Is there neural efficiency in athletes’

brain?
Evidence of neural synchronization and
connectivity
Claudio Babiloni, University of Rome “La Sapienza”; Italy;
Pierluigi Aschieri, FIJLKAM (Italian Federation of Karate, Judo and Martial Arts)
Claudio Del Percio, University of Rome “La Sapienza”; Italy;
Roberta Lizio, University of Rome “La Sapienza”; Italy;
Nicola Marzano, University of Rome “La Sapienza”; Italy;
Mauro Franzetti, University of Rome “La Sapienza”; Italy;
Antonio Fiore, Italian Federation of Fencing
Mirella Pirritano, Institute of Sport Science, CONI, Rome, Italy
Claudio Gallozzi, Institute of Sport Science, CONI, Rome, Italy
Cristina Limatola, University of Rome “La Sapienza”; Italy

claudio.babiloni@uniroma1.it
 Neural efficiency hypothesis
and athletes’ brain activity
NEURAL EFFICIENCY

Subjects with high

intelligent quotient (IQ)
and subjects highly
trained for specific skills
(“experts”) show low-
amplitude alpha ERD Neural efficiency
(low EEG reactivity =
selective cortical activity)
during several cognitive
tasks (Neubauer et al.,
1995; Grabner et a.,
2004; Grabner et al.,
2006)

Is it also true for the brain of

the athletes?
 ELECTROENCEPHALOGRAPHY (EEG)

 non invasive, inexpensive, transportable technique

 high temporal resolution
 recording of event-related cortical activity

Numerous applications in the emergent domains of sport science (Baumeister et al.,

2008; Park et al., 2015; Duvinage et al., 2012)
 STATE OF THE RESEARCH ON EEG AND SPORT:
development of new technologies

 Development of new technologies

Mobile Brain / Body Imaging (MoBi)

Synchronous recording of high-density EEG with body motion capture and eye
gaze tracking, plus other physiological measures, while participants perform
motivated behaviors in three-dimensional environments (Makeig et al.,
2009; Gramann et al., 2010, 2011; Gwin et al., 2010, 2011; reviewed in Cheron et
al. 2016).
 Cortical EEG alpha rhythms
reflect cortical inhibition in
eyes closed resting state
condition
 Dominant resting (eyes-
RESTING closed) alpha rhythms are
EYES synchronous and coherent
over wide cortical areas and
CLOSED corresponding thalamic
nuclei as a sign of
CORTICAL INHIBITION

pyramidal neurons
oscillating at synchronized =All neurons
alpha frequencies (around synchronized at
10 Hz) around 10 Hz
Reticular neurons Relay neurons
BRAIN STEM THALAMUS
Cortical alpha rhythms are
suppressed in amplitude as a
sign of cortical excitation
during sensory stimulation,
cognitive demands,
movements
 Dominant resting (eyes-
RESTING closed) alpha rhythms are
EYES synchronous and coherent
over wide cortical areas and
CLOSED corresponding thalamic
nuclei as a sign of
CORTICAL INHIBITION

pyramidal neurons
oscillating at synchronized =All neurons
alpha frequencies (around synchronized at
10 Hz) around 10 Hz
Reticular neurons Relay neurons
BRAIN STEM THALAMUS
 High-frequency EEG
Event- rhythms (about 30 to 100 Hz
induced or highest) substitute alpha
rhythms during eyes
activation opening. Reduction of alpha
rhythms as a sign of
CORTICAL EXCITATION
Gamma rhythms

pyramidal neurons = synchronous at

oscillating at several around 30 Hz
peculiar high frequencies
(beta2-gamma) = synchronous at
around 40 Hz
Reticular neurons Relay neurons
= synchronous at
BRAIN STEM THALAMUS around 100 Hz
 EVENT RELATED DESYNCHRONIZATION/SYNCHRONIZATION
(ERD/ERS): AN INDEX OF CORTICAL ACTIVITY
Compared to a rest period (baseline) several kind of events (movements, sensorial
stimuli, cognitive tasks etc…) can induce an amplitude decrease/increase (ERD/ERS) of
cortical activity in specific frequency bands (expecially alpha 8-12 Hz).

Decrease of power Increase of power

 STATE OF THE RESEARCH ON EEG AND SPORT:
identification of EEG biomarkers

 Identification of EEG biomarkers

Navigation Motor binding Global resting state Sensorimotor task Memory

Eye-head – Sensorimotor Selective attention Perception binding consolidation
body movement association Cognitive performance Attention (sleep, slow-wave
Episodic memory Sensory Inhibition and gating
Working and activity)
Sensorimotor discrimination Consolidation of associative memory Facilitation of
Fatigue new motor sequence
integration (sleep-spindle) multiple unit
Goal setting Autonomous activity
Network nervous
system Visual
coordination
Motor control regulation discrimination
Emotion Motor imagery
Dream recall

Cheron et al., 2016

 Neural efficiency hypothesis
and athletes’ brain activity
Resting state alpha rhythms
reflect more background
cortical inhibition in athletes
than in controls
More resting state alpha power in elite athletes than in amateur athletes and non-
athletes: athletes’ brain is more inhibited in the background resting state
condition

Resting EEG data:

16 Elite athletes
20 Amateur
athletes
25 non-athletes

Babiloni C, Marzano N, Iacoboni M, Infarinato F, Aschieri P, Buffo P, Cibelli G, Soricelli A, Eusebi F, Del Percio C. Resting state
cortical rhythms in athletes: a high-resolution EEG study. Brain Res Bull. 2010 Jan 15;81(1):149-56.
Less reactivity of alpha power to eyes opening in elite athletes than in amateur
karate athletes and non-athletes: athletes’ brain is less excited during eyes
opening (does it reflect selectivity/efficiency of cortical activation?)

Resting EEG data:

18 Elite karate athletes
28 Amateur karate
athletes

Del Percio C, Infarinato F, Marzano N, Iacoboni M, Aschieri P, Lizio R, Soricelli A, Limatola C, Rossini PM, Babiloni C. Reactivity of
alpha rhythms to eyes opening is lower in athletes than non-athletes: a high-resolution EEG study. Int J Psychophysiol. 2011
Dec;82(3):240-7.
Alpha rhythms are less
suppressed during difficult
upright standing (more
control, selectivity, and
efficiency?) in athletes than in
controls
Alpha rhythms related to visuo-vestibular-motor integration for
upright standing enhanced in elite fencers?

Del Percio C, Babiloni C, Marzano N, Infarinato F, Vecchio F, Lizio R, Aschieri P, Fiore A, Toràn G, Gallamini M, Baratto M,
Eusebi F “NEURAL EFFICIENCY” OF ATHLETES’BRAIN FOR UPRIGHT STANDING: A HIGH-RESOLUTION EEG
STUDY Brain Res Bull. 2009 May; 79(3-4):193-200

VIDEO
Alpha ERD was lower in
amplitude in karate and fencing
athletes than in non-athletes at
central and parietal areas,
during monopodalic referenced
to less engaging bipodalic
condition (neural efficiency)

Del Percio C, Babiloni C, Marzano N, Infarinato F, Vecchio F, Lizio R, Aschieri P, Fiore A, Toràn G, Gallamini M,
Baratto M, Eusebi F “NEURAL EFFICIENCY” OF ATHLETES’BRAIN FOR UPRIGHT STANDING: A HIGH-
RESOLUTION EEG STUDY Brain Res Bull. 2009 May; 79(3-4):193-200
Alpha rhythms are less
suppressed during voluntary
hand movements (more
control, selectivity, and
efficiency?) in athletes than in
controls
Compared to the non-athletes, the elite karate athletes showed a
lower central alpha ERD only for the right movement, as a
possible index of spatially selective cortical activation (neural
efficiency)

Claudio Del Percio, Claudio Babiloni, Francesco Infarinato, Nicola Marzano, Marco Iacoboni, Pierluigi Aschieri,
Fabrizio Eusebi: Neural efficiency" of athletes' brain for voluntary movements: a high resolution EEG study
Neuroimage 2010
Alpha rhythms are less
suppressed during voluntary
(endogenous) visuospatial
attention (more control,
selectivity, and efficiency?) in
athletes than in controls
 Cortical EEG activation during focused attention in elite pistol
shooters. More efficiency?

Del Percio C, Babiloni C, Bertollo M, Marzano N, Iacoboni M, Infarinato F, Lizio R, Stocchi M, Robazza C, Cibelli G,
Comani S and Eusebi F. Visuo-attentional and sensorimotor alpha rhythms are related to visuo-motor performance in athletes
Hum Brain Mapp. 2009
VIDEO
 Postural freezing of elite shooters is related to selectivity/neural
efficiency as revealed by widespread cortical EEG deactivation: a
“disconnection” from irrelevant stimuli of the external world?
More efficiency

Del Percio C, Babiloni C, Bertollo M, Marzano N, Iacoboni M, Infarinato F, Lizio R, Stocchi M, Robazza C, Cibelli G,
Comani S and Eusebi F. Visuo-attentional and sensorimotor alpha rhythms are related to visuo-motor performance in athletes
Hum Brain Mapp. 2009
 The elite athletes showed high-frequency alpha ERS (about 10-12 Hz)
larger in amplitude for high score shots (50%) than for low score shots; this
was true in right parietal and left central areas

Del Percio C, Babiloni C, Bertollo M, Marzano N, Iacoboni M, Infarinato F, Lizio R, Stocchi M, Robazza C, Cibelli G,
Comani S and Eusebi F. Visuo-attentional and sensorimotor alpha rhythms are related to visuo-motor performance in athletes
Hum Brain Mapp. 2009
Linear temporal synchronization (coherence) of EEG rhythms at
electrode pairs as an index of functional cortico-cortical coupling
(information transfer)

brain
frontal EEG frontal
high spectral coherence
electrodes max coh = 1
= high information transfer
parietal EEG

parietal
linear coupling
 Compared to non-athletes, pistol shooters show stronger parieto-
temporal and parieto-occipital alpha coherence

high cortical coherence

Del Percio C, Babiloni C, Bertollo M, Marzano N, Iacoboni M, Infarinato F, Lizio R, Stocchi M, Robazza C, Cibelli G,
Comani S and Eusebi F. Visuo-attentional and sensorimotor alpha rhythms are related to visuo-motor performance in
athletes Hum Brain Mapp. 2009
Alpha rhythms in athletes are
less suppressed during
understanding of expert
actions (more control,
selectivity, and efficiency?)
Efficiency of mirror neuron systems as revealed by mapping of
alpha rhythms

Babiloni C, Del Percio C, Rossini PM, Marzano N, Iacoboni M, Infarinato F, Lizio R, Piazza M, Pirritano M, Berlutti G, Cibelli G,
Eusebi F. Judgment of actions in experts: a high-resolution EEG study in elite athletes. Neuroimage. 2009 Apr 1;45(2):512-21.

VIDEO
 Understanding of the sporting performance by other athletes is
related to selectivity/neural efficiency of parietal cortical
activation (mirror systems) as revealed by EEG mapping. More
efficiency?

Babiloni C, Del Percio C, Rossini PM, Marzano N, Iacoboni M, Infarinato F, Lizio R, Piazza M, Pirritano M, Berlutti G, Cibelli G,
Eusebi F. Judgment of actions in experts: a high-resolution EEG study in elite athletes. Neuroimage. 2009 Apr 1;45(2):512-21.
Low- (about 8–10 Hz) and high-frequency (about 10–12 Hz) alpha
rhythms were lower in amplitude in the elite karate athletes compared
to the non-gymnasts in occipital and temporal areas (ventral pathway)
and in dorsal pathway (neural efficiency)

Babiloni C, Del Percio C, Rossini PM, Marzano N, Iacoboni M, Infarinato F, Lizio R, Piazza M, Pirritano M, Berlutti G,
Cibelli G, Eusebi F. Judgment of actions in elite amateur katate athletes a: a high-resolution EEG study. Behavioral
Brain Research. 2010
 Neural efficiency hypothesis
does not explain athletes’
brain activity in some
conditions
Eyes opening alpha rhythms in
athletes during upright
standing does not fit neural
efficiency hypothesis
 Alpha ERD was stronger in
amplitude in karate and fencing
athletes than in non-athletes
during quiet upright standing at
eyes open reference to eyes
closed condition, , (against
neural efficiency)

Del Percio C, Brancucci A, Bergami F, Marzano N, Fiore A, Di Ciolo E, Aschieri P, Andrea Lino A, Vecchio F, Iacoboni M,
Gallamini M, Babiloni C, Eusebi F. Cortical alpha rhythms are correlated with body sway during quiet open-eyes standing
in athletes: a high-resolution EEG study. Neuroimage 2007, 36(3):822-9.
Alpha rhythms in athletes
during complex visuomotor
integration doe not fit neural
efficiency hypothesis
Successful putts of elite golfers is related to alpha EEG rhythms

Claudio Babiloni, Claudio Del Percio, Francesco Infarinato, Nicola Marzano, Marco Iacoboni, Pierluigi Aschieri,
Fabrizio Eusebi: Sensorimotor rhythms related to precise golf putts: a high resolution EEG study Journal of
Physiology, 2009

VIDEO
 Successful putts of elite golfers is related to strong integrative
frontal executive processes

Claudio Babiloni, Claudio Del Percio, Francesco Infarinato, Nicola Marzano, Marco Iacoboni, Pierluigi Aschieri,
Fabrizio Eusebi: Sensorimotor rhythms related to precise golf putts: a high resolution EEG study Journal of
Physiology, 2009
 Successful putts of elite golfers is related to strong parieto-
central and parieto-frontal alpha coherence

high cortical coherence

Babiloni C, Infarinato F, Marzano N, Iacoboni M, Dassù F, Soricelli A, Rossini PM, Limatola C, Del Percio C. Int J Psychophysiol.
2011 Dec;82(3):260-8. Intra-hemispheric functional coupling of alpha rhythms is related to golfer's performance: a
coherence EEG study.
Alpha rhythms are sensitive to
the intervention on visuomotor
integration in athletes
Does conditioning of pre-stimulus alpha rhythms enhance the
cognitive-motor performance in fencers?

VIDEO
CORRELATION BETWEEN PRE-STIMULUS ALPHA RHYTHMS AND
REACTION TIME: the higher the enhancement of pre-stimulus alpha rhythms,
faster the reaction time in all subjects

14 elite fencers, 8 karate and 14 non-athletes

Del Percio C, Marzano N, Tilgher S, Fiore A, Di Ciolo E, Aschieri P, Lino A, Toràn G, Babiloni C, Eusebi F. Pre-stimulus alpha rhythms are correlated
with post-stimulus sensorimotor performance in athletes and non-athletes: a high-resolution EEG study. Clin Neurophysiol. 2007
Aug;118(8):1711-20.
 Cognitive functions in football players

Football requires complex cognitive skills:

 MOTOR LEARNING
Localization of :
 MOTION PREDICTION
 Ball

 VISUOSPATIAL ABILITY  Team-mates

 Opponents
 SIMULTANEOUS OPERATIONS
 Goal

(Abernethy et al, 1993; Starkes and Allord, 1993; Williams et al, 1999; Roca et al., 2011)
Neural hyper-activity related to visuo-spatial
processing in rugby players

LIMIT: no control (non-spatial)

condition to address specificity

(Sekiguchi et al, 2013)

 Aim of the study

 Develop videos of football scenes to be

used to assess neural correlates of
visuospatial information processing and
decision making in football players
Investigate whether football players show
neural hyper-activity in the visuo-spatial
information processing in football scenes
(with adequate non-spatial control condition
in the experimental design)
 Subjects
13 expert football players (experimental group; mean age: 25.1 years; 13
male), practicing football for more than 12 years at least five times a week. They
also have been regularly competing in national tournaments.

 8 no-athletes (control group; mean age: 25.6 years; 8 male). They had never
practiced any sports at agonistic level.

Experimental design
70 videos with football scenes two times: one time in the called “Football”
(SPATIAL DEMAND) and 70 for the condition called “Control” >(NON-SPATIAL
DEMAND). Order randomized across subjects.
Football
Control
 Videos of football scenes

 Story board of football scenes representing paradigmatic attack and defense

actions performed by two team-mates and two opponents, discussed and agreed
with two expert football trainers (Italian “Serie A”).
 Development of high-resolution videos with expert football players as actors.
Approval of the videos by expert football trainers (Italian “Serie A”) and players.
 EEG recordings

 EEG data were

continuously recorded from
56 scalp electrodes (cap)
positioned over the whole
scalp according to a 10-10
system.
EOG to monitor eyes
movements and blinking.
 EEG power density and ERD/ERS analyses

Two event periods: T1 as the period from+0.5 s to +1.5 s with respect to the
zerotime, T2 as the period from +1.5 s to +2.5 s. The pre-stimulus period was
defined as the period from −1 s to the zerotime.

Zerotime: onset of the video stimulus

 EEG power density and ERD/ERS analyses

 Power spectrum analysis of the artifact-free

EEG data was based on FFT approach.
Individual alpha frequency (IAF) peak defined
as the frequency within the 6–13 Hz range of
the EEG spectrum showing the maximum
power. With reference to the IAF, the alpha sub-
bands of interest were as follows: low
frequency alpha band as IAF−2 Hz to IAF,
and high-frequency alpha band as IAF to
IAF+2 Hz

 ERD index of the cortical activity - ERS index of the cortical inhibition

 ERD-ERS was defined as the percentage decrement/increment of instant power

density at the event period compared to a pre-stimulus.
 Behavioral responses

Football Condition

Football players Control subjects

T-Test*
(N=13) (N=8)

Accuracy (%) 94.6 (±1.9 SE) 94.4 (±1.9 SE) n.s.

Reaction time (ms) 496 (±33SE) 594 (±90 SE) n.s.

Control Condition

Football players Control subjects

T-Test
(N=13) (N=8)

Accuracy (%) 93.9 (±1.8 SE) 96.2 (±0.9SE) n.s.

Reaction time (ms) 441 (±32 SE) 505 (±88 SE) n.s.

*T-Test: p<0.05
 Alpha ERD-ERS
Low-frequency alpha (about 8-10 Hz)

Football condition Control condition

T1 T2 T1 T2
Football Players

ERS(%)
No Football Players

ERD(%)
 Alpha ERD-ERS

High-frequency alpha (about 10-12 Hz)

Football condition Control condition

T1 T2 T1 T2
Football Players

ERS(%)
No Football Players

ERD(%)
 ANOVA statistical results

= Football players ≠ Control subjects(p<0.05)

 In football condition, there was an increase of alpha ERD (i.e. cortical excitation) in
left parietal (P3) and in right central-parietal (C4, P4) electrodes in football players
compared to control subjects.
In control condition, no difference of alpha ERD was found between the two groups.
 FUTURE PERSPECTIVES: COGNITIVE TRAINING IN THE DOMAIN OF
SPORT SCIENCE
EEG Performance
EEG Performance Cognitive training (one month)
recording assessment
recording assessment
(real condition)
(real condition)

┼ ┼

Is cognitive training able to

improve athletes’ performances
and modulate EEG brain rythms?
FUTURE PERSPECTIVES: COGNITIVE TRAINING IN CLINICAL PRACTICE

Investigate brain activity of athletes helps to clarify cerebral mechanisms of

damaged and aged brains.

Is cognitive training able to recover cognitive and

motor performance and modulate EEG brain rythms
in subjects with neurodegenerative disorders
(Alzheimer’s disease, Parkinson’s disease etc…)?
Conclusions (I)

Athletes’ brain is characterized by higher power of eyes closed resting state alpha sources
and lower reactivity to eyes opening, in line with neural efficiency hypothesis

Alpha rhythms in athletes are modulated in relevant cortical networks by task demands
(difficult upright standing, voluntary hand movements, complex visuo-motor integration,
voluntary visuo-spatial attention, etc.)

Athletes’ brain is characterized by neural efficiency in most experimental conditions but not
in all, according to the idea of neural adaptability

Physical and neurocognitive exercise may enhance neural efficiency in developmental age
and across aging. New information and communication technologies may contribute to
provide services in this field

Cognitive-motor
performance

Cortical pyramidal populations

Conclusions (II)

Videos of football scenes were developed and validated for the present experiments
and for future applications

Parieto-occipital cerebral cortex (“where” dorsal pathway) of football players is

activated in line with neural hyper-activity theory in the processing of visuo-spatial
information in football scenes (complex and variable visuo-spatial condition).

The present spatial condition is able to elicit specific cortical activity (as revealed by
EEG markers) in football players and will be used as a neural target of brain visuo-
spatial training in this population for applied neurophysiology (ancillary experimental
activities in progress).

Cognitive-motor
performance

Cortical pyramidal populations

Some heroes of
High resolution EEG lab

View of the Department of Physiology

and Pharmacology, University of Rome
«La Sapienza»

From left: Ana Bujan (Ph.D.), Susanna Lopez

(Ph.D. fellowship), Nicola Marzano (Ph.D.),
Susanna Cordone (Ph.D.), Giuseppe Noce
(Ph.D. fellowship), Claudio Del Percio (Ph.D.),
and Roberta Lizio (Ph.D.). Not illustrated:
Filippo Carducci (Ph.D.) and Giulia Santi
(Eng).

Ivano Triggiani (Ph.D.),

University of Foggia (Italy)