INTRODUCTION

Motor asymmetry is one of the obvious manifestations of functional hemispheric asymmetry (FHA) [1–3]. Its concept is evolving by virtue of analysis of intercentral, including hemispheric interactions during motor imagery [4–6] and real movements [7, 8]. Comparative analysis of electroencephalogram (EEG) in right- and left-handers is an important instrument for studying this aspect of FHA, revealing the peculiarities of central regulatory mechanisms of movements in people with different motor dominance profiles [7].

EEG patterns of imaginary and real movements have mostly been studied for hands. The main markers of cortical activity in these cases are synchronization or desynchronization of α-rhythm [9, 10]; moreover, motor imagery is normally associated with the reduction of µ-rhythm in the α-band registered in sensorimotor areas of the cerebral cortex [11]. Imaginary movements of right and left hands induce contralateral desynchronization of µ-rhythm and its ipsilateral synchronization in right-handers [12]. On the contrary, cophasal changes of α-wave coherence registered from right and left sides in left-handers, suggest the predominance of hemispheric interaction. Meanwhile, real movements show the dependence of increase or decrease of EEG rhythm coherence in different frequency ranges from operation with dominant or non-dominant hand in right- and left-handers [7]. Regarding EEG dynamics in imaginary and real leg movements, there are few studies where FHA is discussed only briefly [13, 14].

Performance of motor tasks affects the vegetative status of organisms reflected in changes of heart rate variability (HRV). During movements certain HRV parameters (SDNN and RMSSD) decline, where as the dynamics of spectral heart rate characteristics demonstrates the increase in the amount of HF waves, reduction of the LF component, and index of vagosympathetic interaction [15]. Certain autonomic responses should be expected during motor imagery, since it is based on the synthesis of mental equivalent for motor action, a typical cognitive activity [14, 16], different types of which are accompanied by changes in HRV [17–19]. Certain studies found functional significance of the α-rhythm in the regulation of cognitive processes and correlations between patterns of α‑activity and HRV [20–22]. It was shown that changes in hemispheric coherence of α-rhythm are consistent with the dynamics of RR intervals and spectral parameters of HRV at different stages of cognitive activity, reflecting the activity of autonomic nervous system divisions [20]. Substantially less attention has been paid to the connections between HRV and EEG during motor imagery. Some data suggest the existence of correlations between the activity of mechanisms of cardiac regulation and EEG changes in central leads when imagining hand movements [12]. Deceleration of heart rate (HR) and concomitant pericentral EEG desynchronization was found during planning of and preparation for leg movements [23]. However, the problem of correlation between HRV and EEG during imagining and performing leg movements in people with different motor dominance profiles is still unsolved. However, its elaboration is important for the development of ideas about voluntary movement regulation and understanding of autonomic adaptation mechanisms for motor loads in right- and left-handers, as well as for solving applied problems in the development of brain computer interfaces.

The purpose of this study was to analyze the changes in spectral power (SP) of the α-rhythm and HRV parameters and to identify their correlations during imaginary and real leg movements in right- and left-handers.

METHODS

The study comprised 26 right-handers and 22 left-handers aged 18–23 years. The individual profile of motor dominance was estimated referring to the results of handedness and footedness tests [1, 7]. EEG and HRV were recorded in the resting state and during motor task performance involving imaginary and real ankle flexion and extension. Subjects were situated in a comfortable armchair in a dark soundproof room and kept their eyes closed throughout the experiment. Motor tasks were performed in the following order: real right foot movement, real left foot movement, imaginary right foot movement, and imaginary left foot movement.

EEG was recorded with an NVX 36 digital DC EEGN eurovisor (Russia). Electrodes were located on the head according to the 10–20 system. The electrodes were fixated with the help of an EEG cap, the reference electrode (linked ear reference) was placed on the right earlobe. At first the resting state EEG was recorded for 1 min. Then, a verbal instruction was given to perform a motor task (e.g., “bend the right ankle”). The instruction “extend the ankle” followed after 3 s. Such a script was applied for all tasks with intervals of 10 s. Considering the importance of α-rhythm in movement performance [10, 12], we collated the EEG wave patterns of the α-band (8–13 Hz) in symmetrical frontal (Fp1–Fp2, F7–F8), central (С3–С4), parietal (Р3–Р4), and occipital (О1–О2) leads. EEG signals were enhanced, filtered using a low pass filter of 100 Hz, and digitalized at a sampling rate of 250 Hz using Neurocortex-C version 2.10 software (Russia). The SP of the α-rhythm (µV2) was analyzedat rest and during motor task implementation.

HRV parameters were registered with ELOKS-01S2 (Russia) hardware using a photo-optical sensor placed on the left index finger. Rhythmograms were recorded for 5 min at rest and during real and imaginary movements. Each task was performed by the subjects upon researcher’s command and repeated every 15 s throughout the above mentioned time period. The following statistical and diagnostic parameters of HRV were evaluated: HR (bpm), coefficients of sympathetic (SIM, c.u.) and parasympathetic (PAR, c.u.) activities, and Baevsky stress index (IB, c.u.). Spectral analysis of HRV was conducted in reference to the total SP of heart rhythm fluctuations (Total, ms2), SP within very low (VLF, ms2), low (LF, ms2), and high (HF, ms2) frequency range and index of centralization (IC, c.u.) [24].

Statistical analysis of the results was performed using the SigmaPlot 12.5 software package (Systat Incorporated, United States). The normality of sample distribution was estimate dusing the Shapiro–Wilk test. Normally distributed data are presented as mean (M) ± standard error (m) and difference of means (D) ± standard error of difference (mD). Non-normally distributed data are presented as median (Me) and interquartile interval (P25–P75). The significance of differences was determined in Student, Wilcoxon, and Mann–Whitney tests. Spearman correlation coefficient (r) was used todefined correlation. Statistical differences were considered with p < 0.05.

RESULTS

Frontal F7 and F8 leads are particularly intriguing because EEG correlates with real and imaginary movements depending on FHA, where the desynchronization of the α-rhythm was the strongest of all cortical areas in both right- and left-handers. In right-handers the SP of α-waves in F7 reduced during all motions compared to resting state on average by 6.8 ± 1.8 µV2 (p < 0.05).The reduction of SP occurred in F8 only during the imaginary left leg movements and real right leg movements on average by 5.1 ± 1.2 µV2 (p < 0.05). Hemispheric asymmetry of the α-rhythm in F7–F8 is noteworthy. In right-handers (Fig. 1a) background SP on the left (F7) was 26.7% higher (p < 0.05) than on the right (F8). Regarding the imaginary movements of the dominant leg, asymmetry was preserved by left-lateral pre dominance of SP by 30.9% (p < 0.05). Performance of other tasks was associated with smoothing of α-wave asymmetry in right-handers due to prevailing desynchronization on the left (F7). At rest α-rhythm asymmetry in F7−F8 also manifested as left-lateral SP predominance in left-handers (by 30.8%; p < 0.05). SP of α-rhythm reduced similarly in F7 and F8 during imaginary and real leg movements of left-handers unlike right-handers, averagely by 4.6 ± 1.6 µV2 (p < 0.05) from the resting level, therefore the hemispheric differences preserved (Fig. 1b).

Fig. 1.
figure 1

Hemispheric differences in spectral power (SP) of frontal α-rhythm in right (a) and left-handers (b): (1) left-lateral leads; (2) right-lateral leads; IRM and ILM, imaginary right and left leg movements; RRM and RLM, real right and left leg movements; * p < 0.05, ** p < 0.01, significance of differences compared to resting state; # p < 0.05, ## p < 0.01, significance of interhemispheric differences.

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Another picture was registered in anterior frontal EEG leads. Particularly, the background asymmetry of α-waves between Fp1 and Fp2 was not seen in subjects. The SP of the α-rhythm in right-handers decreased during motor imagery for the non-dominant leg, specifically by 7.8 ± 1.5 µV2 in Fp1 and 5.9 ± 1.3 µV2 in Fp2 (p < 0.01) compared to resting state, thus leading to the right-lateral predominance of α-waves (Fig. 1a). During real movement with the dominant leg the EEG of right-handers was characterized by symmetrical decline of SP on average by 7.6 ± 1.8 µV2 (p < 0.01). The SP of the α-rhythm of left-handers reduced equally in Fp1 and Fp2 during all tasks on average by 4.7 ± 0.9 µV2 (p < 0.05) from the resting level. Therefore, no hemispheric EEG differences were seen in this range (Fig. 1b).

SP changes of the α-rhythm were similar in central (С3, С4), parietal (P3, P4), and occipital (О1, О2) leads of right-handers performing imaginary or real movements with the right and left legs (Table 1). For left-handers more prominent responses were detected in mental tasks. For example, the SP of the α-rhythm in С3, С4, and О2 decreased during imaginary movement of the dominant leg stronger, than during real movement by 8.4, 8.6, and 21.0%, respectively. As for the hemispheric differences, asymmetry of the α-rhythm was established in O1–O2 during real right leg movement in right-handers by means of right-lateral SP predominance, whereas in left-handers the SP of the α-rhythm distributed asymmetrically in P3–P4 at rest, prevailing on the left (Table 1).

Table 1.   Spectral power of α-rhythm (µV2) in central, parietal, and occipital leads in right- and left-handers during motor task performance
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The relation of the EEG pattern with a motor dominance profile in the process of motion was confirmed by the results of intergroup comparison between absolute SP values of the α-rhythm in right- and left-handers. It was found that a higher SP level of the α‑rhythm was seen in right-handers during motor imagery, particularly, in F7 and C3 leads for the dominant leg and O1 and O2 for the non-dominant one. In most EEG leads in left-handers the α-rhythm was predominant during real movements especially with the non-dominant leg (Fig. 2).

Fig. 2.
figure 2

Differences in spectral power (SP) of the α-rhythm (µV2) in right- and left-handers performing motor tasks. (1) Right-handers; (2) left-handers; IRM and ILM, imaginary right and left leg movements; RRM and RLM, real right and left leg movements; * p < 0.05, ** p < 0.01, significance of intergroup differences.

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Investigation of the HRV dynamics in motor tasks also discovered the presence of certain differences between subjects with various FHA types. For instance, the increase in HR values was typical for right-handers performing real movements by both right and left legs on average by 13.9% (p < 0.05) from the initial level (58.7 (56.3–63.1) bpm). On the contrary, in left-handers the growth of HR occurred during imaginary leg movements on average by 12.3% (p < 0.05) from the initial value (57.9 (55.8–65.1) bpm). This corresponded with the dynamics of SIM, equaling 3.0 (1.8–4.0) and 2.0 (1.8–2.3) c.u. in left-handers, respectively, which was 3 and 2 times (p < 0.05) higher than SIM of right-handers. This difference was probably related to the differences in activation of autonomic mechanisms during motor task implementation.

This conclusion was supported by the changes in PAR and IB (Fig. 3). Thus, PAR changed only in left-handers, being reduced by 38.0 and 19.7% (p < 0.05) from the background (19.0 (15.0–21.8) c.u.) during imaginary movement of the right and real movement of the left leg, respectively. Changes in IB observed in right- and left-handers during imaginary movement of the non-dominant leg were differently directed. In right-handers IB decreased during imaginary movement of the left leg by 20.5% (p < 0.01), whereas in left-handers it increased in the same movement of the right leg by 56.1% (p < 0.05), suggesting different tension of regulatory systems in left- and right-brain individuals. This was also shown in the results of spectral HRV analysis, identifying statistical differences only in left-brain subjects in the form of reduction of LF component of 9545 (6021–9882) ms2 at rest up to 5358 (3449–5744) ms2 during real dominant leg movement (p < 0.05).

Fig. 3.
figure 3

Changes of PAR and IB values in right- and left-handers performing motor tasks: (a) (dark boxes), right-handers; (b) (light boxes), left-handers (box represents median as a line inside box, quartiles as upper and lower sides of the box, 10th and 90th percentiles as lower and upper boundaries of whiskers); IRM and ILM, imaginary right and left leg movements; RRM and RLM, real right and left leg movements; * p < 0.05, ** p < 0.01, significance of differences compared to resting state.

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We studied the correlations of α-rhythm SP with HRV parameters to assess the interaction of central movement regulation and mechanisms of its vegetative support in subjects with different FHA types. It was found that SP of α-waves at rest positively correlated (p < 0.05) with VLF and negatively correlated with LF, TP, and IC (p < 0.05) in all leads of right-handers. In left-handers at rest, positive correlations (p < 0.05) of α-waves with HF, TP, and PAR were observed in frontal leads, whereas negative correlations (p < 0.05) were seen with SIM, IB, and IC. HRV correlated with α-rhythm in the majority of EEG leads during both imaginary and real leg movements of right-handers, whereas in left-handers HRV was predominantly connected with SP of the frontal α-rhythm. It should be noted that more prominent correlations established during imaginary movements, quantitatively prevailing during dominant leg movement in right-handers, while in left-handers the amount of connections during imaginary movements was nearly identical for imaginary movements of both legs (Table 2).

Table 2.   Coefficients of correlation (r) between HRV parameters and SP of α-rhythm in different leads of right- and left-handers during motor imagery
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DISCUSSION

The results suggest that α-rhythm desynchronization is a typical response to imagery and performance of leg movements, prevailing in frontal and central cortical regions, consistent with the reports on activation of the identical neural networks during real and imaginary movements [25]. It is thought that the initiation of voluntary movement and its execution begin from the excitation of the prefrontal cortex, spreading to primary motor and sensorimotor areas [26]. The involvement of frontal regions in motor imagery can originate from the modulating influence of premotor zones on efferent signals from the primary motor cortex [27]. Desynchronization or synchronization of α‑rhythm in central C3–C4 leads is considered as the key parameter of cognitive and motor activity of humans [12, 14, 28]; furthermore, the desynchronization of frontal and central α-rhythm might be connected with activation of the motivational system and intensification of attention [22].

In the present study the EEG of subjects with different FHA types showed a reduction of SP in the central α-rhythm during real and imaginary movements of both legs; however, a lower SP level in the C3 lead was detected in left-handers using the left leg than in the right-handers. Low power of the α-rhythm in the left central area corresponds to a high level of anxiety [22], typical for people with a dominating right hemisphere [2, 29, 30]. From the perspective of FHA it is also important to emphasize different severity of changes in the α-rhythm in symmetrical frontal F7 and F8 leads during motor tasks in left-hemispheric subjects and similar severity in right-hemispheric individuals. This observation corresponds to the concept of more labile mechanisms of brain activity of right-handers than left-handers, allowing them to quickly adapt for changing conditions [7, 31]. Interestingly, that in right-handers the reduction of α-rhythm SP in Fp1, Fp2, F7, and F8 leads predominated during real dominant leg movements, overall corresponding to the results of other studies [9]. In left-handers such a reaction predominated during imaginary dominant leg movements and was more commonly seen in C3 and C4 leads. Non-dominant leg movements were associated with more expressed suppression of α-waves in the frontal EEG leads during motor imagery of right-handers, whereas in left-handers the effects of imaginary and real movements with the non-dominant leg manifested with equal levels of desynchronization throughout the cortex. These data indicate zonality of activity of neural networks participating in the formation of motor patterns, preparation for movement, and its execution in people with different types of FHA. Referring to the concept of a dynamic neural network providing imaginary movements [4] and results of our previous studies [31], it can be concluded that this neural network might be connected with motor and premotor cortices more closely in right-handers than in left-handers.

Parieto-occipital cortex also contributes to the motor regulation at the stages of preparation for movement and its performance [26] due to the necessity for construction of perceptive models of movement, especially during motor imagery [5]. In our study the involvement of parietal and occipital areas in imagination and execution of leg movements was shown in the reduction of α-rhythm SP in Р3, Р4, О1, and О2 leads of all subjects. However, in the О2 lead of left-handers this effect was only seen during imaginary dominant leg movement, which might be associated with sensory modality forming movement or its image, according to the literature data [32]. For example, reduction of α‑waves in parieto-occipital areas is explained by predominantly visual type of imagination [10], potentially more expressed in studied left- rather than right-handers. Overall, the detection of specific differences in EEG patterns during right and left leg movements requires further investigation and what is more, many authors report the associated similarity of cortical activation [12].

During imagination and execution of leg movements the FHA type did not only affect the EEG pattern, but also HRV parameters, their changes specific for right- and left-handers. For instance, HR values increased during real movements of right-handers and during imaginary movements of left-handers, which we explain by the peculiarities of regulatory mechanism activation. HR is known to increase during physical and mental loads and psychological stress [15]. Elevation of the HR is also considered a sign of concentration on the performance of goal-directed activity, whereas its reduction is considered a cardiac component of orientation reflex [33] accompanying goal-directed action. Referring to this it can be proposed that the exertion of cardiac regulation mechanisms during real movement is higher in right-handers and is associated with higher degree of psychological tension and concentration on the performed movement. Imaginary leg movements obviously provoke larger exertion of autonomic mechanisms in left-handers, additionally demonstrated by the reduction of PAR and increase of IB in them, probably due to high emotionality and sensitivity to stress of right-brain persons [7].

The ideas about peculiarities in vegetative support of motor actions of right- and left-handers are sustained by the results of correlation analysis for the α‑rhythm and HRV, appearing both similar and different in people with different types of motor asymmetry. Thus, the correlation between desynchronization of the α-rhythm and growing IC was a substantial common sign of right- and left-handers during movement performance, reflecting the predominance of central contour of cardiac regulation over autonomic one [24]. However, strong negative correlations were seen between α-rhythm, SIM, and IB of left-handers, unlike right-handers, probably ensuing from stronger activation of central regulatory contour of the sinoatrial node during motor acts of people with right-hemispheric domination, referring to the opinion [34]. The intergroup differences also affected the dynamics of positive correlations between the α‑rhythm and HRV, their amount prevailing during motor imagery and real leg movements of left-handers. Based on the discovered regularities, it can be assumed that there are differences in dynamic interaction between motion regulation mechanisms and HR in right- and left-handers during imaginary and real leg movements.

CONCLUSIONS

To summarize, movement control implies different severity of involvement of cortical neural networks and mechanisms of autonomic regulation of heart rhythm in the processes of imagination and leg movement in people with right and left motor dominance profiles. More labile type of EEG changes and stable autonomic status of organism were typical for right-handers, probably allowing them to quickly and easily adapt for the reorganization of motor programs . Imagination and execution of leg movements induced prominent desynchronization of α-rhythm in left-handers, predominantly focusing in the frontal and central brain areas, combined with substantial growth of exertion of autonomic mechanisms. Discovered interaction between the dynamics of α-wave SP and HRV parameters in right- and left-handers reflected the peculiarities of interaction of voluntary movement control and brain areas participating in the autonomic support of leg movements in people with different types of motor dominance profiles. Obviously, left-handers have the strongest connections of cerebral cortex with structures responsible for sympathetic control over visceral functions, determining larger activation of central contour of heart rhythm regulation in them than in right-handers during the execution and especially imagination of leg movements.