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Assessing vibratory stimulation-induced cortical activity during a motor task—A randomized clinical study
Accepted Manuscript Title: Assessing vibratory stimulation-induced cortical activity during a motor task — A randomized clinical study Author: Jana´ına de Moraes Silva Mario Oliveira Lima Fernanda Pupio Silva Lima Alderico Rodrigues de Paula J´unior Silmar Teixeira Lima Victor Hugo Bastos Rayele Pricila Moreira dos Santos Charlanne de Oliveira Marques Maria da Conceic¸a˜ o Barros Oliveira Felipe Aur´elio Nunes de Sousa PII: DOI: Reference:
S0304-3940(15)30158-0 http://dx.doi.org/doi:10.1016/j.neulet.2015.09.032 NSL 31561
To appear in:
Neuroscience Letters
Received date: Revised date: Accepted date:
29-6-2015 24-9-2015 25-9-2015
Please cite this article as: Jana´ina de Moraes Silva, Mario Oliveira Lima, Fernanda Pupio Silva Lima, Alderico Rodrigues de Paula J´unior, Silmar Teixeira Lima, Victor Hugo Bastos, Rayele Pricila Moreira dos Santos, Charlanne de Oliveira Marques, Maria da Conceic¸a˜ o Barros Oliveira, Felipe Aur´elio Nunes de Sousa, Assessing vibratory stimulation-induced cortical activity during a motor task mdash A randomized clinical study, Neuroscience Letters http://dx.doi.org/10.1016/j.neulet.2015.09.032 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ASSESSING VIBRATORY STIMULATION-INDUCED CORTICAL ACTIVITY DURING A MOTOR TASK — A RANDOMIZED CLINICAL STUDY
Janaína de Moraes Silvaa, Mario Oliveira Limab, Fernanda Pupio Silva Limab, Alderico Rodrigues de Paula Júniorc, Silmar Teixeira Limad, Victor Hugo Bastosd, Rayele Pricila Moreira dos Santosd, Charlanne de Oliveira Marquese, Maria da Conceição Barros Oliveiraf, Felipe Aurélio Nunes de Sousag .
a
Universidade do Vale do Paraíba – UNIVAP, São José dos Campos – SP. Endereço: Conjunto
Saci
Quadra-31Casa-26;
64020-290;
Teresina-PI
(86)99931-7552.
[email protected] b
c
Universidade do Vale do Paraíba - UNIVAP, São José dos Campos-SP
Instituto Nacional de Pesquisas Espaciais - INPE, São José dos Campos-SP
d
Universidade Federal Do Piauí – UFPI, Parnaíba –Pi
e
Universidade Federal do Rio Grande do Sul - UFRS, Porto Alegre - RS
f
Universidade Federal do Piauí - UFPI, Teresina-PI
g
Faculdade Santo Agostinho, Teresina-PI.
E-mail:
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HIGHLIGHTS
Evaluation of the vibration therapy effect on cortical dynamics is proposed
The vibratory stimulation causes a variability in cortical activation
Beta band alteration was found both in the ipsi-lateral and contra-lateral cortexes
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ABSTRACT Effects of vibratory stimulation on motor performance have been widely investigated. Many theories have been applied, in order to evaluate its influence on individuals; however, very few studies have researched vibratory stimulation-induced cortical behavior. The aim of the present study is to investigate behavioral changes, such as reaction time and index finger movements, as well as electrophysiological changes, using beta band absolute power, in subjects submitted to vibratory stimulation. For this study, 30 healthy subjects were randomly selected and divided into two groups, experimental and control, and were submitted to a right index finger task, before and after vibratory stimulation, which was applied to the right upper limb, while their standard cerebral activity was recorded through electroencephalogram. No significant difference was found among behavioral variables. On the other hand, beta band absolute power significantly increased in the experimental group for the C3, C4 and P4 derivations, while it decreased at P3. The results suggest that electrophysiological changes were induced by vibratory stimulation, while reaction time and task-related movements were not affected by it.
Keywords: Electroencephalography, beta band, vibration, somatosensory stimulation, motor cortex
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1. INTRODUCTION Vibratory stimulation has been used in programs for functional sensory-motor rehabilitation. During the last decade, this therapeutic modality stood out in clinical practice, providing benefits such as bone formation and hormone production improvement, functional capacity, strength, balance and proprioception enhancement [1,2,3,4]. Vibratory effects on the musculoskeletal system include motor unity synchronization, and synergism enhancement between agonistic and antagonistic muscles [5]. Studies report that modulating afferent inputs can bring persistent neuroplastic changes into motor cortical areas through the peripheral nerve [6]. Vibrations increase primary muscle spindle afferent influx, which stimulates the so-called tonic vibration reflex [7,8,9]. This suggests that somesthetic cortex projections can modulate motor cortex excitability, reinforcing the thesis of vibratory stimulation influencing cortical dynamics [10,11]. While vibratory stimulation is clinically and experimentally relevant, studies relating such practice to cortex dynamics using electroencephalography (EEG) are rare in the literature. In order to assess cortex activity during vibratory stimulation, electroencephalography may be used. This instrument allows us to register electrical activity in the brain cortex, and it is a useful tool for the study of functional states in different situations, as well as of responses to different external stimulus modalities, for the research on brain damage and disorder diagnoses. It is a simple, non-invasive test of high temporal resolution. Therefore, the research of neural patterns related to sensory and motor processes may be conducted by monitoring cortical activity, which helps to analyze sensory-motor integration mechanisms [12,13]. Thus, this study aims to evaluate the effects of vibratory stimulation on cortical electric potential in young healthy adults, with the hypothesis that vibratory stimulation-induced cortical activity increases after a motor task.
2. METHODS The present randomized controlled trial was conducted at the Brain Mapping and Functionality Laboratory at the Federal University of Piauí at Parnaíba (PI), and was approved by the Research Ethics Committee under the protocol number 573,552, in agreement with the Resolution 466/12, and after all subjects signed the Free and Informed Consent form.
2.1 Sample Thirty healthy volunteers participated in the study. In order to be included, all subjects: reported no history of mental or physical illness, verified through previous clinical assessment;
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were right-handed, according to the Edinburgh Inventory [14]; and did not use any psychoactive or psychotropic substance. The exclusion criteria included those participants who: did not adapt to the data-collection equipment; slept less than a 6 to 8-hour period the night before the task; had already been submitted to vibratory training in previous occasions; and who featured adverse conditions for vibratory stimulation, such as non-healed fractures, surgery scars, pregnancy and post-childbirth [15]. The present study comprised a sample of volunteer participants, randomly divided into two groups. The control group consisted of 3 women and 7 men (mean ±SD=24.1±3.9 years) and the experimental group consisted of 13 women and 7 men (mean ±SD=21.4±2.1 years). Participants were instructed to stop ingesting food three hours before the study and to abstain from coffee, alcohol and tobacco for at least 10 hours before the task.
2.2 Experimental Procedure First, personal data were collected for each participant; then, all subjects were clinically assessed, in order to determine their inclusion or not in the study. Once admitted to the research, each participant was comfortably seated in a chair. A 15-inch monitor was positioned on a table in front of the subjects. The right hand and forearm were leaned on a vibratory cushion, and the left upper limb was resting on the left leg. Then, the EEG cap was arranged onto the subjects, following all the pre-requisites for ideal signal acquisition, and electrodes (Ag/AgCl) were placed on a cap according to the International 10–20 system [16],
yielding monopole
derivations to linked earlobes set as reference points (biauriculate). Then, the EEG signal was amplified with a gain of 20,000. The data acquisition software (Delphi 5.0) was employed. Reaction time and task movement time were registered by the MMA 7340 accelerometer. A soundproof and electrically insulated room was prepared for the experiment, and lights were turned off during EEG signal acquisition. EEG signal was captured using BrainNet BNT 36-EEG (EMSA - Medical Instruments, Brazil). Initially, EEG signal acquisition consisted of an 8-minute data collection at rest; then, an accelerometer was coupled onto the right hand index finger, and the monitor was turned on, randomly providing a visual feedback. Volunteers were instructed to execute the index finger flexion and extension movement, as soon as the visual feedback appeared, generated by an image on the monitor. The experiment consisted of 3 blocks of 15 trials each, during which EEG signal and behavioral parameters were collected. In order to avoid muscular fatigue, the
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subjects had a 3-minute rest interval between each block. After completing the task, the monitor was turned off, the accelerometer was removed, and the volunteers were submitted again to EEG for 8 minutes. After EEG recording, subjects in the experimental group were submitted to 15-minute vibratory stimulation (Frequency: 56 Hz and Amplitude: 1.8 mm), using a Digital Vibration Cushion. Instead, in the control group, the cushion was kept off for fifteen minutes and, after such period of time, the same procedures described above were applied to both groups.
2.3 Signal Processing Initially, a visual inspection of received signals was conducted, in order to quantify reference-free data and identify and remove artefacts. Independent component analysis (ICA) was then applied, in order to identify and remove any remaining artefacts, which were doublechecked [17]. This process was performed by MATLAB (Mathworks®). Quantitative EEG parameters were obtained from data collected two second before and two seconds after the movement. Beta band absolute power was obtained by estimating the power spectral density. For this study, the C3, C4, P3 and P4 electrodes were selected. Band and derivation selection is important, because they are particularly associated with neural oscillations and with sensory-motor integration process areas [16].
2.4 Statistical Analysis Electrophysiological data analysis considered the functional cortical behavioral test before and after vibratory stimulation during a motor task. Data were normalized and standardized into absolute power values. Repeated measure ANOVA was used for statistical analysis, considering between group and moment factors; due to interaction, we later applied the paired t-test (independent groups). For the behavioral analysis, the Lilliefors test for normality and the paired t-test were applied, in order to compare the moment before and after in each group. The significance level was set at p ≤ 0.0125, following the Bonferroni test corrections. Analyses were conducted using the SPSS software for Windows, Version 18.0.
3. RESULTS In the behavioral analysis, time values measured in milliseconds (ms) were observed, for the moments before and after stimulation, in the control and experimental groups, respectively. The paired t-test results showed no significant difference for reaction time (Graph 1), between moments in the control (t =1.26; p =0.24) and experimental (t =0.50; p =0.61)
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groups, and for movement time (Graph 2) between the control group (t =0.63; p =0.54) and the experimental one (t =1.40; p =0.17). This means that motor performance was not affected by vibration application. For the electrophysiological analysis, beta band absolute power values were considered, collected two seconds before and two seconds after each flexion and extension movement of the index finger, before and after vibration. Using repeated measure ANOVA, interaction was found between the group and moment factors for the C3 derivation [F=(1,2520) =18.343; p=0.001; ƞ² =0.11]. This way, when investigating interaction with the paired t-test, significant difference was found between moments, for the control (t =1.17; p = 0.001) and experimental (t =1.01; p = 0.001) groups. In the experimental group, beta band absolute power mean increased after vibration, while it decreased in the control group; this indicates greater vibrationinduced contra-lateral motor cortex activity during the task in the experimental group, shown by the C3 derivation (Graph 3). When looking at the C4 derivation [F= (1, 2520) =2.373; p=0.001; ƞ² =0.027], interaction was found between the group and moment factors; after applying a paired t-test, significant difference was observed between moments, for the control (t =1.01; p = 0.001) and experimental (t =1.05; p = 0.001) groups. Beta band absolute power mean increased after vibration in the experimental group, while it decreased in the control group, showing greater vibration-induced ipsi-lateral motor cortex activity during the task, indicated by the C4 derivation (Graph 4). With relation to the P3 derivation [F=(1,2520) =51.500; p=0.001; ƞ² =0.17], significant difference was registered between moments, for the control (t =1.03; p = 0.001) and experimental (t =1.04; p = 0.001) groups. In the experimental group, beta band absolute power mean decreased after vibration, while it increased in the control group. This indicates lower vibration-induced contra-lateral somatosensory cortex activity during the task in the experimental group, shown by the P3 derivation (Graph 5). For the P4 derivation [F = (1,2520) =1.508; p=0.001; ƞ² =0.01], significant difference was detected between moments for the control (t =0.98; p = 0.001) and experimental (t =1.02; p = 0.001) groups. In the experimental group, beta band absolute power mean increased after vibration, while it decreased in the control group. This demonstrates greater vibration-induced ipsi-lateral (with respect to the stimulated limb) somatosensory cortex activity during the task in the experimental group, indicated by the P4 derivation (Graph 6). The control and experimental groups consisted of different subjects, featuring their own individual neurophysiological activity, thus justifying the difference between the control and
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the experimental group at the baseline levels (rest), which were significantly different for the four considered cortical regions. It is worth highlighting that significant difference was especially important when considering the moments before and after each group and the absolute power mean between groups.
4. DISCUSSION The aim of the present study was to analyze behavioral and electrophysiological alterations induced by vibratory stimulation in subjects submitted to a motor task. In particular, both reaction and movement time will be initially discussed; then cortical dynamics after vibratory stimulation application will be examined, through the beta band absolute power mean, for the C3, C4, P3 and P4 derivations. Behavioral Variables (Reaction Time and Movement Time) – the research has highlighted that both control and experimental group participants increased their reaction time to the visual feedback, while they decreased their movement time (right index finger flexion/extension); however, such results were not significant between groups and moments, thus going against the findings from other studies about vibration use and motor performance improvement [18,11,8,15]. Although the present study does not allow for determining the possible reasons for such findings, we may suggest that the sensorial stimulus-focused attention influence might have triggered such results. The body representation reorganization within the somatosensory cortex, after prolonged sensorial stimulation, may be achieved if attention is given to sensorial entrances [19]. Similar results were observed in a study that applied 15minute vibration onto the upper limb muscle tendon of individuals, resulting in a spatial distribution alteration of sensorial inputs to the sensory-motor areas, depending on the subjects’ attention given to vibration during the intervention [20]. In addition, different vibration parameters may influence such findings. A pioneering study, conducted with the aim of analyzing a short vibration intervention using different amplitudes and a frequency of 80 Hz, showed no significant difference in cortical excitability [10]. On the other hand, a research conducted using 25 Hz-vibratory stimulation on the upper limb increased corticospinal excitability within two hours after the stimulus removal. [7]. Other factors may have affected the behavioral variable results, such as: genetics, training time and modality, emotional status and cognitive level [21]; however, such factors have not been fully addressed in the literature yet, and they have not been included into the sample legitimacy criteria, thus showing the study limitations.
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Electrophysiological Variables –Contra-lateral Hemisphere: considering the literature establishing that: 1) repeated vibration sensorial inputs are maintained for a period of up to 30 minutes after the stimulus end, thus causing a significant reorganization of sensory-motor representations [22]; and that, 2) according to the methodological design of this study, vibration was applied for 15 minutes and electroencephalographic data collection was conducted for 23 minutes, we understand that the sensorial inputs were still present, even after the stimulus end and during the task blocks (experimental group). According to the electroencephalographic analysis, interaction between the group and moment factors demonstrated the control group participants to feature beta band absolute power value decrease at C3, while increase occurred in the experimental group, showing significant differences for groups and moments. The motor cortex electrophysiological behavior decrease (C3) in the control group may be associated with efficient processing in the cortical area, thanks to motor learning. When a subject extensively practices certain movement, the motor standards are memorized and automatized during the experience. This means that the individual does not need to execute them consciously and can focus his/her attention on all motor elements of the task he/she is executing [23]. On the other hand, C3 increased in the experimental group. Such results suggest that the application of vibratory stimulation induced cortical activity increase in the motor area, during the index finger task execution. After concluding a voluntary movement or after responding to somatosensory stimulation, cortical beta rhythm synchronization is observed in the contra-lateral cortex; this depends on the afferent entrance type and quantity, being more significant in the cutaneous stimulation [24,25]. In addition to this, beta band synchrony in response to motor imagery can be highlighted [26,27]. A type of motor imagery is kinesthetic illusion. The illusory sensation of the limb movement may be provoked by artificial manipulation of proprioceptive ways through vibration. Positron emitting-tomography studies suggest kinesthetic illusions to be experienced through vibration, which then leads to contra-lateral primary motor cortex activation. [28]. The movement illusion triggers a new sensory-motor representation reorganization by referring to a new movement or by maintaining tonic activity, therefore originating a new motor activity standard and activation of specialized cortical areas [5,29]. Considering this, cortical activity increase in the motor cortex during an index finger task would indicate kinesthetic illusion to be underlying vibratory stimulation. As for the P3 derivation, interaction between the group and moment factors showed control participants to feature increase in the beta band absolute power values, while decrease occurred in the experimental group. Such findings in the control group may be associated with the final stage of learned movement automatization, highlighting an increase in the efficiency
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and capacity to detect, recognize and correct mistakes, that originate from an imperfect muscular selection, which leads to inappropriate execution of the intended behavior during the task, therefore affecting afferent retro-feeding , through greater somatosensory area activity [30]. Beta absolute power decrease at P3 in the experimental group may be caused by cortical neuron response attenuation, by an adaptation to stimulus characteristics, and by prolonged exposure. This may be explained by a vibration influence on the connections between the motor and somatosensory cortexes [31] and may be controlled through various subtypes of gammaaminobutyric receptors [32]. Gabaminergic transmissions may have led to gradual synaptic transmission decrease, thus reducing the response to vibratory stimulation during the motor task [20]. The results from the present study are in agreement with those researches showing that the spindle afferent response capacity decreases after prolonged vibration, and is expressed by the somatosensory cortical electrophysiological behavior reduction, indicated by the P3 derivation [33,34]. Electrophysiological Variables –Ipsi-lateral Hemisphere: Considering the C4 and P4 behavior, decrease was found in the control group, while increase was observed in the experimental group. The possible mechanisms for such results to occur at C4 are related to inter-hemispheric connections, and for them to occur at P4, they are related to cerebral hemispheric specializations. Vibration training in healthy individuals affects the muscles both contra-lateral and ipsi-lateral to the stimulus, thus showing inter-hemispheric connection of the sensorial information through the supplementary motor area and the corpus callosum [16]. In addition, among the many specializations of the brain hemispheres, the right one stands out because of its response to environmental unexpected stimuli, geometric figure identification and visuomotor tasks [35]. Since the research experimental procedure generated a squared geometric visual feedback in a vibratory additional afferent input situation, it is possible to understand the activity increase in the somatosensory cortex ipsi-lateral to the vibration (P4). The cortical behavior in the control group was expected, since voluntary movements, as well as proprioceptive information, originate in the cortex on the opposite side, thus indicating little cortical activity in the cortex ipsi-lateral to the target limb. The present study has demonstrated cortical activity to increase after a motor task, due to vibration. However, no significant difference was found for the behavioral variables, suggesting that other factors may have influenced the results. Among them, sample size is addressed. In this case, a greater number of subjects could present different results. One more limitation of this research refers to the statement that vibratory stimulation-induced changes in cortical activity would be clinically important for rehabilitation. However, this study was
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conducted with healthy subjects, thus leaving a gap with relation to vibratory stimulation influence in groups with neurological dysfunctions, especially when we consider their inherent heterogeneity and the fact that ideal stimulus standards necessary for promoting cortical changes through various regeneration processes are still unknown. Despite this, the present research highlights the power of vibratory stimulation, not only for cortical behavior changes, but also for sensory-motor integration modulation in healthy individuals. REFERENCES
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Graph 1: Mean and Standard Deviation (SD) for Reaction Time before and after vibratory stimulation application, obtained through a paired t-test. Control Group (p=0.24); Experimental Group (p=0.61).
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Graph 2: Mean and SD for Movement Time before and after vibratory stimulation application, obtained through a paired t-test. Control Group (p=0.54); Experimental Group (p=0.17).
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Graph 3: Mean and SD for beta absolute power before and after vibratory stimulation application at C3, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
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Graph 4: Mean and SD for beta absolute power before and after vibratory stimulation application at C4, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
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Graph 5: Mean and SD for beta absolute power before and after vibratory stimulation application at P3, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
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Graph 6: Mean and SD for beta absolute power before and after vibratory stimulation application at P4, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
S0304-3940(15)30158-0 http://dx.doi.org/doi:10.1016/j.neulet.2015.09.032 NSL 31561
To appear in:
Neuroscience Letters
Received date: Revised date: Accepted date:
29-6-2015 24-9-2015 25-9-2015
Please cite this article as: Jana´ina de Moraes Silva, Mario Oliveira Lima, Fernanda Pupio Silva Lima, Alderico Rodrigues de Paula J´unior, Silmar Teixeira Lima, Victor Hugo Bastos, Rayele Pricila Moreira dos Santos, Charlanne de Oliveira Marques, Maria da Conceic¸a˜ o Barros Oliveira, Felipe Aur´elio Nunes de Sousa, Assessing vibratory stimulation-induced cortical activity during a motor task mdash A randomized clinical study, Neuroscience Letters http://dx.doi.org/10.1016/j.neulet.2015.09.032 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ASSESSING VIBRATORY STIMULATION-INDUCED CORTICAL ACTIVITY DURING A MOTOR TASK — A RANDOMIZED CLINICAL STUDY
Janaína de Moraes Silvaa, Mario Oliveira Limab, Fernanda Pupio Silva Limab, Alderico Rodrigues de Paula Júniorc, Silmar Teixeira Limad, Victor Hugo Bastosd, Rayele Pricila Moreira dos Santosd, Charlanne de Oliveira Marquese, Maria da Conceição Barros Oliveiraf, Felipe Aurélio Nunes de Sousag .
a
Universidade do Vale do Paraíba – UNIVAP, São José dos Campos – SP. Endereço: Conjunto
Saci
Quadra-31Casa-26;
64020-290;
Teresina-PI
(86)99931-7552.
[email protected] b
c
Universidade do Vale do Paraíba - UNIVAP, São José dos Campos-SP
Instituto Nacional de Pesquisas Espaciais - INPE, São José dos Campos-SP
d
Universidade Federal Do Piauí – UFPI, Parnaíba –Pi
e
Universidade Federal do Rio Grande do Sul - UFRS, Porto Alegre - RS
f
Universidade Federal do Piauí - UFPI, Teresina-PI
g
Faculdade Santo Agostinho, Teresina-PI.
E-mail:
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HIGHLIGHTS
Evaluation of the vibration therapy effect on cortical dynamics is proposed
The vibratory stimulation causes a variability in cortical activation
Beta band alteration was found both in the ipsi-lateral and contra-lateral cortexes
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ABSTRACT Effects of vibratory stimulation on motor performance have been widely investigated. Many theories have been applied, in order to evaluate its influence on individuals; however, very few studies have researched vibratory stimulation-induced cortical behavior. The aim of the present study is to investigate behavioral changes, such as reaction time and index finger movements, as well as electrophysiological changes, using beta band absolute power, in subjects submitted to vibratory stimulation. For this study, 30 healthy subjects were randomly selected and divided into two groups, experimental and control, and were submitted to a right index finger task, before and after vibratory stimulation, which was applied to the right upper limb, while their standard cerebral activity was recorded through electroencephalogram. No significant difference was found among behavioral variables. On the other hand, beta band absolute power significantly increased in the experimental group for the C3, C4 and P4 derivations, while it decreased at P3. The results suggest that electrophysiological changes were induced by vibratory stimulation, while reaction time and task-related movements were not affected by it.
Keywords: Electroencephalography, beta band, vibration, somatosensory stimulation, motor cortex
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1. INTRODUCTION Vibratory stimulation has been used in programs for functional sensory-motor rehabilitation. During the last decade, this therapeutic modality stood out in clinical practice, providing benefits such as bone formation and hormone production improvement, functional capacity, strength, balance and proprioception enhancement [1,2,3,4]. Vibratory effects on the musculoskeletal system include motor unity synchronization, and synergism enhancement between agonistic and antagonistic muscles [5]. Studies report that modulating afferent inputs can bring persistent neuroplastic changes into motor cortical areas through the peripheral nerve [6]. Vibrations increase primary muscle spindle afferent influx, which stimulates the so-called tonic vibration reflex [7,8,9]. This suggests that somesthetic cortex projections can modulate motor cortex excitability, reinforcing the thesis of vibratory stimulation influencing cortical dynamics [10,11]. While vibratory stimulation is clinically and experimentally relevant, studies relating such practice to cortex dynamics using electroencephalography (EEG) are rare in the literature. In order to assess cortex activity during vibratory stimulation, electroencephalography may be used. This instrument allows us to register electrical activity in the brain cortex, and it is a useful tool for the study of functional states in different situations, as well as of responses to different external stimulus modalities, for the research on brain damage and disorder diagnoses. It is a simple, non-invasive test of high temporal resolution. Therefore, the research of neural patterns related to sensory and motor processes may be conducted by monitoring cortical activity, which helps to analyze sensory-motor integration mechanisms [12,13]. Thus, this study aims to evaluate the effects of vibratory stimulation on cortical electric potential in young healthy adults, with the hypothesis that vibratory stimulation-induced cortical activity increases after a motor task.
2. METHODS The present randomized controlled trial was conducted at the Brain Mapping and Functionality Laboratory at the Federal University of Piauí at Parnaíba (PI), and was approved by the Research Ethics Committee under the protocol number 573,552, in agreement with the Resolution 466/12, and after all subjects signed the Free and Informed Consent form.
2.1 Sample Thirty healthy volunteers participated in the study. In order to be included, all subjects: reported no history of mental or physical illness, verified through previous clinical assessment;
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were right-handed, according to the Edinburgh Inventory [14]; and did not use any psychoactive or psychotropic substance. The exclusion criteria included those participants who: did not adapt to the data-collection equipment; slept less than a 6 to 8-hour period the night before the task; had already been submitted to vibratory training in previous occasions; and who featured adverse conditions for vibratory stimulation, such as non-healed fractures, surgery scars, pregnancy and post-childbirth [15]. The present study comprised a sample of volunteer participants, randomly divided into two groups. The control group consisted of 3 women and 7 men (mean ±SD=24.1±3.9 years) and the experimental group consisted of 13 women and 7 men (mean ±SD=21.4±2.1 years). Participants were instructed to stop ingesting food three hours before the study and to abstain from coffee, alcohol and tobacco for at least 10 hours before the task.
2.2 Experimental Procedure First, personal data were collected for each participant; then, all subjects were clinically assessed, in order to determine their inclusion or not in the study. Once admitted to the research, each participant was comfortably seated in a chair. A 15-inch monitor was positioned on a table in front of the subjects. The right hand and forearm were leaned on a vibratory cushion, and the left upper limb was resting on the left leg. Then, the EEG cap was arranged onto the subjects, following all the pre-requisites for ideal signal acquisition, and electrodes (Ag/AgCl) were placed on a cap according to the International 10–20 system [16],
yielding monopole
derivations to linked earlobes set as reference points (biauriculate). Then, the EEG signal was amplified with a gain of 20,000. The data acquisition software (Delphi 5.0) was employed. Reaction time and task movement time were registered by the MMA 7340 accelerometer. A soundproof and electrically insulated room was prepared for the experiment, and lights were turned off during EEG signal acquisition. EEG signal was captured using BrainNet BNT 36-EEG (EMSA - Medical Instruments, Brazil). Initially, EEG signal acquisition consisted of an 8-minute data collection at rest; then, an accelerometer was coupled onto the right hand index finger, and the monitor was turned on, randomly providing a visual feedback. Volunteers were instructed to execute the index finger flexion and extension movement, as soon as the visual feedback appeared, generated by an image on the monitor. The experiment consisted of 3 blocks of 15 trials each, during which EEG signal and behavioral parameters were collected. In order to avoid muscular fatigue, the
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subjects had a 3-minute rest interval between each block. After completing the task, the monitor was turned off, the accelerometer was removed, and the volunteers were submitted again to EEG for 8 minutes. After EEG recording, subjects in the experimental group were submitted to 15-minute vibratory stimulation (Frequency: 56 Hz and Amplitude: 1.8 mm), using a Digital Vibration Cushion. Instead, in the control group, the cushion was kept off for fifteen minutes and, after such period of time, the same procedures described above were applied to both groups.
2.3 Signal Processing Initially, a visual inspection of received signals was conducted, in order to quantify reference-free data and identify and remove artefacts. Independent component analysis (ICA) was then applied, in order to identify and remove any remaining artefacts, which were doublechecked [17]. This process was performed by MATLAB (Mathworks®). Quantitative EEG parameters were obtained from data collected two second before and two seconds after the movement. Beta band absolute power was obtained by estimating the power spectral density. For this study, the C3, C4, P3 and P4 electrodes were selected. Band and derivation selection is important, because they are particularly associated with neural oscillations and with sensory-motor integration process areas [16].
2.4 Statistical Analysis Electrophysiological data analysis considered the functional cortical behavioral test before and after vibratory stimulation during a motor task. Data were normalized and standardized into absolute power values. Repeated measure ANOVA was used for statistical analysis, considering between group and moment factors; due to interaction, we later applied the paired t-test (independent groups). For the behavioral analysis, the Lilliefors test for normality and the paired t-test were applied, in order to compare the moment before and after in each group. The significance level was set at p ≤ 0.0125, following the Bonferroni test corrections. Analyses were conducted using the SPSS software for Windows, Version 18.0.
3. RESULTS In the behavioral analysis, time values measured in milliseconds (ms) were observed, for the moments before and after stimulation, in the control and experimental groups, respectively. The paired t-test results showed no significant difference for reaction time (Graph 1), between moments in the control (t =1.26; p =0.24) and experimental (t =0.50; p =0.61)
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groups, and for movement time (Graph 2) between the control group (t =0.63; p =0.54) and the experimental one (t =1.40; p =0.17). This means that motor performance was not affected by vibration application. For the electrophysiological analysis, beta band absolute power values were considered, collected two seconds before and two seconds after each flexion and extension movement of the index finger, before and after vibration. Using repeated measure ANOVA, interaction was found between the group and moment factors for the C3 derivation [F=(1,2520) =18.343; p=0.001; ƞ² =0.11]. This way, when investigating interaction with the paired t-test, significant difference was found between moments, for the control (t =1.17; p = 0.001) and experimental (t =1.01; p = 0.001) groups. In the experimental group, beta band absolute power mean increased after vibration, while it decreased in the control group; this indicates greater vibrationinduced contra-lateral motor cortex activity during the task in the experimental group, shown by the C3 derivation (Graph 3). When looking at the C4 derivation [F= (1, 2520) =2.373; p=0.001; ƞ² =0.027], interaction was found between the group and moment factors; after applying a paired t-test, significant difference was observed between moments, for the control (t =1.01; p = 0.001) and experimental (t =1.05; p = 0.001) groups. Beta band absolute power mean increased after vibration in the experimental group, while it decreased in the control group, showing greater vibration-induced ipsi-lateral motor cortex activity during the task, indicated by the C4 derivation (Graph 4). With relation to the P3 derivation [F=(1,2520) =51.500; p=0.001; ƞ² =0.17], significant difference was registered between moments, for the control (t =1.03; p = 0.001) and experimental (t =1.04; p = 0.001) groups. In the experimental group, beta band absolute power mean decreased after vibration, while it increased in the control group. This indicates lower vibration-induced contra-lateral somatosensory cortex activity during the task in the experimental group, shown by the P3 derivation (Graph 5). For the P4 derivation [F = (1,2520) =1.508; p=0.001; ƞ² =0.01], significant difference was detected between moments for the control (t =0.98; p = 0.001) and experimental (t =1.02; p = 0.001) groups. In the experimental group, beta band absolute power mean increased after vibration, while it decreased in the control group. This demonstrates greater vibration-induced ipsi-lateral (with respect to the stimulated limb) somatosensory cortex activity during the task in the experimental group, indicated by the P4 derivation (Graph 6). The control and experimental groups consisted of different subjects, featuring their own individual neurophysiological activity, thus justifying the difference between the control and
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the experimental group at the baseline levels (rest), which were significantly different for the four considered cortical regions. It is worth highlighting that significant difference was especially important when considering the moments before and after each group and the absolute power mean between groups.
4. DISCUSSION The aim of the present study was to analyze behavioral and electrophysiological alterations induced by vibratory stimulation in subjects submitted to a motor task. In particular, both reaction and movement time will be initially discussed; then cortical dynamics after vibratory stimulation application will be examined, through the beta band absolute power mean, for the C3, C4, P3 and P4 derivations. Behavioral Variables (Reaction Time and Movement Time) – the research has highlighted that both control and experimental group participants increased their reaction time to the visual feedback, while they decreased their movement time (right index finger flexion/extension); however, such results were not significant between groups and moments, thus going against the findings from other studies about vibration use and motor performance improvement [18,11,8,15]. Although the present study does not allow for determining the possible reasons for such findings, we may suggest that the sensorial stimulus-focused attention influence might have triggered such results. The body representation reorganization within the somatosensory cortex, after prolonged sensorial stimulation, may be achieved if attention is given to sensorial entrances [19]. Similar results were observed in a study that applied 15minute vibration onto the upper limb muscle tendon of individuals, resulting in a spatial distribution alteration of sensorial inputs to the sensory-motor areas, depending on the subjects’ attention given to vibration during the intervention [20]. In addition, different vibration parameters may influence such findings. A pioneering study, conducted with the aim of analyzing a short vibration intervention using different amplitudes and a frequency of 80 Hz, showed no significant difference in cortical excitability [10]. On the other hand, a research conducted using 25 Hz-vibratory stimulation on the upper limb increased corticospinal excitability within two hours after the stimulus removal. [7]. Other factors may have affected the behavioral variable results, such as: genetics, training time and modality, emotional status and cognitive level [21]; however, such factors have not been fully addressed in the literature yet, and they have not been included into the sample legitimacy criteria, thus showing the study limitations.
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Electrophysiological Variables –Contra-lateral Hemisphere: considering the literature establishing that: 1) repeated vibration sensorial inputs are maintained for a period of up to 30 minutes after the stimulus end, thus causing a significant reorganization of sensory-motor representations [22]; and that, 2) according to the methodological design of this study, vibration was applied for 15 minutes and electroencephalographic data collection was conducted for 23 minutes, we understand that the sensorial inputs were still present, even after the stimulus end and during the task blocks (experimental group). According to the electroencephalographic analysis, interaction between the group and moment factors demonstrated the control group participants to feature beta band absolute power value decrease at C3, while increase occurred in the experimental group, showing significant differences for groups and moments. The motor cortex electrophysiological behavior decrease (C3) in the control group may be associated with efficient processing in the cortical area, thanks to motor learning. When a subject extensively practices certain movement, the motor standards are memorized and automatized during the experience. This means that the individual does not need to execute them consciously and can focus his/her attention on all motor elements of the task he/she is executing [23]. On the other hand, C3 increased in the experimental group. Such results suggest that the application of vibratory stimulation induced cortical activity increase in the motor area, during the index finger task execution. After concluding a voluntary movement or after responding to somatosensory stimulation, cortical beta rhythm synchronization is observed in the contra-lateral cortex; this depends on the afferent entrance type and quantity, being more significant in the cutaneous stimulation [24,25]. In addition to this, beta band synchrony in response to motor imagery can be highlighted [26,27]. A type of motor imagery is kinesthetic illusion. The illusory sensation of the limb movement may be provoked by artificial manipulation of proprioceptive ways through vibration. Positron emitting-tomography studies suggest kinesthetic illusions to be experienced through vibration, which then leads to contra-lateral primary motor cortex activation. [28]. The movement illusion triggers a new sensory-motor representation reorganization by referring to a new movement or by maintaining tonic activity, therefore originating a new motor activity standard and activation of specialized cortical areas [5,29]. Considering this, cortical activity increase in the motor cortex during an index finger task would indicate kinesthetic illusion to be underlying vibratory stimulation. As for the P3 derivation, interaction between the group and moment factors showed control participants to feature increase in the beta band absolute power values, while decrease occurred in the experimental group. Such findings in the control group may be associated with the final stage of learned movement automatization, highlighting an increase in the efficiency
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and capacity to detect, recognize and correct mistakes, that originate from an imperfect muscular selection, which leads to inappropriate execution of the intended behavior during the task, therefore affecting afferent retro-feeding , through greater somatosensory area activity [30]. Beta absolute power decrease at P3 in the experimental group may be caused by cortical neuron response attenuation, by an adaptation to stimulus characteristics, and by prolonged exposure. This may be explained by a vibration influence on the connections between the motor and somatosensory cortexes [31] and may be controlled through various subtypes of gammaaminobutyric receptors [32]. Gabaminergic transmissions may have led to gradual synaptic transmission decrease, thus reducing the response to vibratory stimulation during the motor task [20]. The results from the present study are in agreement with those researches showing that the spindle afferent response capacity decreases after prolonged vibration, and is expressed by the somatosensory cortical electrophysiological behavior reduction, indicated by the P3 derivation [33,34]. Electrophysiological Variables –Ipsi-lateral Hemisphere: Considering the C4 and P4 behavior, decrease was found in the control group, while increase was observed in the experimental group. The possible mechanisms for such results to occur at C4 are related to inter-hemispheric connections, and for them to occur at P4, they are related to cerebral hemispheric specializations. Vibration training in healthy individuals affects the muscles both contra-lateral and ipsi-lateral to the stimulus, thus showing inter-hemispheric connection of the sensorial information through the supplementary motor area and the corpus callosum [16]. In addition, among the many specializations of the brain hemispheres, the right one stands out because of its response to environmental unexpected stimuli, geometric figure identification and visuomotor tasks [35]. Since the research experimental procedure generated a squared geometric visual feedback in a vibratory additional afferent input situation, it is possible to understand the activity increase in the somatosensory cortex ipsi-lateral to the vibration (P4). The cortical behavior in the control group was expected, since voluntary movements, as well as proprioceptive information, originate in the cortex on the opposite side, thus indicating little cortical activity in the cortex ipsi-lateral to the target limb. The present study has demonstrated cortical activity to increase after a motor task, due to vibration. However, no significant difference was found for the behavioral variables, suggesting that other factors may have influenced the results. Among them, sample size is addressed. In this case, a greater number of subjects could present different results. One more limitation of this research refers to the statement that vibratory stimulation-induced changes in cortical activity would be clinically important for rehabilitation. However, this study was
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conducted with healthy subjects, thus leaving a gap with relation to vibratory stimulation influence in groups with neurological dysfunctions, especially when we consider their inherent heterogeneity and the fact that ideal stimulus standards necessary for promoting cortical changes through various regeneration processes are still unknown. Despite this, the present research highlights the power of vibratory stimulation, not only for cortical behavior changes, but also for sensory-motor integration modulation in healthy individuals. REFERENCES
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Graph 1: Mean and Standard Deviation (SD) for Reaction Time before and after vibratory stimulation application, obtained through a paired t-test. Control Group (p=0.24); Experimental Group (p=0.61).
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Graph 2: Mean and SD for Movement Time before and after vibratory stimulation application, obtained through a paired t-test. Control Group (p=0.54); Experimental Group (p=0.17).
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Graph 3: Mean and SD for beta absolute power before and after vibratory stimulation application at C3, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
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Graph 4: Mean and SD for beta absolute power before and after vibratory stimulation application at C4, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
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Graph 5: Mean and SD for beta absolute power before and after vibratory stimulation application at P3, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.
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Graph 6: Mean and SD for beta absolute power before and after vibratory stimulation application at P4, obtained through a repeated measure ANOVA, followed by a paired t-test. Significant difference between groups and moments was set at: p=0.001.