peak

Research 207 (2010) 466–475

as evaluated by an ANOVA (p > 0.4). However, the IAF peak was used as a covariate(together with age and gender) for further statistics on EEG data to control for slighteffects of IAF on the EEG comparisons.

2.6. Cortical source analysis of the EEG rhythms by sLORETA

The artifact-free EEG data were given as an input to the original standardizedlow-resolution brain electromagnetic tomography (sLORETA) software for the EEGsource analysis ([50]; http://www.unizh.ch/keyinst/NewLORETA/LORETA01.htm).sLORETA is a functional imaging technique belonging to a family of standardizedlinear inverse solution procedures, modeling 3D distributions of the cortical sourcepatterns generating scalp EEG data [50]. With respect to the dipole modeling ofEEG cortical sources, no a priori decision of the dipole position is required by theinvestigators in sLORETA estimation. In a previous paper, it has been shown thatsLORETA is quite efficient when compared to linear inverse algorithms like min-imum norm solution, weighted minimum norm solution or weighted resolutionoptimization [50]. Furthermore, sLORETA has been successfully used in recent EEGand MEG studies [27,51–53,54].

sLORETA computes 3D linear solutions (sLORETA solutions) for the EEG inverseproblem standardized with respect to instrumental and biological noise as mathe-matically defined in the original paper by Pascual-Marqui [50]. sLORETA solutionsare computed within a three-shell spherical head model including scalp, skull, andbrain compartments. The brain compartment is restricted to the cortical grey mat-ter/hippocampus of a head model co-registered to the Talairach probability brainatlas, which has been digitized at the Brain Imaging Center of the Montreal Neu-rological Institute [55]. This compartment includes 6239 voxels (5 mm resolution),each voxel containing an equivalent current dipole. The head model for the inversesolution uses the electric potential lead field computed with a boundary elementmethod (BEM) applied to the MNI152 template [56]. The electrode coordinates werebased on the average location of the 10–5 system placement system [57].

As a methodological remark, the use of sLORETA cannot resolve fine functionaltopographical details in parietal and premotor areas, when compared to PET orfMRI. Nevertheless, we preferred the use of the present high-resolution EEG tech-nique, since it allowed testing the hypothesis that the modulation of dominant alpharhythms is a putative physiological mechanism at the basis of the judgment of theobserved actions in experts.

2.7. Event-related desynchronization/synchronization (ERD/ERS)

The sLORETA solutions were used to index the magnitude of the brainrhythmicity. Specifically, they served to compute the event-related desynchroniza-tion/synchronization (ERD/ERS) of the low- and high-frequency alpha sub-bands.The alpha ERD/ERS was defined as the percentage decrement/increment of instantpower density at the event period compared to a pre-stimulus. The formula was thefollowing:

(event − pre

pre× 100

).

Three event periods were considered: T1 as the period from +1 to +3 s withrespect to the zerotime, T2 as the period from +3 to +5 s, and T3 as the period from+5 to +7 s. The pre-stimulus period was defined as the period from −2 s to the zero-time in all artifact-free EEG single trials. The three time periods served to evaluatewhether “neural efficiency”, as revealed by alpha ERD, was evident along the wholevideo presentation or only during the beginning of the video presentation as shownby Orgs et al. [37].

2.8. Alpha ERD/ERS at Brodmann areas

Since the sLORETA procedure intrinsically provides “low-resolution” EEG sourcesolutions, we decided to evaluate these solutions at the rough level of Brodmannareas (BAs). At this level, the sLORETA solutions for a certain BA were defined as themean of the sLORETA solutions across all the voxels of that BA. The following BAswere considered: BA 5, BA 6 dorsal (6d), BA 6 ventral (6v), BA 7, BA 19, BA 20, BA 37,BA 40, and BA 44/45. It is supposed that these BAs roughly belong to 3 main braincircuits: the BAs 19, 37, 20 would be part of a ventral cortical visual pathway; theBAs 7, 5, 6d would be part of a dorsal cortical visual pathway; and the BAs 40, 6v,44/45 would be part of the so called mirror systems [30–32].

2.9. Statistical analysis

Statistical comparisons were mainly performed by ANOVA. With the ANOVA,Mauchley’s test evaluated the sphericity assumption when necessary. Correction ofthe degrees of freedom was made with the Greenhouse–Geisser procedure, and Dun-

can’s test was used for post hoc comparisons (p < 0.05). Specifically, the following 2statistical sessions were performed.

The first session tested the hypothesis of a progressive increase of the evalua-tion of athletes’ performance across the non-athletes, the amateur karate athletes,and the elite karate athletes. In other words, the working hypothesis was that theelite karate athletes globally followed the implicit judgment rules of their coach, the

Brain Research 207 (2010) 466–475 469

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Table 1Values (Spearman R coefficient and p level) of the linear correlation between thejudgment score of each subject and that of his/her coach.

Spearman R p level

Non-athletesSubj. 01 −0.16 >0.1Subj.02 −0.11 >0.1Subj.03 0.04 >0.1Subj.04 0.03 >0.1Subj.05 0.06 >0.1Subj.06 −0.03 >0.1Subj.07 0.05 >0.1Subj.08 0.17 >0.05Subj.09 0.23 <0.05Subj.10 0.19 >0.05Subj.11 −0.05 >0.1Subj.12 −0.07 >0.1Subj.13 −0.01 >0.1Subj.14 0.17 >0.05Subj.15 0.04 >0.1Subj.16 −0.04 >0.1Subj.17 0.08 >0.1

Subj. 01 0.26 <0.05Subj.02 0.26 <0.05Subj.03 0.11 >0.1Subj.04 0.08 >0.1Subj.05 0.19 >0.05Subj.06 0.09 >0.1Subj.07 0.16 >0.1Subj.08 0.15 >0.1Subj.09 0.21 <0.01Subj.10 0.16 >0.1Subj.11 0.25 <0.05Subj.12 0.24 <0.05Subj.13 0.15 >0.1Subj.14 0.4 <0.01Subj.15 0.12 >0.1

Elite athletesSubj. 01 0.61 <0.01Subj.02 0.5 <0.01Subj.03 0.34 <0.01Subj.04 0.31 <0.01Subj.05 0.38 <0.01Subj.06 0.34 <0.01Subj.07 0.26 <0.01Subj.08 0.45 <0.01Subj.09 0.37 <0.01Subj.10 0.38 <0.01Subj.11 0.53 <0.01Subj.12 0.45 <0.01Subj.13 0.27 <0.01

C. Babiloni et al. / Behavioural

mateur karate athletes globally gave an approximate evaluation of athletes’ per-ormance, and the non-athletes globally gave an uneducated evaluation of athletes’erformance. To this aim, we evaluated for each subject the correlation between the

udgment value of the subject and that of the coach for the videos associated withhe (artifact-free) EEG single trials (Spearman test, p < 0.01). A statistical thresholdf p < 0.01 was established to take into account the repetition of the correlationnalysis in the 16 elite karate athletes, 15 amateur karate athletes and 17 non-thletes. Furthermore, we performed an ANOVA having the Spearman R coefficients a dependent variable and the factor Group (elite karate athletes, amateur karatethletes). Age and gender were used as covariates. Of note, the Spearman R coef-cient values were subjected to hyperbolic tangent transformation to make thesealues Gaussian.

The second session (EEG data) tested the hypothesis of a reduction in magni-ude of the alpha ERD across non-athletes, amateur karate athletes, and elite karatethletes, in line with the idea of “neural efficiency”. To this aim, we performed 6NOVAs (2 alpha sub-bands × 3 brain circuits). The ANOVAs had the alpha ERD/ERSs a dependent variable. The ANOVA factors were Group (elite karate athletes, ama-eur karate athletes, non-athletes), Time (T1, T2, T3), Side (Left, Right), and ROI (BAs9, 37, 20 for the ventral cortical visual pathway; BAs 7, 5, 6d for the dorsal corti-al visual pathway; and the BAs 40, 6v, 44/45 for the mirror systems). The workingypotheses would be confirmed by the following statistical results: (i) a statisticalNOVA effect including the factor Group (p < 0.05); (ii) a post hoc test indicatingtatistically significant differences of the alpha ERD with the pattern elite karatethletes < non-athletes; (iii) a post hoc test indicating statistically significant dif-erences of the alpha ERD with the pattern elite karate athletes < amateur karatethletes < non-athletes (Duncan test, p < 0.05).

. Results

.1. Behavioural data (judgment error)

For descriptive purposes, the “mean (±SE) judgment error”,efined as the absolute value of the difference between the scoref the subject and that of the coach of the Italian team of karatecross videos, was 0.97 (±0.05 SE) for the elite karate athletes, 1.13±0.1 SE) for the amateur karate athletes, and 1.51 (±0.1 SE) forhe non-athletes. Of note, we did not perform a statistical compar-son of these mean values among the groups, since this procedures not able to take into account that giving a medium-high score toll videos, the “mean (±SE) judgment error” would be quite low.o obtain a valid index of the judgment correctness with referenceo that of the coach of the Italian karate team, we computed theorrelation between the judgment score of each subject and thatf that coach (Spearman test). Table 1 reports the values of suchorrelation. There was a statistically significant positive linear cor-elation for all elite karate athletes (r = 0.3–0.55; p = 0.01–0.000001;ean r = 0.4). On the contrary, there was no statistically significant

ositive linear correlation for the karate amateur athletes exceptwo subjects (r = 0.08–0.4; p = 0.4–0.001; mean r = 0.19). Similarly,here was no statistically significant positive linear correlation forll non-athletes (r = −0.15 to 0.23; p = 0.8–0.02; mean r = 0.04). Asxpected, the ANOVA showed a main effect for the factor GroupF(2,43) = 54.2; p < 0.0001). Duncan post hoc testing indicated thatpearman R coefficient was stronger in the elite karate athletesompared to the amateur karate (p < 0.0001) and the non-athletesp < 0.0006). It was also stronger in the amateur karate athletesompared to the non-athletes (p < 0.0002). These results confirmedhe hypothesis of a progressive increase of the evaluation of ath-etes’ performance across the non-athletes, the amateur karatethletes, and the elite karate athletes. This is probably due to theact that the proper use of the mentioned subjective scale impliesquite long training (several years).

.2. Cortical alpha ERD/ERS: elite karate athletes vs. amateurarate athletes vs. non-athletes

For illustrative purpose, Fig. 2 shows the grand average ofhe sLORETA solutions modeling distributed EEG sources of theow- (about 8–10 Hz) and high-frequency (about 10–12 Hz) alphaRD/ERS in the elite karate athletes, karate amateur athletes, and

Subj.14 0.41 <0.05Subj.15 0.46 <0.01Subj.16 0.29 <0.01

non-athletes. The maps of the non-athletes were characterized byan evident alpha ERD, more represented in parietal and occipi-tal areas. Compared to the non-athletes, the elite karate athletesshowed a lower alpha ERD along the whole video presentation, asa possible index of spatially selective cortical activation (neural effi-ciency). With respect to the non-athletes and elite karate athletes,the amateur karate athletes showed an intermediate magnitude ofthe alpha ERD at parietal and occipital areas. This was true alongthe whole video observation period.

The ANOVA of the low-frequency alpha ERD/ERS in the ventralpathway showed no statistically significant difference (p > 0.1). TheANOVA of the low-frequency alpha ERD/ERS in the dorsal pathwaypointed to just one statistically significant effect including the fac-

tor Group, namely an interaction (F(8,180) = 2.96; p < 0.004) amongthe factors Group (elite karate athletes, amateur karate athletes,non-athletes), Time (T1, T2, T3), and ROI (BA 7, BA 5, BA 6d; see Fig. 3top). Duncan post hoc testing indicated that low-frequency alpha

470 C. Babiloni et al. / Behavioural Brain Research 207 (2010) 466–475

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ig. 2. Grand average of sLORETA solutions modeling the distributed EEG sources othletes, and non-athletes.

RD followed the pattern elite karate athletes < amateur karate ath-etes < non-athletes at BA 7 (Time T2; p < 0.05), BA 5 (Time T1 and2; p < 0.05), and BA 6d (Time T2; p < 0.0005). Furthermore, theow-frequency alpha ERD followed the pattern elite karate ath-etes < non-athletes at BA 7 (Time T1, T2; p < 0.0005), BA 5 (Time T1,2 and T3; p < 0.0005), and BA 6d (Time T1, T2 and T3; p < 0.0005).inally, the ANOVA of the low-frequency alpha ERD/ERS in themirror” pathway showed no statistically significant differencesp > 0.15).

The ANOVA of the high-frequency alpha ERD/ERS in the ven-ral pathway showed no statistically significant differences (p > 0.1).he ANOVA of the high-frequency alpha ERD/ERS in the dorsal path-ay pointed to just one statistically significant effect including

he factor Group, namely an interaction (F(8,180) = 2.04; p < 0.05)mong the factors Group (elite karate athletes, amateur karate ath-etes, non-athletes), Time (T1, T2, T3), and ROI (BA 7, BA 5, BAd; see Fig. 3 bottom). Duncan post hoc testing indicated thatigh-frequency alpha ERD followed the pattern elite karate ath-

ig. 3. (Top) Across subject means of the low-alpha ERD/ERS amplitude illustrating statarate athletes, non-athletes), Time (T1, T2, T3) and ROI (BA 7, BA 5, BA 6d). (Bottom) Atatistical ANOVA interaction among the factors Group (elite karate athletes, amateur ksterisks indicate the sLORETA solutions at which alpha ERD presented statistically signifithletes < non-athletes (Duncan post hoc testing, ***p < 0.0005; **p < 0.005; *p < 0.05).

ow- and high-frequency alpha ERD/ERS in the elite karate athletes, amateur karate

letes < amateur karate athletes < non-athletes at BA 7 (Time T1, T2and T3; p < 0.05), BA 5 (Time T1, T2 and T3; p < 0.05), and BA 6d(Time T2; p < 0.005). Furthermore, the high-frequency alpha ERDfollowed the pattern elite karate athletes < non-athletes at BA 7(Time T1, T2 and T3; p < 0.05), BA 5 (Time T1, T2 and T3; p < 0.0005),and BA 6d (Time T1, T2 and T3; p < 0.0005). Finally, as unique statis-tically significant effects including the factor Group, the ANOVA ofthe high-frequency alpha ERD/ERS in the “mirror” pathway pointedto a main effect (F(2,42) = 3.5; p < 0.03). Indeed, the high-frequencyalpha ERD was lower in the elite karate athletes (25%) than in thenon-athletes (40%).

For illustrative purpose, Figs. 4 and 5 show the across subjectmeans of the low- and high-frequency alpha ERD/ERS amplitude

illustrating non-statistical ANOVA interactions among the factorGroup (elite karate athletes, amateur karate athletes, non-athletes),Time (T1, T2, T3), and ROI (BA 19, BA 37, BA 20 for the ventral corticalpathways; BA 40, BA 6d, BA 44/45 for the mirror pathways) for theventral and mirror pathways.

istical ANOVA interaction among the factors Group (elite karate athletes, amateurcross subject means of the high-frequency alpha ERD/ERS amplitude illustratingarate athletes, non-athletes), Time (T1, T2, T3) and ROI (BA 7, BA 5, BA 6d). Thecant differences with respect to the pattern: elite karate athletes < amateur karate

C. Babiloni et al. / Behavioural Brain Research 207 (2010) 466–475 471

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ig. 4. Across subject means of the low- and high-frequency alpha ERD/ERS amplituthletes, amateur karate athletes, non-athletes), Time (T1, T2, T3) and ROI (BA40, B

The present results confirmed the second working hypothe-is, namely a progressive reduction of cortical activity (alpha ERD)cross non-athletes, amateur karate athletes and elite karate ath-etes along the whole video observation period.

.3. Control analyses

One might argue that the above between-groups differences ofhe alpha ERD can be ascribed to different levels of subjects’ atten-ion, motivation, interest, and habituation. If this is true, subjects ofcertain group would be characterized by a different global sourceower of the baseline alpha rhythms, especially at low frequencies48]. To address this issue, we compared the global source powerf the alpha rhythms among the groups of the elite karate athletes,mateur karate athletes, and non-athletes. The global source poweras defined as the mean of the source power across all voxels of

he sLORETA brain volume (dependent variable). A control ANOVAncluded the factors Group (elite karate athletes, amateur karatethletes, and non-athletes) and Band (low- and high-frequencylpha). The results showed no statistically significant effect includ-ng the factor Group (p > 0.3), indicating that it is improbable thatubjects’ attention, motivation, interest, and habit explain the dif-

erences of alpha ERD of the main experiment.

In the main experiment, only one condition was examined,amely the judgment of karate videos. To demonstrate that theeduced elite athletes’ brain activity as revealed by alpha ERD inhe dorsal and “mirror” pathways is specifically related to their

ig. 5. Across subject means of the low- and high-frequency alpha ERD/ERS amplitude illthletes, amateur karate athletes, non-athletes), Time (T1, T2, T3), and ROI (BA40, BA 6v,

ustrating non-statistical ANOVA interactions among the factors Group (elite karateA 44/45).

favourite discipline, we performed a control experiment aimed atevaluating whether such a reduction is also present when the elitekarate athletes are engaged in judging sport actions that they donot practice. To address this issue, we performed a control experi-ment aimed at testing two hypotheses: (i) the elite karate athletesand control subjects do not provide expert judgments when theyevaluate the performance of athletes of a sport they do not prac-tice such as rhythmic gymnastic; (ii) the elite karate athletes andcontrol subjects do not show differences in the alpha ERD of dorsaland “mirror” pathways during the judgment of the “extraneous”rhythmic gymnastic performance. For this purpose, EEG data wererecorded in 6 elite karate athletes and 7 control subjects (amateursubjects and non-athletes) of the main experiment, namely the onlywho accepted to come back for a new EEG recording. The group ofthe elite karate athletes was formed by 4 women, whereas those ofthe control subjects by 6 women. The mean subjects’ age was 22.3years in the elite karate athletes (±1.4 SE; range: 20–29 years) and19.5 years in the control subjects (±1 SE; range: 18–23 years). Theyobserved a series of 120 rhythmic gymnastic videos. At the end ofeach video, the subjects had to judge the artistic/athletic level of theexercise by a scale from 0 to 10. The mismatch between their judg-ment and that of the coach of Italian team of gymnastics indexed

the correctness of action judgment, similarly to the procedure ofthe main experiment. The EEG data analysis and ANOVAs strictlyfollowed those of the main experiment. The mean IAF value was11 Hz (±0.2 SE) for the elite karate athletes and 10.7 Hz (±0.5 SE)for the control subjects.

ustrating non-statistical ANOVA interactions among the factors Group (elite karateBA 44/45).

472 C. Babiloni et al. / Behavioural Brain

Fig. 6. Across subject means of the low- and high-frequency alpha ERD/ERS ampli-tude illustrating a statistical ANOVA interaction among the factors Group (elitekarate athletes, control subjects), and ROI (BA19, BA 37, BA 20). The asterisks indicatetep

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Another interesting result of the present study is the global

he sLORETA solutions at which alpha ERD presented statistically significant differ-nces with respect to the pattern: elite karate athletes /= control subjects (Duncanost hoc testing, *p < 0.05).

Regarding the hypothesis of an uneducated evaluation of thehythmic gymnastic performance for the elite karate athletes andontrol subjects, the mean judgment error (±SE) was 1.64 (±0.05E) for the elite karate athletes and 1.69 (±0.05 SE) for the controlubjects. A correlation analysis (Spearman test, p < 0.01) betweenhe judgment score of each subject of the two groups and thatf the rhythmic gymnast coach showed no statistically significantffect for any subject (r = −0.06–0.21; p = 0.8–0.1), indicating theoor familiarity of the two groups with the gymnastics.

Regarding the hypothesis of a similar cortical activity in the elitearate athletes and control subjects during the judgment of theextraneous” rhythmic gymnastic performance, the ANOVA of theow-frequency alpha ERD/ERS in the ventral pathway showed a sta-istically significant interaction (F(2,22) = 9.79; p < 0.001) betweenhe factors Group (elite karate athletes, control subjects) and ROIBA 19, BA 37, BA 20; see Fig. 4 top). Duncan post hoc testing indi-ated that the low-frequency alpha ERD was lower in the elitearate athletes than in the control subjects at BA 20 (p < 0.002). Onhe contrary, the low-frequency alpha ERD was higher in the elitearate athletes than in the control subjects at BA 19 (p < 0.02). TheNOVA of the low-frequency alpha ERD/ERS in the dorsal and “mir-or” pathways showed no statistically significant effects (p > 0.1).hese control results suggest that the evaluation of gymnasticideos induced no reduction of brain activity (“neural efficiency”) asevealed by low-frequency alpha ERD in dorsal and “mirror” path-ays in the elite karate athletes compared to the control subjects.

The ANOVA of the high-frequency alpha ERD/ERS in the ventralathway showed a statistically significant interaction (F(2,22) = 7.4;< 0.004) between the factors Group (elite karate athletes, control

ubjects) and ROI (BA 19, BA 37, BA 20; see Fig. 6 bottom). Dun-an post hoc testing indicated that the high-frequency alpha ERDas lower in the elite karate athletes than in the control subjects atA 20 (p < 0.005). On the contrary, the high-frequency alpha ERD

as higher in the elite karate athletes than in the control sub-

ects at BA 19 (p < 0.03). The ANOVA of the high-frequency alphaRD/ERS in the dorsal and “mirror” pathways showed no statis-ically significant effects (p > 0.1). As for the low-frequency alpha

Research 207 (2010) 466–475

ERD, the evaluation of gymnastic videos induced no reduction ofhigh-frequency alpha ERD in the dorsal and “mirror” pathways inthe elite karate athletes compared to the control subjects.

4. Discussion

In line with the “neural efficiency” hypothesis in experts, wetested the hypothesis that compared to non-athletes, elite karateathletes are characterized by a reduced cortical activation (lesspronounced alpha ERD) in dorsal cortical visual pathway andfronto-parietal “mirror” systems during the judgment of observedkarate actions. Furthermore, we predicted a progressive reduc-tion of cortical activation (less pronounced alpha ERD) acrossnon-athletes, amateur karate athletes, and elite karate athletesin visuomotor system. In line with a reference study [27], thejudgment of the observed sporting actions was indexed as thedifference between the judgment by the participants and that ofthe elite athletes’ coach. We chose the elite karate athletes forthree main reasons. In karate, the evaluation of athletes’ perfor-mance is based on a standardized subjective scale used by judges ofkarate competitions (Kata speciality), which is well known by eliteathletes. Furthermore, the high-level performance is intrinsicallybased on a strict coordination and synchronization among ath-letes, which implies an efficient judgment of the observed actions.Finally, the understanding of the karate actions do not impliesobject recognition, so we could predict no “neural efficiency” effectat the level of ventral cortical visual systems in the elite ath-letes.

Concerning the working hypothesis of reduced activity in elitekarate athletes compared to non-athletes during the judgment ofkarate action, we showed that alpha ERD in dorsal (about 8–12 Hz)and “mirror” (about 10–12 Hz) systems was lower in amplitude inthe elite karate athletes than in the non-athletes. This was truealong the whole video observation period. These results suggestthat the judgment of observed karate actions is related to a loweralpha ERD in the elite athletes than in the non-athletes, as a possibleindex of spatially selective cortical activation (“neural efficiency”).Furthermore, it should be remarked that only some areas of corti-cal visuomotor systems reflected “neural efficiency” in the presentexperimental conditions, namely the dorsal and “mirror” pathwaysbut not the ventral pathway. This finding complements previousevidence showing a decrease of alpha ERD (about 8–12 Hz) in eliterhythmic gymnasts compared to non-gymnasts in ventral and dor-sal pathways [27]. The diverse “neural efficiency” effect in theventral pathways between the reference study [27] and the presentone is probably due to the different features of the gymnastic andkarate videos. The understanding of rhythmic gymnastic videosimplies the recognition of rope, hoop, ball, ribbon, and clubs byvisual ventral system [28], whereas this is not the case for theunderstanding of karate videos in which no relevant object hasto be recognized. Of course, this does not mean that understand-ing karate actions does not imply object recognition at all. We justspeculate that the training of elite karate athletes is focused ona skilful rapid processing of visuo-spatial and motor informationduring the karate action rather than on the effective processing ofinformation relative to the shape of face, hands, legs, and wearsof the opponent. It is then presumably that in the elite karate ath-letes, “neural efficiency” mechanisms operate on the brain circuitsmainly sub-serving the processing of visuo-spatial and motor infor-mation.

reduction of the alpha ERD amplitude across the fronto-parietalareas of “mirror” systems in the elite karate subjects. This is proba-bly due to the fact that the “mirror” systems are markedly involvedin the understanding of the karate videos showing elite athletes

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erforming kicks and punches against imaginary opponents. Thisnding in elite athletes extends previous evidence of the activationf “mirror” systems in animals and human non-experts [30–32,58],nd complements previous evidence on the activation of “mirror”ystems in experts [42,36,38,39,59]. A more detailed discussion ofhese findings is provided in the following paragraphs.

The present results lead support to the idea that alpha rhythmsight represent one of the physiological mechanisms at the basis

f “neural efficiency” during the judgment of the observed actions.hese rhythms reflect the functional modes of thalamo-corticalnd cortico-cortical loops that facilitate/inhibit the transmissionnd retrieval of both sensorimotor and cognitive information intohe brain [60–62]. The functional meaning of low- (about 8–10 Hz)nd high-frequency (about 10–12 Hz) alpha rhythms is supposedo be different. On one hand, low-frequency alpha rhythms wouldubserve subject’s global attentive readiness. On the other hand,igh-frequency alpha rhythms would reflect the task-related oscil-

ation of specific neural systems for the elaboration of sensorimotorr semantic information [47–49]. In this sense, the present resultsint that compared to the brain of non-athletes, the brain of elitethletes requires a quite selective engagement of thalamo-corticalnd cortico-cortical loops spanning dorsal and “mirror” pathwaysor a successful judgment of observed karate actions. It can be spec-lated that such modulation of alpha rhythms might support bothlobal attentional (low-frequency alpha rhythms) and task-specifichigh-frequency alpha rhythms) processes [47–49]. This might behe same mechanism at the basis of a well known phenomenonbservable in healthy subjects: the progressive reduction of event-elated cortical activity along learning phases (for a review see42,36]). In this vein, it has been shown that training induces aecrease of activity in motor cortex from pre- to post-training phaseuring motor tasks [20,63,64]. Furthermore, the trained motorasks were performed with a suppression of cognitive processes65].

Concerning the working hypothesis of intermediate corticalctivity in amateur karate athletes compared to elite karate ath-etes and non-athletes during the judgment of karate action, weeport that along the whole video observation period, low- andigh-frequency alpha ERD showed intermediate amplitude in themateur karate athletes with respect to the non-athletes and tohe elite karate athletes in dorsal pathway. These findings aren line with previous evidence showing that action observationnduces long lasting ERD effects during the observation period [66],nd with previous fMRI evidence showing that expert guitaristsere characterized by significantly smaller BOLD signals in “mir-

or” system during the observation of the practiced compared toonpracticed actions [36]. In contrast, the present findings are atdds with previous evidence showing that professional dancersere characterized by an alpha ERD higher in amplitude during

he early phase of the mere recognition of a video with dancing per-ormance [37]. These findings are also at odds with previous fMRIvidence showing (i) greater activation in “mirror” system whenxpert dancers merely recognized movements that they had beenrained to perform compared to movements they had not [38]; (ii)reater activation in premotor, parietal, and cerebellar areas whenancers merely recognized moves from their own motor repertoire,ompared to moves that they frequently saw but did not perform39]; (iii) greater activation in the “mirror” system when dancers

erely recognized dancing movements that were part of the indi-idual’s motor repertoire, compared to observation of nonpracticedovements [40]; and (iv) greater activation in the “mirror” sys-

em when naïve subjects simply watched a musician playing guitarccords [41]. How can the present and previous findings be recon-iled? At this early stage of the research, a definitive explanationannot be provided. A tentative explanation is that in experts, “neu-al efficiency” mechanism is not automatically triggered by the

Research 207 (2010) 466–475 473

mere recognition of trained action. Rather, such a mechanism mightbe triggered by expert operations performed along most part ofthe visual stimuli, in the framework of a technical evaluation ofthe observed performance. Future investigations should systemat-ically test this tentative explanation and evaluate the implicationsof the present finding on the judgment of sporting performance ininternational tournaments.

The present results complement a recent transcranial magneticstimulation study [67] showing that (i) corticospinal excitability ofelite basketball athletes and watcher subjects (basketball coachesor sports journalists) was stronger during the observation of basketshots compared to soccer kicks and static images; (ii) corticospinalexcitability of non-athletes was stronger during the observation ofbasket shots and soccer kicks compared to static images; (iii) onlyelite basketball athletes showed a stronger corticospinal excitabil-ity during the observation of erroneous compared to successfulbasket shots. In line with the mentioned relevant study [67], futureinvestigations should use a group of karate referee and/or coach tocompare the brain activity in subjects who are experts in perform-ing and judging karate exercises with subjects who are not ableto perform the karate exercises but are able to use the judgmentscale (unfortunately, we were not able to recruit all these kinds ofsubjects in this study). Indeed, the present evidence just supportsthe hypothesis of spatially selective cortical activation (“neural effi-ciency”) into human visuomotor systems of elite athletes during thejudgment of the observed actions. It does not clarify whether this“neural efficiency” is due to prolonged motor experience or to aprolonged visual and cognitive experience.

Moreover, the present results complement those showing thatthe amplitude of alpha ERD was lower in amplitude in brighterpeople engaged in cognitive tasks such as stimulus encoding, work-ing memory, and memory retrieval processes [13–16]. In addition,the present results expand previous EEG findings showing thatobservation of movements is associated with alpha ERD over senso-rimotor cortex in healthy subjects [33,34] but not in patients withautism [35].

As a final consideration, we think that the “neural efficiency”hypothesis, which is historically focused on the brain featuresof more intelligent people during the performance of cognitivetasks, reflects one of the neurophysiological mechanisms typicallyexplored in the larger theoretical framework on practice-relatedchanges in brain structure and function. Indeed, previous neu-roimaging studies have described patterns of both practice-relatedincrease and decrease of regional activations as a function of brainreorganization and redistribution of cognitive and sensorimotorprocesses [42]. It can be speculated that these functional mecha-nisms are associated with changes in grey and white matter volumeor in hippocampus as revealed by previous evidence in musicians(see [45,68]), in London taxi-drivers [43], and in non-experts [44].Finally, an open issue is the role of genetic determinants on thementioned structural/functional brain changes in more intelligentpeople and in experts.

In conclusion, the present study showed that that low- andhigh-frequency alpha ERD was less pronounced in the elite karateathletes compared to the non-athletes in the dorsal and fronto-parietal “mirror” pathways. Furthermore, low-frequency alpha ERDshowed a intermediate amplitude in amateur karate with respectto the non-athletes and elite karate athletes in the dorsal pathway.These results globally suggest that the judgment of observed sport-ing actions is related to relatively less pronounced alpha ERD, asa possible index of spatially selective cortical activation or “neu-

ral efficiency”. However, such a “neural efficiency” would occuraccording to a complex topographic and temporal pattern. Futureexperiments should evaluate the hypothesis that in human sub-jects, these patterns of “neural efficiency” are modulated by bothintensive task-specific training and neuro-feed-back of alpha ERD.

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cknowledgements

The research was granted by Sport Medicine School - Univer-ity of Rome Sapienza, Tosinvest Sanità, and Federazione Italianaudo, Lotta, Karate ed Arti Marziali (FIJLKAM). Drs. Francesco Infar-nato, Nicola Marzano, and Marco Iacoboni carried out this researchn the framework of Doctoral School on “Neurophysiology” at theepartment of Physiology and Pharmacology, University of Romeapienza, Italy.

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