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NEUROSCIENCE

RESEARCH ARTICLE
Davide Crivelli et al. / Neuroscience 412 (2019) 83–93

Neurocognitive Enhancement Effects of Combined Mindfulness–


Neurofeedback Training in Sport
Davide Crivelli,ab* Giulia Frondaab and Michela Balconi ab
a
Research Unit in Affective and Social Neuroscience, Catholic University of the Sacred Heart, Largo A. Gemelli 1, 20123, Milano, Italy
b
Department of Psychology, Catholic University of the Sacred Heart, Largo A. Gemelli 1, 20123, Milano, Italy

Abstract—To foster performance across all levels of sports practice, physical training has been integrated with various
mental training practices. Recently, an integrative approach to neurocognitive enhancement tried to combine the
strengths of mental practices (i.e. mindfulness) and of training with neurofeedback devices. Based on previous validation
studies showing the effect of a combined mindfulness–neurofeedback program on neurocognitive efficiency and stress/
anxiety levels, we aimed at testing the feasibility and potential of that intensive combined program for improving psycho-
logical well-being and attention regulation in sport contexts. 50 participants (sportspeople and volunteers not regularly
involved in sports) were divided into groups undergoing experimental and active control training programs. The experi-
mental one was based on breathing-awareness practices supported by a wearable neurofeedback, while the active con-
trol one included only breathing practices. Before and after training participants underwent standardized
neuropsychological and electrophysiological assessment. Data analysis highlighted a significant reduction of response
times and false alarms at computerized cognitive tasks in sportspeople who completed the training, as well as a consis-
tent improvement of the N2 event-related potential — a marker of attention regulation processes. We have also observed
a general reduction of perceived stress and increased ability to keep a non-evaluative stance. Findings extend available
observations on cognitive and neural effects of combined mindfulness–neurofeedback practice by showing that it is pos-
sible to observe training effects even after a limited period of practice among sportspeople. Such early training effects
might mirror optimized implicit learning curves due to peculiar sensitivity to bodily signals and awareness. © 2019 IBRO.
Published by Elsevier Ltd. All rights reserved.

Key words: neuroenhancement, sport, mindfulness, neurofeedback, wearable devices, self-regulation.

INTRODUCTION acceptance and self-control (Gardner and Moore, 2004,


Both amateur and professional sport activities demand prac- 2007). The possibility for athletes to improve performances
ticers' efforts and commitment and may exert pressure on and to enter optimized mindsets during training and competi-
performance and challenges (Gustafsson et al., 2011; Arnold tion is, indeed, known to be critically influenced by various
and Fletcher, 2012; Sarkar and Fletcher, 2014). In order to factors such as clarity in goal setting, mental focus and
relaxation, intrinsic motivation, and positive thinking (Jackson
foster performance and to achieve optimal results across all
levels of sports practice, physical exercise and training of ath- et al., 2001). Considering such influence of internal feelings
letic gestures are nowadays commonly integrated with var- on performance success, self-awareness – one of the core
ious mental training, coaching and ‘psyching-up’ practices targets of mental training and, in particular, mindfulness med-
(Williams and Straub, 2010; Macnamara et al., 2016; Bisio itation – has become a specific strategy to increase focus
and Bove, 2019; Balconi et al., 2019c). Specifically, the atten- and performance within sport contexts.
tion of recent mental training approaches aimed at promoting Recent studies have shown that an increase of self-aware-
optimal performance has increasingly focused on internal ness is associated with decreased of burn-out levels in ath-
processes, emotions and bodily sensations awareness, letes, greater ability to manage stress, and lower risk of
exhaustion, as well as greater self-regulation, better self-
and context-monitoring, and positive self-talk (Gardner and
Moore, 2007; Kee and Wang, 2008; Bernier et al., 2009; Bir-
*Corresponding author at: Research Unit in Affective and Social
Neuroscience, Department of Psychology, Catholic University of the
rer et al., 2012; Walker, 2013). In addition, trained self-aware-
Sacred Heart, Largo A. Gemelli 1, 20123, Milano, Italy. ness and self-regulation skills have been associated with
E-mail address: davide.crivelli@unicatt.it (Davide Crivelli). greater ability to enter a flow state and benefit from such
https://doi.org/10.1016/j.neuroscience.2019.05.066
0306-4522/© 2019 IBRO. Published by Elsevier Ltd. All rights reserved.

83
84 Davide Crivelli et al. / Neuroscience 412 (2019) 83–93

peculiar optimized experience (Kee and Wang, 2008; Bernier of neurocognitive efficiency (i.e. reduced response times
et al., 2009; Kaufman et al., 2009). Finally, attention regula- under stressful conditions and optimized allocation of
tion skills and the capability to focus on athletic performance attention resources on target stimuli), as well as improved
during competition despite personal or contextual distracters subjective reports and objective markers (i.e. vagal tone
are known to increase even athletes' chance of achieving as measured by heart rate variability) of stress, anxiety
career success in sports (Thelwell et al., 2010). Given the and mental energy (Balconi et al., 2019a; Crivelli et al.,
benefits that better self-regulation and self-awareness may 2019a; Balconi et al., 2019b).
entail in achieving optimal sports performance, several pro- Extended testing of potential outcomes of integrated pro-
grams for different categories of athletes and degree of com- grams like the above-described one, even if not yet
mitment in sport activity have been developed to try and focused on implications for athletic performance, has actu-
improve performance (Gardner and Moore, 2004; Bernier et ally allowed to overcome some of the limitations observed
al., 2009). in investigations of the potential of more traditional training
Some techniques and methods have been based mainly protocols. Namely, notwithstanding the quantity of empiri-
on making sport practicers learn psychological strategies to cal reports suggesting that mental training by itself can
modify the quality of their inner experience (Birrer and Mor- be a valuable tool for enhancement of athletic perfor-
gan, 2010; Kudlackova et al., 2013). Other approaches, on mances and for promoting well-being, it should be
the contrary, work on basic but fundamental skills that acknowledged that the vast majority of such reports take
enhance athletic performance and profile, such as focusing into account behavioral or self-report outcome measures
attention on the goal while avoiding irrelevant activities alone, thus neglecting objective physiological markers of
(Locke and Latham, 2002). In particular, growing evidence the efficiency of attention control and regulation. By taking
on the outcomes provided by mindfulness-based trainings into account the ample literature on physiological and
has led to the development of specific protocols that sustain neural correlates of mindfulness practice, not strictly
self-regulation and attention control by training open-monitor- related to its application with sportspeople, it is instead
ing and focused attention skills, non-reactive emotion-regula- generally and consistently suggested that such form of
tion, and present awareness (Birrer et al., 2012; Pineau et al., mental training could be associated with significant modu-
2014). Similarly, the ability to enter focused and relaxed lation of physiological markers of neurocognitive effi-
mindsets even under stress, to manage automatic affective ciency. Indeed, positive effects of meditation practice –
and physiological reactions, and to adaptively regulate and mindfulness, in particular – have been reported with regard
reorient attention resources on task goals while actively inhi- to spectral and time-domain electrophysiological corre-
biting distracting stimuli has been targeted by different neuro- lates of optimized regulation of attention resources (Cahn
feedback programs (Mirifar et al., 2017; Balconi et al., 2019c). and Polich, 2006; Lutz et al., 2008; Tang et al., 2015).
Neurofeedback, as applied psychophysiology technique, Namely, the modulation of early endogenous event-related
aims at improving awareness of central physiological corre- potentials associated with mindfulness meditation (N2 and
lates of inner experiences and at training adaptive regulation P3; Lutz et al., 2008; Moore et al., 2012; Malinowski et al.,
of such correlates and of related mindsets. Depending on 2017) may mark the progressive modulation of attention
specific needs of different sport specializations, different neu- resources during practice and an increase in neural efficiency
rofeedback-based training programs have been devised and and optimization of attention orienting processes. The N2
tested as empowerment tools for athletes — e.g. programs marker – an early anteriorly-distributed electrophysiological
devoted to enhance mental focus and concentration by mod- component – in particular is considered a valuable tool to
ulating sensorimotor rhythm (SMR) and programs devoted to assess the effects of meditation practice on attention and
train the ability to relax and decrease arousal and perfor- executive control mechanisms, since it has been associated
mance anxiety by modulating alpha and theta EEG bands with detection of attended stimuli, behavior inhibition and sti-
(Mirifar et al., 2017; Balconi et al., 2019c). Nonetheless, it is muli–response monitoring (Folstein and Van Petten, 2008).
worth noting that available empirical reports concerning neu- Interestingly, the N2 component is also among the few elec-
rofeedback-based programs to improve performance in trophysiological markers of cognitive processes that was
sports – though hinting at potentially interesting implications reported to be modulated by aerobic fitness and prolonged
for practice – still often present methodological inconsisten- training in sports. Indeed, for example, it was shown that both
cies, with partly contrasting results. professional athletes (Taddei et al., 2012; Bianco et al., 2017)
More recently, an integrative approach to neurocognitive and people with high levels of physical activity (Winneke et
enhancement tried to combine the strengths of traditional al., 2012) present enhanced N2 deflections during cognitive
mental training techniques and of training with neurofeed- tasks, which have been deemed as an evidence of optimized
back devices. Reports of validation studies of such inte- allocation of attention resources and improved inhibitory
grated approach with a wide range of meditation-naïf processes.
participants showed that carrying out mindfulness-based In addition it is worth underlining that, since traditional
practices (i.e. breathing awareness exercises) with the mindfulness-based protocols applied to sports consis-
support of a neurofeedback device able to provide real- tently drew from available models and protocols devel-
time feedbacks on physiological changes accompanying oped in clinical practice, they have been also typically
practice and to signal the occurrence of mind-wandering structured as long-term programs that include weekly 2-
can lead to improved behavioral and physiological markers to 3-h sessions guided by the trainer (in group or
Davide Crivelli et al. / Neuroscience 412 (2019) 83–93 85

individual) as well as quite demanding daily individual EXPERIMENTAL PROCEDURES


practice (e.g. Gardner and Moore, 2007; Kaufman et al.,
Participants
2009). Besides valuable evidence on the efficacy of such
long-term programs in terms of both athletes' wellbeing and 50 subjects – 15 sportspeople who regularly train in sports
performance, the commitment they require may act as a dis- and practice physical activity and 35 young adults not regu-
couraging factor for beginners and semi-professional sports- larly involved in sports or physical activity – took part in the
people, as well as for smaller teams and sporting clubs study. The inclusion criterion to be classified as sportsmen/
having access to sparse budget. It has been proposed that sportswomen was to dedicate at least 12 h a week to indivi-
integrating mindfulness-based practices with neurofeed- dual or group sessions of physical training or sports practice.
back/biofeedback devices able to support mental training by Participants in the sportspeople group were regularly practi-
providing real-time information on the modulation of bodily cing football (N = 7), basketball (N = 4), volleyball (N = 2),
correlates of practice may help to optimize the training and or martial arts (N = 2). All of them have trained for at least
to reduce time requirements (Balconi et al., 2017; Sliwinski 10 years, though none of them has become a professional
et al., 2017). athlete or profit from practicing sports. Table 1 summarizes
Following previous proof-of-concept and testing in experi- demographic details for each group and for the whole sam-
mental and applied settings (Balconi et al., 2017, 2019a; Bal- ple. History of psychiatric or neurological diseases, presence
coni and Crivelli, 2019a; Crivelli et al., 2019a; Crivelli et al., of cognitive deficits, ongoing concurrent therapies based on
2019b), the present study was therefore designed to test psychoactive drugs that could have altered central nervous
the feasibility and potential for improving psychological well- system functioning, clinically relevant stress level, and occur-
being and for enhancing attention regulation in applied sport rence of significant stressful life events during the last
contexts of a novel mental training protocol combining mind- 6 months were all reasons for exclusion from recruitment. In
fulness-based practice with a supporting neurofeedback particular, participants’ cognitive profile was screened for clin-
device. In particular, training effects have been investigated ical or subclinical signs of deficit based on a brief standar-
by comparing psychometric, cognitive and electrophysiologi- dized neuropsychological assessment battery including
cal measures collected before and after the training period tests tapping on attention, executive functions and cognitive
across sportspeople undergoing the combined mindful- control, and short-term memory skills (Spinnler and Tognoni,
ness–neurofeedback training, a group of non-athletic partici- 1987; Caffarra et al., 2002). At the same time, absence of
pants undergoing the same training program and an clinically-relevant signs of stress, anxiety or depression was
additional active control group. We expected that participants checked, respectively via the Perceived Stress Scale (PSS)
who would have completed the mindfulness–neurofeedback (Cohen et al., 1983), the trait subscale of the State/Trait Anxi-
program would have showed improved psychometric, beha- ety Inventory (STAI-trait) (Pedrabissi and Santinello, 1989),
vioral, and physiological markers of attention control, as mir- and the Beck Depression Inventory (BDI) (Ghisi et al.,
rored by: (i) greater performance outcomes at challenging 2006). All participants had normal hearing and normal or cor-
computerized tasks tapping on attention and executive con- rected-to-normal vision. After recruitment, non-athletic partici-
trol skills; and (ii) the enhancement of electrophysiological pants have been randomly divided into an active control
markers of cognitive control and automatic attention orienta- (N = 18) and an experimental (N = 17) group to be com-
tion — namely, the N2 event-related potential, which is pared with the experimental group of sportspeople. Differ-
thought to mirror the allocation of attention resources towards ences between such groups in terms of age, level of stress,
relevant stimuli. In addition, based on available pieces of evi- trait anxiety, and signs of depression have been checked
dence on the effect of mindfulness-based protocols on sub- via statistics and excluded. One of the sportsmen had to be
jective perception of well-being and at the light of empirical excluded from data analysis due to technical problems during
observations from previous studies implementing the pro- recordings.
gram, we also expected that participants who would have The study has been designed following the principles of the
completed the mindfulness–neurofeedback program would Declaration of Helsinki. Procedures and methods were
have showed reduced subjectively-perceived levels of approved by the Ethics Committee of the Department of Psy-
distress. chology of the Catholic University of the Sacred Heart.

Table 1. Demographic and psychometric data for subgroups and for the whole sample. Means, standard deviations, and significance of between-group sta-
tistical comparisons.

Athletic participants Non-athletic participants Total sample Sig.


Mean (SD) Mean (SD) Mean (SD)
Age 22.00 (2.83) 23.21 (1.85) 22.94 (2.22) n.s.
PSS-10 15.43 (5.08) 17.80 (3.62) 17.12 (4.17) n.s.
STAI-trait 34.64 (6.48) 38.64 (5.94) 37.20 (6.24) n.s.
BDI 4.43 (2.90) 5.74 (3.14) 5.37 (3.10) n.s.
n.s.: not significant.
86 Davide Crivelli et al. / Neuroscience 412 (2019) 83–93

Written informed consent to participate in the study was agitated and distracted mindset is mirrored by the progres-
obtained from all participants. sive increase of the intensity of wind and rainstorm sounds.
The control training protocol had the same overall structure
and amount of commitment of the experimental one, in that
Procedure
even control participants were asked to perform daily ses-
In order to assess potential effects of the combined mindful- sions of breathing practices. Nonetheless, differently from
ness–neurofeedback training program in sports with regard participants in the experimental groups, they completed such
to levels of stress and anxiety, bodily- and self-awareness, practices without the neurofeedback device, while listening to
and behavioral and physiological markers of attention regula- audio tracks with natural sounds that did not adapt to the
tion, we devised a three-branch pre–post experiment study modulation of practicers' EEG activity and that, therefore,
comparing three groups of participants before and at the could not provide them with real-time feedbacks on their
end of a training period. The three groups were constituted focused/inattentive mindsets. The use of such audio tracks
by: people who regularly train in sports and physical activity, was included to make acoustic sensory experience during
undergoing the combined mindfulness–neurofeedback train- practice similar between the groups.
ing program (Experimental Athletic group; EA); people not Both the experimental and the active control protocols
regularly involved in sports or physical activity, undergoing included daily sessions of individual practice for 2 consecu-
the combined mindfulness–neurofeedback program (Experi- tive weeks (total number of sessions: 14). The duration of
mental Non-Athletic group; ENA); people not regularly daily practices was gradually incremented starting from
involved in sports or physical activity, undergoing an alterna- 10 min a day till 20 min a day (first to fifth session: 10 min;
tive control program (Active Control group; AC). sixth to 10th session: 15 min; 11th to 14th session: 20 min),
As for the assessment of participants' information-proces- to introduce progressively increasing levels of commitment
sing efficiency and of their executive control abilities, we and challenge. Daily practices were to be performed at home,
opted for challenging computerized tasks tapping on atten- since we wanted to keep them as independent as possible
tion, monitoring and behavioral inhibition skills instead of tra- from other contextual factors and, for sportspeople, from daily
ditional paper-and-pencil tests to possibly record even fine- workout activities. Nonetheless, in order to grant homogene-
grained training-induced modulation. Besides such beha- ity and comparability of the training across participants, dur-
vioral measures of performance and psychometric outcomes ing the first session of the protocol participants individually
measures, we also collected electrophysiological markers of met an expert who introduced and guided them through the
automatic attention regulation processes during a challen- breathing awareness practice. Participants included in the
ging cognitive task. experimental groups were also introduced to the use of the
As for the mental training program, the practices that have wearable neurofeedback device, to the rewarding vs. punish-
been included in the experimental protocol derive from the ment connotation of the acoustic feedbacks provided by the
Vipaśyanā and mindfulness meditation tradition. In particular, device, and to the way they could use such feedbacks to
participants completed breathing awareness sessions, which guide their mental training.
are a form of focused attention meditation (FAM) practice In addition, participants were asked to systematically plan
where the practicer is asked to orient his/her attention focus practice sessions at the same time of the day to control for
on breathing and related physical sensations (e.g. interocep- potential influence of the physiological modulation of cogni-
tive and temperature changes accompanying the flow of air tive and bodily processes due to circadian rhythms. Further-
though the nose and the throat). FAM practices proved to more, participants in the sportspeople group were asked to
be able to foster concentration, focusing, and self-regulation plan the neurofeedback-guided mental training sessions
skills (Lutz et al., 2008; Lippelt et al., 2014; Hommel and Col- away from workout and physical training sessions to keep
zato, 2017). the combined neurofeedback–mindfulness program as inde-
A peculiar aspect of the tested experimental protocol, how- pendent as possible from their sport-related practices and to
ever, is that such mental training practices were supported by prevent potential biases due to uncontrolled systematic inte-
a dedicated wearable neurofeedback device (Muse™ head- gration of the mental and physical training. All participants
band, InteraXon Inc., Toronto, ON, Canada). By using five fully completed the protocol.
dry electrodes (three of them, including the reference sensor,
placed in correspondence to the forehead and the other two
Psychometric outcome measures
placed in correspondence to the ears), the wearable neuro-
feedback non-invasively collects practicer's EEG activity As for psychometric outcome measures, potential changes
and transfers it via Bluetooth to a smartphone app, which in perceived levels of stress, anxiety and bodily-/self-awareness
turn uses such source of information to deliver real-time were respectively assessed via the Perceived Stress Scale
acoustic feedbacks on the modulation of physiological signa- (PSS) (Cohen et al., 1983), the State subscale of the State/
ture of practicer's mindset. Going down to specifics, a pro- trait Anxiety inventory (STAI-state) (Pedrabissi and Santi-
prietary algorithm processes and combines power density nello, 1989), and the Five Facet Mindfulness Questionnaire
data concerning standard EEG frequency bands to accord- (FFMQ) (Giovannini et al., 2014).
ingly manipulate the sound environment (sound environ- The PSS has a single scale structure constituted by 10
ment) in which the practicer is immersed: the modulation of items. The responder has to rate on a 5-point Likert scale
EEG profile when moving from a focused mindset to an the frequency of specific thoughts or feelings and such data
Davide Crivelli et al. / Neuroscience 412 (2019) 83–93 87

are used to obtain a situational measure of subjectively-per- stimuli appearing on the PC screen were congruent or not.
ceived level of stress. The STAI-state subscale of the STAI Stimuli were four color-related words – the Italian words for
inventory is constituted by 20 items, where the responder ‘yellow’, ‘blue’, ‘green’, and ‘red’ – and could appear written
has to rate on a 4-point Likert scale how much each item in one of those four colors, thus defining congruent combina-
describes how he/she presently feels. The sum of such tions (i.e. matching word–color stimuli) and incongruent com-
scores provides a situational measure of the level of anxiety binations. Stimuli sequence was rapid and pressing. A total of
and related negative affectivity. Finally, the FFMQ is a 39- 160 stimuli were randomly presented. Stimuli duration was
item questionnaire in which responders are asked to rate, set to 300 ms. Performance was scored as a measure of
by using 5-point Likert scales, the frequency of specific beha- response times (RT), accuracy (ACC), and number of
vior or events that mirror different aspects of awareness of omitted responses (OR).
own thoughts, feelings and behaviors. The structure of the
questionnaire includes five main subscales related to specific Physiological markers of attention regulation
facets of being self-aware: ability to attend to external/internal
sensory stimuli and related thoughts and emotions During the execution of the Stroop-like task, participants’
(Observe); ability to label inner experiences with words electroencephalographic activity (EEG) was monitored and
(Describe); ongoing aware attention towards presents beha- recorded to extract event-related potentials and compute
viors, feelings, thoughts and inner experiences (Act with electrophysiological markers of attention regulation and effi-
Awareness); keeping an a-critical and non-evaluative stance ciency (Crivelli and Balconi, 2017). EEG was recorded with
when focusing on own thoughts, emotions, feelings and inner low invasivity by using a 15-channel montage (V-Amp record-
experiences (Non-Judge); and being able to perceive and ing system, Brain Products GmbH, Gilching, Germany). Ag/
focus on thoughts, feelings, emotions, and inner experiences AgCl electrodes were referenced to linked earlobes and
without feeling compelled to react or being overwhelmed by placed according to the 10–20 International System (Jasper,
their affective and stressful connotation (Non-React). 1958; see Fig. 1). Vertical EOG was also recorded in order to
keep track of ocular artifacts for subsequent correction and
rejection. EEG data were then filtered offline (bandpass filter,
Behavioral measures of cognitive performance range: 0.1–30 Hz, slope: 24 dB/OCT) and passed through
As for behavioral measures of cognitive performance, we an artifact correction ICA-based algorithm (Jung et al.,
asked participants to complete the MIDA battery (De Tanti 2000). Following automatized artifact correction, data were
et al., 1998) and a Stroop-like digitalized task (Stim2 soft- segmented with reference to the stimuli onset (epoch length:
ware, Compumedics Neuroscan, Charlotte, NC). MIDA is a 1000 ms; baseline: 200 ms) and visually inspected for resi-
standardized reaction-times battery based on a series of sub- dual ocular, muscle, or movement artifacts. Artifact-free seg-
tasks designed to assess different aspects of attention and ments (mean rejection rate: 9%) were then used to compute
executive control skills (Italian normative sample N = 354). condition-specific average waveforms. On average, 145 arti-
Subtasks focus on basic vigilance level (BasicRT subtask, fact-free segments have been included in the computations
in which participants have to react to a simple stimulus by of condition-specific waveforms. Morphological analysis of
pressing a button as quickly as possible), selective attention
(SimpleRT subtask, in which participants have to detect and
respond to a complex stimulus by pressing a button as
quickly as possible), extended spatial attention (SpatialRT
subtask, similar to the SimpleRT subtask though in this sub-
task the stimuli appear in different spatial locations), and per-
ceptual discrimination and inhibition skills (ComplexRT
subtask, in which participants have to detect and discriminate
two different stimuli and respond to only one of them by
pressing a button as quickly as possible while inhibiting the
response to the other one). Besides reaction times (RT),
scoring of performance during each subtask includes also
specific measures for omitted responses (OR; i.e. the num-
ber of missed responses, thus mirroring lack of attention),
early responses (ER; i.e. the number of responses that are
given before any stimulus appears, thus mirroring lack of
behavioral control), and false alarms (FA; i.e. the number of
time a response was given when it should have been
retained, thus mirroring impulsivity and lack of inhibition).
The digitalized Stroop-like task was introduced to further test
complex response selection skills and executive control
mechanisms under time pressure. Indeed, during such task
participants were asked to press one of two different Fig. 1. EEG montage according to the 10–20 International System. N:
response buttons as quickly as they could to signal whether nasion; I: inion; A1–A2: left and right pre-auricular points.
88 Davide Crivelli et al. / Neuroscience 412 (2019) 83–93

condition-specific waveforms consistently highlighted event- Mpost = 31.29, SDpost = 7.71; p ≤ .001, d = 0.622) at the
related negative deflections peaking around 200 ms, which end of the training.
have been classified as N2 ERP components. Finally, peak No other psychometric outcome measure presented statis-
latency and amplitude metrics at Fz, Cz, and Pz electrode tically significant modulations.
positions were extracted by using a semi-automatic weighted
peak detection algorithm. Behavioral measures of cognitive performance
Inferential statistics applied to pre- and post-training mea-
sures of behavioral performance at the computerized
Statistical analyses
Stroop-like task highlighted a significant main effect of the
Data collected during pre- and post-training assessment ses- Time factor (F[1,46] = 11.586, p = .001) and of the Group fac-
sions have been compared between groups trough linear tor (F[2,46] = 9.398, p ≤ .001) on RTs. Namely, reaction times
mixed-effects models (PASW Statistics 18, SPSS Inc., were generally lower after the training than before (Mpre =
Quarry Bay, HK) including Time (pre vs. post) and Group 622.01, SDpre = 91.10; Mpost = 604.07, SDpost = 96.24; p =
(Active Control [AC], Experimental Non-Athletic [ENA], and .001, d = 0.349) and were lower in the EA group than in the
Experimental Athletic [EA]) as fixed effects and subjects as AC (MAC = 652.34, SDAC = 85.09; MEA = 538.18, SDEA =
random effect. The inclusion of subjects as random effect 95.54; p ≤ .001, d = 1.262) and ENA (MENA = 633.09, SD-
allowed us to better control for potential confounding effects ENA = 61.52; MEA = 538.18, SDEA = 95.54; p = .004, d =
due to inter-individual differences. In addition, in order to 1.181) groups. No statistically significant difference was
account for time-related confounds while exploring interven- instead found between AC and ENA groups (p ≫ .05).
tion effects, we used a first-order autoregressive covariance Furthermore, the interaction between Group and Time was
matrix to model autocorrelations between data from subse- found to be significant (F[2,46] = 11.488, p ≤ .001). In particu-
quent assessments. Conditional F-tests were used to deter- lar, pair-wise comparisons highlighted a statistically-signifi-
mine the significance of terms in fixed effects. Main cant reduction of response times between pre- and post-
contrasts and simple effects for statistically significant inter- training assessments only in the EA group (MEA-pre =
actions were further checked via pair-wise comparisons. In 567.31, SDEA-pre = 107.09; MEA-post = 509.05, SDEA-post =
such cases, the Cohen's d index has been computed to 75.24; p ≤ .001, d = 1.006; see Fig. 2a). No other simple
obtain effect-size estimates of significant effects. Effect sizes effect was significant.
have been deemed as small when ≥0.2, medium when ≥0.5, Again, analysis of behavioral data of the MIDA battery high-
and large when ≥ 0.8, in agreement with Cohen's norms lighted a significant main effect of the Group factor on RTs at
(Cohen, 1988). Bonferroni correction was also applied to the ComplexRT subtask (F[2,46] = 6.554, p = .003), as well as
probability values in order to account for potential biases a significant Group × Time interaction effect on FA at the
due to multiple comparisons. Normality of the distribution of ComplexRT subtask (F[2,46] = 6.205, p = .004). Going down
data was preliminarily checked by computing kurtosis and to specifics, RTs at the ComplexRT subtask were lower in
asymmetry indices. the EA group than in the AC (MAC = 465.75, SDAC = 50.53;
The tested outcome measures included: psychometric MEA = 415.18, SDEA = 46.06; p = .005, d = 1.046) and
data — i.e. PSS and STAI-state scores, subscale scores for ENA (MENA = 460.32, SDENA = 47.25; MEA = 415.18, SD-
the five dimensions of the FFMQ questionnaire (Observe, EA = 46.06; p = .014, d = 0.967) groups. No statistically sig-
Describe, Act with Awareness, Non-Judge, and Non-React); nificant difference was instead found between AC and ENA
behavioral markers of cognitive performance — i.e. RTs, groups (p ≫ .05). As for the interaction effect, pair-wise com-
omitted responses (OR), early responses (ER), and false parisons performed on FA data at the ComplexRT subtask
alarms (FA) at the four subtasks of the MIDA battery, as well highlighted a statistically-significant reduction of false alarm
as RTs, accuracy (ACC), and omitted responses (OR) at the in the EA group following training (MEA-pre = 1.29, SDEA-pre =
Stroop-like digitalized task; and physiological markers of 1.64; MEA-post = 0.43, SDEA-post = 0.65; p = .001, d = 0.782;
attention regulation — i.e. amplitude and peak latency of see Fig. 2b). No other simple effect was significant.
the N2 ERP component. No other behavioral measure of performance presented
statistically significant modulations.

Physiological markers of attention regulation


RESULTS
The analysis of physiological markers of attention regulation
Psychometric measures
during the challenging cognitive task highlighted a significant
Statistical analysis applied to psychometric outcome mea- Group × Time interaction effect modulating peak amplitudes
sures highlighted a significant main effect of the Time factor of the N2 ERP component at the Fz electrode position
on PSS scores (F[1,46] = 7.054, p = .011) and on scores at (F[2,46] = 7.541, p = .001). In particular, pair-wise compari-
the Non-Judge subscale of the FFMQ (F[1,46] = 17.829, sons showed that N2 amplitude was significantly enhanced
p ≤ .001), with – respectively – a significant reduction of following the training in the EA group (MEA-pre = − 5.93, SD-
PSS scores (Mpre = 17.94, SDpre = 5.42; Mpost = 16.01, SD- EA-pre = 2.77; MEA-post = − 7.69, SDEA-post = 3.07; p = .011,
post = 5.02; p = .011, d = 0.418) and a significant increase of d = 0.791; see Fig. 3) and significantly reduced in the AC
FFMQ Non-Judge scores (Mpre = 27.73, SDpre = 6.60; group (MAC-pre = − 6.21, SDAC-pre = 2.12; MAC-post = − 4.78,
Davide Crivelli et al. / Neuroscience 412 (2019) 83–93 89

and applied investigations (Fronda et al., 2018; Balconi et


al., 2019a; Crivelli et al., 2019a; Balconi et al., 2019b), where
the combined protocol was tested in experimental settings
and with professionals exposed to work-related stressors,
and aimed at extending previous findings.
By comparing per-and post-training assessments between
experimental and active control groups we observed: (i) gen-
eralized reduction of perceived stress and increase of the
ability to keep a non-evaluative stance when focusing on feel-
ings and inner experiences across all participants; (ii) signifi-
cantly reduced response times and of false alarm responses
at challenging digitalized tasks tapping on attention and
executive control skills among sporty participants who com-
pleted the combined training program; and (iii) statistically
significant enhancement of an electrophysiological marker
of automatic attention orientation and regulation – i.e. the
N2 event-related potential – during a cognitively activating
task among the sporty participants who completed the
experimental training, while the active control group showed
reduced N2 amplitudes.
The generalized change of subjectively-perceived level of
stress and of the non-evaluative stance towards inner experi-
ences, feelings, and thoughts – even if negatively connoted –
suggests that both the experimental training program and the
active control one could ease participants' levels of distress,
even if mild, and improve their ability to accept their feelings,
emotions and thought, with a potentially-relevant effect on
subjective well-being. This might be due to the possibility that
both programs gave to participants the opportunity to
strengthen their self-awareness skills and their ability to get
close to inner experiences and related bodily sensations.
Indeed, participants in the Active Control group were actively
involved in an alternative structured protocol based on
breathing practices. An alternative explanation might take
into account the potential effect of those trainings on relaxa-
tion mechanisms, though this account seems to struggle with
Fig. 2. Pre- and post-training behavioral measures of cognitive perfor-
justifying observed modulations of the FFMQ Non-Judge
mance: (a) response times (RTs) at the digitalized Stroop-like task; (b)
false alarms (FAs) at the ComplexRT subtask of the MIDA battery. Bars scores. While those findings are in line with available litera-
represent ± 1 SE. Stars mark statistically significant pair-wise compari- ture on the effect of mental practices aimed at promoting
sons (p ≪ .05) for significant interaction effects. self-awareness and awareness of bodily sensations on emo-
tion regulation, self-acceptance and detachment skills (Vago
and Silbersweig, 2012; Creswell, 2017; Guendelman et al.,
SDAC-post = 3.40; p = .018, d = 0.474). Finally, pair-wise 2017; Subhani et al., 2018), the lack of measurable differ-
comparisons also revealed significantly greater N2 ampli- ences between groups opens interesting questions that are
tudes in the EA group than in the AC one at the end of the worth further investigations.
training (MAC-post = − 4.78, SDAC-post = 3.40; MEA-post = Findings of improved behavioral measures of performance
− 7.69, SDEA-post = 3.07; p = .010, d = 0.898). No other sim- during standardized cognitive tasks are consistent with the
ple effect was significant. set of empirical observations concerning the effect of mental
No other physiological marker presented statistically signif- training and meditation on cognitive functions (Lutz et al.,
icant modulations. 2008; Hommel and Colzato, 2017). Namely, sporty partici-
pants who completed the combined experimental training
became quicker in discriminating between conflicting stimuli
to correctly classify them and proved to aptly control beha-
DISCUSSION vioral reactions to correctly inhibit impulsive responses. It is
The present study aimed at investigating the potential for worth noting that the tasks that allowed detecting such mod-
improving for empowering attention control and psychological ulations of performance were actually the most effortful
well-being of a novel combine mindfulness–neurofeedback among the ones included in the assessment procedure. Both
training protocol, and at testing its feasibility in the applied the Stroop-like task and the ComplexRT subtask of the MIDA
sport context. This work build on previous proof-of-concept battery do indeed heavily rely on executive control and
90 Davide Crivelli et al. / Neuroscience 412 (2019) 83–93

Fig. 3. (a) Pre- and post-training physiological markers of attention regulation: peak amplitude for the N2 ERP component at Fz electrode position. Bars repre-
sent ±1SE. Stars mark statistically significant pair-wise comparisons (p ≪ .05) for significant interaction effects. (b) Scalp voltage maps related to the N2 ERP
component: grand average for groups and assessment steps.

response inhibition skills, both under time pressure and dur- process fostered by the technology-supported mental training
ing sustained performance. Since easier tasks tapping on program (Balconi et al., 2017) might need more time to yield
basic alertness and selective attention skills did not highlight substantial and statistically-robust changes of behavioral out-
relevant modulations of accuracy or reaction times, we sug- come measures, thus being characterized by a progressively
gest that observed improvement of performance at complex growing learning curve. On the other hand, the significant
tasks may plausibly follow the fine-tuning of participants' early improvement of sportspeople's behavioral performance
higher attention regulation skills via technology-supported suggests that formal sport training might have fostered
practices included in the protocol, besides the already opti- responsivity and proneness to learning of their psychomotor
mal performance level of lower psychomotor abilities. system, thus allowing them to optimize the implicit learning
While globally lower response times at the most-effortful curve sustained by practice with the neurofeedback device.
computerized tasks of participants that regularly practice Athletes are indeed thought to present remarkable sensitivity
sports may plausibly mirror their greater psychomotor skills to bodily and physical signals and notable bodily awareness
with respect to age-matched people who did not systemati- skills (Toner and Moran, 2014). We suggest that those pecu-
cally undergo sports training, additional data exploration of liar skills could have helped sporty participants to make better
the statistically significant interaction between Group and use of real-time feedbacks on implicit physiological modula-
Time factors on RTs highlighted a second interesting point. tions accompanying mental practice, and could have then
Indeed, though also participants not practicing sports who led them to benefit from the combined mindfulness–neuro-
completed the combined mindfulness–neurofeedback pro- feedback training earlier and more effectively than their non-
gram showed qualitatively reduced response times at the athletic counterparts.
Stroop-like task, only those who systematically undergo phy- Such interpretations seem supported even by the observed
sical practice presented a statistically significant change of enhancement of an electrophysiological marker of automatic
performance after just 2 weeks of intensive training. This attention orientation and regulation — namely, the N2 event-
empirical observation notably highlights the presence of early related potential (ERP). When recorded over anterior sites,
enhancement effects among sporty participants and plausi- the N2 ERP is indeed thought to mirror attention processes
bly mirrors some form of facilitation effect with regard to their subserving detection of novel and attended stimuli, cognitive
learning curves. Indeed, previous investigation of the effect of control, and stimuli–response monitoring (Folstein and Van
combined mindfulness–neurofeedback training programs on Petten, 2008). Moreover, such event-related potential was
neurocognitive efficiency markers revealed significant perfor- shown to be enhanced in expert athletes practicing sports
mance improvements after 4 weeks of practice in young that require notable attention regulation and orientation skills,
adults (Crivelli et al., 2019b). The observed trend in non-ath- such as fencing (Taddei et al., 2012; Bianco et al., 2017). And
letic experimental group is globally consistent with those pre- again, greater N2 deflections were even observed in associa-
vious observations and may suggest that the implicit learning tion to better cognitive performances following both
Davide Crivelli et al. / Neuroscience 412 (2019) 83–93 91

systematic physical training and acute exercise (Winneke et training grows with the level of sport proficiency (Kudlackova
al., 2012; Ligeza et al., 2018). et al., 2013).
Relevantly, such physiological marker was also found to be
enhanced by both mindfulness expertise (Atchley et al.,
2016) and trait mindfulness (Quaglia et al., 2016), mirroring
optimized attention regulation skills fine-tuned by mental
CONCLUSIONS
practice. Besides being consistent with limited available lit- Taken together, above-discussed findings hint at a quite con-
erature on task-related electrophysiological outcomes of sistent scenario characterized by improved attention regula-
mindfulness practice (Cahn and Polich, 2006; Lutz et al., tion and cognitive control mechanisms following the
2008; Atchley et al., 2016; Balconi and Crivelli, 2019a; Crivelli completion of a combined mindfulness–neurofeedback pro-
et al., 2019b), the remarkable increase of the N2 ERP com- gram, in agreement with previous proof-of-concept and
ponent that was observed even in the present group of sporty experimental studies (Balconi et al., 2017, 2019a, 2019a;
participants adds to behavioral measures of improved perfor- Balconi and Crivelli, 2019a; Crivelli et al., 2019b, 2019a).
mance and strengthens the hypothesis that the intensive We therefore suggest that constant mental practice helped,
combined mindfulness–neurofeedback training has led to in particular, participants who regularly practice sports to fos-
an improvement of participants' conflict monitoring and atten- ter their ability to focus and to intentionally reorient their atten-
tion orientation mechanisms. tion resources, that the integration with the highly-usable
It is also worth noting that also post-hoc analyses of wearable neurofeedback system eased such implicit learning
electrophysiological markers of attention regulation course and helped them to obtain measurable outcomes
mechanisms revealed, as observed for behavioral mea- quicker than when such empowerment effects are typically
sures of cognitive performance, a similar improvement reported, and that such early training effects might be
pattern among athletic and non-athletic participants, explained at the light of their optimized learning skills and
though only the former presented statistically-significant sensitivity to bodily signals. Namely, the neurofeedback
modulations of the N2 amplitude. We suggest that the device fostered empowerment effects by providing the practi-
consistency of pictures sketched by the analysis of elec- cers with real-time feedbacks on physiological changes
trophysiological and cognitive outcomes corroborates induced by awareness practices. In other words, neurofeed-
above-discussed interpretation of training-induced back gave the practicers the opportunity to access an other-
changes observed in our group of sportspeople. Namely, wise hidden source of information and then use those
the graded change of the physiological marker of atten- pieces of information to support implicit learning and training
tion regulation across sporty and non-sporty experimental of self-regulation mechanisms.
participants might mirror different implicit learning curves As an additional note, as underlined by Colzato and Kibele
between those categories of people in spite of the admin- (2017), extensive experience with mindfulness meditation
istration of the same experimental training protocol, and a has been associated with enhanced experience of flow
sort of bolstering effect induced by regular physical train- (Kee and Wang, 2008; Bernier et al., 2009; Kaufman et al.,
ing in sports. 2009), which is in turn known to influence athletic perfor-
As a further point, we have also qualitatively observed mance by sustaining motivation and focus over time. Present
good compliance levels among participants. Even if the train- initial findings do not allow a better investigation of the rela-
ing protocol was mostly managed autonomously – daily ses- tion between the intensive mindfulness–neurofeedback train-
sions were, indeed, performed by participants individually ing and experience of flow among our participants;
and at their residence – all of participants completely followed nonetheless, we think that this would be a critical issue for
the protocol and kept constant with their mental training ses- future investigation and would also help to better define tar-
sions. The combined training protocol therefore seemed not gets for intervention in sport contexts.
to interfere with their weekly schedule and with daily routine The present research report is not, nonetheless, exempt
and personal duties. We suggest that the integration of men- from limitations. Firstly, we acknowledge that further investi-
tal training practices with the supporting wearable neurofeed- gations with larger samples of participants who regularly
back system, by reducing the daily commitment required by practice sports and with professional athletes are needed to
the mental training protocol and by actively fostering implicit strengthen empirical observations and related remarks on
learning mechanisms, made participants experience it as the potential of the combined mindfulness–neurofeedback
not so invasive and sustained their engagement, as we pre- protocol for supporting sport training. Secondly, implications
viously observed also in other contexts. By making the for research and practice would benefit from broader investi-
access to those mental training forms easier and less expen- gations including a matched active control group composed
sive (both with respect to time and money), it might then be by sportspeople, as well as from critical comparisons with
possible to let even beginners, semi-professional athletes, other mental training protocols. For example, at the moment
and smaller teams or sporting clubs benefit from such addi- of testing, the protocol was completely based on FAM prac-
tional training opportunities. It is indeed worth noting that tices. However, Colzato and Kibele (2017) recently sug-
mental practices and meditation are already perceived by gested that different kinds of athletes may specifically
athletes as valuable and critical ways to enhance sport per- benefit from different forms of meditation depending on the
formance thanks to the improvement of self-regulation and type of sport they practice. In particular, performance in
focus, and that the importance attributed to such forms of closed-skills sports – i.e. sports where the action environment
92 Davide Crivelli et al. / Neuroscience 412 (2019) 83–93

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DECLARATION OF COMPETING INTEREST Crivelli D, Balconi M. (2017) Event-related electromagnetic responses.
Ref Modul Neurosci Biobehav Psychol :1-27.
Declarations of interest: none. Crivelli D, Fronda G, Venturella I, Balconi M. (2019) Stress and neuro-
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(Received 4 March 2019, Accepted 31 May 2019)


(Available online 10 June 2019)

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