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BJMB!
Brazilian Journal of Motor Behavior
!
Research Article!
!
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Apolinário-Souza et
al.!
2023!
VOL.17!
https://doi.org/10.20338/bjmb.v17i5.359 !
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Study of cerebral cortico-cortical coherence during motor practice!
TÉRCIO APOLINÁRIO-SOUZA
1
| GUILHERME M. LAGE
2
| LIDIANE A. FERNANDES
3
!
1
Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil!
2
Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil!
3
Universidade Federal de Juiz de Fora, Governador Valadares, MG, Brazil!
Correspondence to:!Tércio Apolinário-Souza. Address: R. Felizardo, 750 - Jardim Botânico, Porto Alegre - RS, Brasil; CEP: 90690-200.!
email: edf.tercio@gmail.com!
https://doi.org/10.20338/bjmb.v17i5.359
HIGHLIGHTS!
Coh increases areas related to motor execution and
decreases in those that are less related.!
The motor practice related to reduced cortico-cortical
communication in cognitive brain regions.!
Upsurge in neural plasticity in motor-related area during
practice.!
ABBREVIATIONS!
AE Absolute timing error!
Coh Coherence!
d Cohen’s d!
EEG Electroencephalogram!
FIR Finite impulse response!
Fz Frontal region!
IQR Interquartile range!
LTP Long-term potentiation!
M1 Primary motor cortex!
PLV Phase Locked Value!
q1 First quartile!
q3 Third quartile!
RE Relative timing error!
PUBLICATION DATA!
Received 13 04 2023!
Accepted 21 06 2023!
Published 30 09 2023!
BACKGROUND: Coherence is one of the neural mechanisms related to communication and
plasticity. The literature presents two divergent results regarding coherence and motor practice.
One result suggests a decrease in coherence during practice, while the other indicates an
increase in coherence throughout practice.!
AIM: Considering these two divergent results in the literature, this study aimed to examine the
role of coherence in motor practice. We hypothesize that electrode pairs related to C3 (C3-P3
and C3-F3) show an increase of coherence during practice, while electrodes less related to
motor action (F4, C4, and P4) may exhibit decreased. !
METHOD: Twenty-four right-handed participants practice 120 trials of a sequential key-pressing
task. !
RESULTS: The results indicated, in the alpha upper and theta bands, from initiation to end of
practice, the coherence increased in the F3-C3 electrode pair and decreased in the C3-C4, C3-
P3, P3-P4, F3-P3, and C4-P4 electrodes pairs. !
CONCLUSION: The results partially confirmed the hypothesis. The coherence increases in the
electrode pairings related to the motor execution and decreases between the lesser related.
During the motor learning process, communication reduction occurred in groups of neurons not
associated with the stimulus, and the potentiation of synaptic plasticity within groups of neurons
associated with the stimulus occurred.!
KEYWORDS: Motor learning | Motor control | Implicit learning | Neurophysiology!
INTRODUCTION!
The practice itself is the most critical variable in motor skill acquisition ¹, whether in music, rehabilitation, or sports. With practice,
the learner improves performance, becomes more speedy and accurate, and decreases errors ². Within a single practice session, it is
already possible to observe performance improvement, with much of this improvement depending on error detection and correction
mechanisms ³.!
A series of psychophysiological studies using electroencephalogram (EEG) have shown mechanisms underlying the modification
of brain activity due to practice (Reuter, Booms and Leow
4
for review). The EEG, via scalp, records the electrical signals produced by the
neurons, neurons are embedded in assemblies in which they influence mutually through excitatory and inhibitory synaptic connections
5
.
Neuronal assemblies refer to a group or ensemble of neurons that exhibit synchronized activity to perform a specific function or represent
certain information within the brain
6
. Individual neurons communicate with each other through synaptic connections, forming complex
networks
7
. Within these networks, the neuronal assemblies are functional units that require coordinated activity of multiple neurons to
accomplish specific tasks, such as motor response
8
. These assemblies are dynamic and flexible, reconfiguring themselves according to
demands
9
. The execution of motor actions per se generates perceptual-motor demands that reconfigure neuronal assemblies
10
.!
With practice, neurons are expected to change synchronization levels, increasing or decreasing specific neural response patterns
within neuronal assemblies
11
. This synchronized activity among neurons constitutes one of the principal mechanisms of memory formation
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Brazilian Journal of Motor Behavior
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Research Article!
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Apolinário-Souza et
al.!
2023!
VOL.17!
https://doi.org/10.20338/bjmb.v17i5.359 !
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255 of 265
for two principal reasons: cortico-cortical communication and mechanisms of plasticity
12
. In cortico-cortical communication terms,
synchronization may support neural communication by establishing transient associations between different brain areas
13
. For example,
when performing a throw, information regarding the ball's weight and color, the opponent's position vision, and the arm's speed are
processed in distinct brain regions. These pieces of information must be connected through a mechanism has ensured that the brain
associates them with the same action. The synchronization enables communication among the different brain regions. The mechanisms of
plasticity function of synchronization are associated with a classical concept of Hebbian learning
6
. Hebbian learning suggests that when
two neurons are repeatedly activated together, the strength of the synaptic connection between them is increased
6
. In this logic, the
increased synchronization results from several synaptic inputs arriving at postsynaptic neurons simultaneously (spatial summation),
enabling rapid depolarization
14
. This rapid depolarization increases the postsynaptic membrane potential above the firing threshold,
triggering the neural plasticity processes
15
.!
Two main results about synchronization and motor practice are found in the literature. The first result shows that synchronization
decreases with practice, reflecting the refinement of cortical resources
16
. Refinement of cortical resources refers to perfecting the available
resources within the brain's cortical areas to maximize their efficiency and capacity to perform specific functions. During motor practice,
reduced activity in frontal regions characterizes the refinement of cortical resources
17
. A series of processes occur through practice, leading
to decreased cognitive demand
18,19
. The frontal regions' activity is traditionally associated with cognitive processes
20
. Gentilli et al.
10
showed a reduction of synchronization in the early to late practice. This reduction occurred among electrode pairs considering the frontal
(Fz) region as the reference [FzF3, FzC3, FzC4, FzT4 (...)]. As mentioned above, the frontal regions’ activity would be more related
to the cognitive processes
20
, and the decreasing synchronization during practice would indicate movements less dependent on cognitive
processes
17
. In this rationale, synchronization is seen as cortico-cortical communication among brain areas
21
. As movements are less
dependent on cognitive processes with the advancement of practice
18,19
, the cortico-cortical communication between the frontal and other
areas could be decreased. Thus, the authors explain the reduction of synchronization as a decrease in cortico-cortical communication due
to a decrease in cognitive demand, typical of the motor learning process
10,22
.!
On the other hand, the previous results claim that with the practice, there is an increase in synchronization and not a decrease
23,24
. In this case, the increased synchronization during practice is an effect of the mechanisms of plasticity
11
. Kranczioch et al.
3
showed
better performance is related to increased synchronization between contralateral fronto-central and ipsilateral parieto-occipital brain
regions. The tenet here is that synchronous activity in the brain, precisely presynaptic and postsynaptic neurons, can lead to long-lasting
changes
25
.!
At first glance, one would consider these two kinds of results divergent. In the study of Gentilli et al.
10
, the synchronization
decreased considering reference to the frontal areas (Fz). While in the Kranczioch et al.
23
study, the synchronization was increased in the
local motor more related to movement. Perhaps, there is no divergence between results. The motor learning process may be associated
with a decrease in cortico-cortical communication among brain areas associated with cognitive processes
10
and a simultaneous increase
in neural plasticity processes in the brain areas related to movement
23
.!
Most often, researchers infer synchronization by observing coupling between different points. In animal experiments, researchers
record extracellular action potentials and analyze the local field potentials in the same or different regions. Human scalp EEG studies do
not measure action potentials. Here, synchronization refers either to the phase relation of EEG oscillations between two regions or
coherence. This way of inferring synchronization is similar to the one used by other studies in motor practice
10,22,23,26,27
.!
Considering this divergence in literature, there is a need to further examine the role of coherence in motor practice. We
hypothesize that, from initiation to end of practice, the coherence will increase in the electrode pairings more related to the motor execution
and decrease among less related electrode pairings to the motor execution. The primary motor cortex of the contralateral hemisphere
predominantly originates the descending projections that control unilateral movements
28
. In the present study, we used the right hand to
control movement. The C3 is equivalent to the M1 contralateral hemisphere for our motor task. Thus, we expect electrode pairs related to
C3 (C3-P3 and C3-F3) to exhibit increased coherence. On the other hand, electrodes less related to motor action, such as F4, C4, and P4,
may exhibit a decrease in coherence. Researchers have highlighted that brain activity in the theta and alpha frequency bands highly
responds to cognitive processing
29
. As is well known, the process of motor practice involves cognitive processing
18,19
; thus, using these
two frequency bands could indicate cognitive processing. Our study aims to shed light on this matter by exploring the potential coexistence
of two explanations for coherence results. Specifically, we investigate the possibility that the system operates in both ways, with increased
coherence observed in areas more closely associated with motor action. In contrast, areas less relevant to the task exhibit decreased
coherence.!