Application of neurofeedback for correction of cognitive and psychoemotional disorders after stroke

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INTRODUCTION

Modern methods of rehabilitation, including the various technologies of physical therapy, of logopedic correction and psychological counseling, do not always provide the complete restoration of the lost functions, due to which, a search of new rehabilitation methods still continues. One of them — the neurofeedback (the biological feedback) — represents a method of self-regulation by means of visual perception of graphic images (graphics, animation, sound) of the bioelectrical activity of the brain (electroencephalogram), which allows the patient to learn to control the activity of his own brain. This approach is being widely researched both in the international and in the national practice.

The development of the neurofeedback (NF) was contributed by the emergence of modern mobile devices and applications, which allow for arranging the brain training sessions outside the clinical settings, by this increasing the method availability [1–3]. The main goal of NF is the stimulation of processes, which help restoring the lost functions of the brain. The principle of therapy is based on creating the specific signals that are perceived by the patient, by which the patient is consecutively and targetedly modifying his own brain rhythms.

There are several protocols of arranging the neurofeedback sessions, each of which is aimed at solving a specific task: training the sensory-motor rhythm; the alpha and beta training.

One of the popular strategies is the sensory-motor rhythm training. This protocol is aimed at increasing the sensory-motor rhythm falling within the frequency range of 12–15 Hz. Training the specific rhythms promotes to the re-organization of neuronal networks and to the formation of new functional links in the areas that are damaged after a stroke. The research findings show an increase in the density of neural links in the trained zones after the NF course, which helps the patients in restoring the emotion control and in decreasing the muscle spasticity [4].

The alpha range (approximately 8–12 Hz) is recorded at the state of relaxation and calmness. The increase in the amplitude of alpha waves promotes to decreasing the anxiety and the tension, also increasing the attention span. The alpha protocol is effective in decreasing the tiredness and anxiety characteristic for many patients with a history of stroke, which demonstrate the activity imbalance between the affected and the intact hemispheres [5].

The increased beta range activity (13–30 Hz) is associated with high attention focusing and with the thinking processes. The improvement of the beta range parameters is associated with the acceleration in the processes of restoring the cognitive capabilities, required for everyday activities, such as the orientation in time and space, solving simple arithmetic tasks and memorizing new information [6].

The large-scale implementation of neurofeedback for the correction of psychoemotional and cognitive disorders after stroke is limited by the small number of research works for the last 10 years, with this, the accumulated experience confirms the significant therapeutic benefit.

Our research includes the analysis of the modern state of scientific research works and practical developments in the field of neurofeedback and the data on their efficiency in correcting the neuropsychological impairments after stroke; the drawbacks and benefits were shown for various protocols with examining the tendencies and perspective of implementing this technology in the rehabilitation practice.

Search Methodology

The review includes the full-text scientific articles published during the period from 2010 until 2025. The majority of research works had a pre-post design, with the two research works being the randomized controlled trials. The sample size varied from 15 to 100 patients. The neurofeedback session duration was 30–40 minutes with the number of sessions ranging from 10 to 30. In all the cases, the standard equipment set was used for the registration and for displaying the electroencephalography signals. The primary outcomes were evaluated using the standardized scales: the Mini-Mental State Examination (MMSE), the Montreal Cognitive Assessment (MoCA), the Hamilton Depression Rating Scale (HDRS), the generic quality of life questionnaire (Short Form-36, SF-36) and the the Fugl-Meyer Assessment scale for motor function evaluation (the Fugl-Meyer Assessment, FMA).

NEUROFEEDBACK SESSION PROTOCOLS: TENDENCIES AND PERSPECTIVES OF IMPLEMENTING IT INTO THE REHABILITATION PRACTICE

SMR-neurofeedback (SMR-training) for the correction of psychoemotional and cognitive disorders after stroke

The training of slow waves (sensorimotor rhythm (SMR) training) is aimed at the increased activity in the 12–15 Hz range, which is related to the sensory-motor cortex in the brain. This technique is used for improving the motor functions, for decreasing the anxiety and for increasing the attention span. The majority of presented research works were showing the positive effect of sensorimotor rhythm (SMR) training in terms of the cognitive state and the emotional aspects in stroke patients. Thus, the research by М.N. Puzin et al. [7] has found a decrease in the anxiety levels in patients after the SMR-training course, also reporting the significant improvement of the executive function, of spatial perception and of the total mood after the neurofeedback course. The authors came to the conclusion that this method increases neuroplasticity and stimulates the compensatory processes. The described effects were persisting for a long-term period, which is also confirmed by the results of follow-up period. For example, in patients participating in the neurofeedback program, after 6 months there was a persisting stable improvement of the cognitive parameters and of the emotional background. The research by Y. Huang [8] reports the improvement of the cognitive functions in patients with hemiplegia after stroke. Nevertheless, separate research works demonstrate the variability of the patient response to therapy.

Along with multiple confirmations of the SMR-protocol efficiency, there are also the critical views regarding the scientific justification of such research. Serious methodоlogical errors were noted when evaluating the SMR-NF results: small sample size, absence of proper placebo-control, non-conformity to the criteria of evidence-based medicine [9]. The emphasized aspects were the complexity of interpreting the SMR-NF-training results due to the inhomogeneity of patients’ samples and due to the diversity of the technological conditions when arranging the research works [10]. Such disagreements can also be found in the national scientific community. Despite the available encouraging results of using the SMR-protocol in the post-stroke rehabilitation process, P.V. Bykovskiy et al. [11] have expressed doubt that the accumulated data are sufficient for acknowledging the SMR-protocol as a multi-purpose rehabilitation method. The authors have pointed out the small number of patients in the samples and the absence of adequate placebo-groups, which complicates the determination of the true role of neurofeedback in the rehabilitation processes.

Based on the data obtained from the published research, it can be suggested that the effects of NF depended on the severity degree of the initial brain damage, on the age of the patient and on the concomitant diseases, due to which, the personalized approach is deemed the necessary prerequisite for the successful application of NF. It worth noting that none of the analyzed research works has shown the significant adverse effects or negative reactions in the organism in response to the SMR-training. Regular NF training sessions stimulate the re-organization of the neuronal links, increase the adaptivity of the damaged brain areas and improve the inter-hemispheric interactions. The important issue remaining is selecting the optimal number of sessions and the duration of a single session. It was found that the small number of sessions (up to 10) is insufficiently effective, but also the excessively long course (more than 30 sessions) did not show any additional benefits. The optimal number is considered the course of 20–25 sessions with a total duration of approximately 30 minutes each. Another problem is the complexity of the interpretation in separate cases. The individual differences in patient reactions make it difficult to compile the universal recommendations on arranging the NF.

Summing up the results, it can be stated that the majority of investigators see huge perspectives in using the SMR-protocol, considering it a reliable tool in restoring the motor and the cognitive functions. Further investigation on the topic requires arranging the large-scale international research with following the principles of evidence-based medicine, which could allow for definitely determining the role of SMR-protocol in the rehabilitation of the stroke patients and for compiling the unified standards of using the NF.

Alpha neurofeedback (alpha training) for the correction of psychoemotional and cognitive disorders after stroke

One of the most widespread NF protocols is the alpha training associated with the frequency of brain waves within a range of 8–12 Hz, which prevail at the state of relaxation and rest. In the analyzed research works, the neurofeedback procedures were arranged daily or three times a week and the total duration of each session varied from 20 to 45 minutes with the number of sessions ranging from 10 to 40. The evaluation of the efficiency was done using the standardized instruments: the Mini-Mental State Examination (MMSE), the Beck Depression Inventory (BDI), the Spielberger’s State-Trait Anxiety Inventory (STAI), the Barthel index of everyday life activity (Barthel Index, BI) and other widely acknowledged indexes.

The investigators have confirmed the positive effect of alpha training in terms of decreasing the anxiety and depressive symptoms in stroke patients: in particular, the participants completing the whole course of alpha training were reporting the significant improvement of the emotional state and the increased vitality [12]. Similar results were obtained by the American specialists, showing that alpha training helps stabilizing the emotional background and decreases the intensity of negative emotions, which is of special value for the elderly individuals [13]. S. Gupta [14] has shown that alpha NF promotes to the normalization of anxiety level and to the improvement of sleep quality in stroke patients. C. Chen et al. [15] have shown a significant decrease of fear and anxiety in patients experiencing the fear of disease recurrence. T. Renton et al. [16] have demonstrated the improvement of the working memory and attention after the alpha NF course.

Alongside with the reports of the positive results, multiple doubts exist regarding the efficiency of alpha training. Western investigators point out the difficulties in compiling the representative patient samples and the impossibility of arranging the double-blind trials, which seriously decreases the validity of the obtained data. In particular, a group of scientists came forward actively criticizing the method, stating that the provided research works are based on small groups of test subjects without taking into account the most important factors, such as the duration of the disease and the severity of brain damage [17]. The experts note that the efficiency of alpha training depends on multiple variables, including the eagerness of the patient to cooperate, his compliance regarding the prescribed treatment scheme, as well as the competency of the medical staff. T.A. Suhail et al. [18] have reported about the mild changes in the cognitive parameters or the insignificant mood improvement after using the alpha training. Such discrepancies could be explained by various severity of brain damage, by the inhomogeneity of the population of patients and by various therapy settings. All the research works were emphasizing the safety of alpha training. No serious adverse events were registered.

The materials provided confirm the suggestions that alpha training can beneficially effect the restoration of the cognitive and the emotional functions after stroke. It is necessary to improve the methods of evaluating the results, to more clearly formulate the patient inclusion criteria and to compile the specialized standards of providing the services. The uncertainty factor in the results from some research works can indicate the necessity of differentiated approach to selecting the groups of patients, which indeed can benefit from alpha training. Future research could be focused on searching the criteria helping to find the patients that are more susceptible for such a type of therapy. The additional benefits of alpha training include the low cost and the relative simplicity of implementing it in the settings of an in-patient unit or in the out-patient facility.

According to the conclusions drawn by the majority of authors in the analyzed literature sources, it can be stated that alpha training is potentially useful, but its application must be followed by using the strict criteria for selecting the patients, by the conduction of preparation stages and by the obligatory monitoring of the patient status during the treatment. Further research works are needed for the purpose of verifying the indications and the contraindications, for developing the personalized NF programs and for implementing the better experience into the wide medical practice. It can be concluded that alpha NF represents a safe and potentially efficient method for improving the emotional state and the cognitive functions in patients with a history of stroke.

Beta neurofeedback (beta training) for the correction of psychoemotional and cognitive disorders after stroke

Special attention is paid to beta training related to the increase in the activity at the range of high frequencies (16–30 Hz), which are traditionally associated with the state of activity and increased attention. Authors emphasize the importance of individual approach to selecting the NF modes. For example, J.H. Gruzelier [19] has investigated the long-term effects of beta training on the cognitive functioning and the emotional wellness among the elderly individuals with reporting a noticeable decrease in the manifestations of depression and fatigue, which confirms the usefulness of this method in cognitive rehabilitation. Е.V. Kostenko et al. [20] have demonstrated the decreased anxiety and depression levels after a course of beta NF. W. Nan et al. [21] have published a research work confirming the efficiency of NF combined with traditional treatment modalities in stroke patients. The researchers have found that NF positively affects the parameters of attention and memory. Y. Lee et al. [22] have performed the comparative research on the NF and the traditional medication therapy in patients with cognitive disorders after stroke. The analysis has shown the benefits of NF comparing to the standard pharmacological therapy in the aspect of decreasing the severity of depressive and anxiety disorders. M. Ulanov et al. [23] have found an interrelation between the changes in the levels of brain β-activity and the degree of restoring the cognitive functions in patients with speech disorders after stroke. International research works show the high efficiency of NF, including the beta training, in restoring the cognitive and the emotional functions in patients after a stroke.

The obtained results have confirmed the high efficiency of the integrated approach, allowing for achieving the significant progress in restoring the intellectual and mnestic functions. Nevertheless, domestic research works are still insufficiently large, and the most part of the publications is represented by separate clinical cases or by small patient samples, which limits the possibility of summarizing the conclusions drawn. А.L. Kulik et al. [24] have compared the traditional method of rehabilitation to the beta training, noting the significant superiority of the latter in terms of improving the visual-spatial orientation and the verbal memory.

Some research works call into question the unambiguousness of the positive effects of beta NF. Thus, M. Schönenberg et al. [25] have suggested that the mechanisms of the efficiency depend not only on the changes in the brain activity, but rather on the expectations and on the motivation of the patients themselves, that the significant part of the effect can be resulting from the placebo component and from the expectations of the patients. The critics of the method point out a whole number of disadvantages and limitations. The Australian specialists have questioned the efficiency of early research, showing the low quality of experimental design and small samples of participants [26]. Besides, the Iranian scientists have reported about the issues of the method tolerability: the part of the patients had complaints of discomfort and fatigability during the training sessions, which prevented them from achieving good results [27]. It was reported that the age-related changes within the brain structure make the patients that are older than 65, more susceptible to such reactions, which reduces to nothing the suggested benefits of the method. The German scientists have suggested that the effect of beta training is caused by the placebo effect. The control experiments have demonstrated similar results in groups of patients participating in the “fake” sessions, and in those receiving the real beta training [28]. The age-related factors (patients older than 65 years) can decrease the efficiency of beta training due to the age-related changes within the brain structure, due to which it is necessary to take into account the individual specific features of the patients and the possible adverse effects, such as the overexcitation of the nervous system [29]. The insufficiency of understanding the fundamental mechanisms of the method was emphasized, which complicates its practical application. Some specialists consider that the real benefit of the method is achievable only when combining it with the classic rehabilitation. With no additional correction of the physical activity, of the nutrition and social factors, it is difficult to expect the complete restoration of the cognitive and emotional functions after stroke [30].

Thus, the majority of authors considers that the practical application of NF must become the integral component of the standard rehabilitation programs after stroke. For this, it is necessary to compile the corresponding guidelines and instructions providing the uniformity of the approaches to diagnostics and treatment. Based on the results of analyzing the accessible scientific literature, it becomes evident that the issue of the efficiency of beta training remains disputable. The followers of the method assure that it can significantly accelerate the rehabilitation after stroke, strengthening the cognitive functions and the emotional stability. The critics, on the contrary, suggest that the current body of evidence is insufficient for wide implementation, emphasizing the lack of reliable data and of understanding the basics of the mechanism of action. Probably, the optimal way is the combination of beta training with the classic approaches to rehabilitation with taking into account the individual specific features of each patient (age, motivation etc.). In future, the continuation is expected for the developments aimed at improving the NF methods, at the adaptation of individual programs and at compiling the multi-purpose protocols for the maximal coverage of patients.

Combined neurofeedback protocols (alpha, beta and SMR-rhythms) for the correction of cognitive and emotional disorders after stroke

The group of European researchers in their large-scale research published in the “Life” journal, have found that the combined use of alpha, beta and SMR-protocols lead to a significant improvement in as many as several aspects of cognitive functions — memory, attention and voluntary control [31]. The participants completing the full rehabilitation program with using the complex protocols have demonstrated the better dynamic changes in their rehabilitation comparing to the participants from the control group. The American specialists have also confirmed the efficiency of the combined usage of various NF protocols. After examining the results of the 12-week course of combined training (combined use of alpha, beta and SMR-protocols) in stroke patients, the authors came to the conclusion that the combination of protocols results in the significant activation of the prefrontal cortex and of the temporal regions in the brain, which promotes to the improvement of communication skills and of processing the complex information [32]. Another important aspect is the insufficiency of data on the long-term effect of such a therapy. As reported by the German researchers, it is not clear whether the positive changes after the completion of the NF program persist or they resolve soon after the discontinuation of training sessions [28, 34].

The combined approach to NF (using the alpha, the beta and the SMR-protocols) has gained its acknowledgement both in the Western and in the domestic science, however, the evaluation of its efficiency and safety remains questionable. There is a sufficient body of data confirming the efficiency of combined training in restoring the cognitive and the psychoemotional functions after stroke.

Critical analysis of neurofeedback efficiency

Despite the promising results, the usage of NF in the rehabilitation after stroke faces a number of substantial limitations, among which are the following:

• methodоlogical downsides of the research works (the majority of works are carried out using small samples — less than 30 patients; absence of adequate placebo-groups and blinded trials, which complicates the objective evaluation of the efficiency [9, 25]);
• heterogeneity of the protocols (no standardization regarding the session duration, number of sessions, target frequencies and electrode configuration, which makes it impossible to directly compare the results from various research works [12, 20]);
• the problem of effect specificity (the significant part of the effect can be resulting from the placebo-component and from the expectations in the patients, but not the direct changes in the brain activity [26]);
• individual variability of the response (such factors as the age [the patients older than 65 years tolerate the training sessions in a much worse manner], the severity of stroke and the time of initiating the rehabilitation, significantly affecting the efficiency of NF [13, 30]);
• insufficient exploration degree of the long-term effects (the majority of research works have a follow-up period of not more than 6 months, which is not enough for the evaluation of stability of the results achieved [18, 19]);
• technical and the organizational limitations (the high equipment costs, the necessity for special training of personnel, the absence of unified protocols of arranging the procedure [20, 35]).

CONCLUSION

Thus, the biological feedback methods (the neurofeedback) demonstrate the significant potential in the correction of cognitive and psychoemotional disorders after stroke. The most effective protocols are the SMR-training sessions for improving the motor and the cognitive functioning, the alpha training for decreasing the anxiety and for improving the sleep quality, the beta training for restoring the attention and the executive functions. The efficiency of neurofeedback is determined by the individual approach to selecting the protocols, by taking into account the specific brain damage, by the time of initiating the rehabilitation and by the concomitant factors.

The main limitations of the wide usage of alpha, beta and SMR-training sessions are the methodоlogical drawbacks of the existing research works, the absence of standardized protocols and the insufficient exploration degree of the long-term effects. The most perspective strategy is deemed the integration of neurofeedback into the combined rehabilitation programs.

ADDITIONAL INFORMATION

Author contributions: M.G. Khlyustova, Yu.V. Mikadze, M.N. Gordeev, G.E. Ivanova, A.K. Dorozhkina, setting the concept, data operations, reviewing and editing the manuscript; M.G. Khlyustova, setting the concept, visualization, drafting the initial manuscript; Yu.V. Mikadze, M.N. Gordeev, G.E. Ivanova, validation, reviewing and editing the manuscript. Thereby, all authors provided approval of the version to be published and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Funding sources: The research was carried out as a part of the scientific research activities as set by the State assignment on the “Development and implementation of the mobile electroencephalography device with the biological feedback unit for the correction of cognitive and stress disorders”, Code: ENCEPH 25-26.

Disclosure of interests: The authors declare no conflict of interests.

Statement of originality: The authors did not utilize previously published information (text, illustrations, data) in conducting the research and creating this paper.

Data availability statement: The editorial policy regarding data sharing does not apply to this work, data can be published as open access.

Generative AI: Generative AI technologies were not used for this article creation.

About the authors

Maria G. Khlyustova

Federal Center of Brain Research and Neurotechnologies

Author for correspondence.
Email: khlyustova.maria@mail.ru
ORCID iD: 0009-0005-4477-6155
SPIN-code: 3653-9420
Russian Federation, Moscow

Yury V. Mikadze

Federal Center of Brain Research and Neurotechnologies; Lomonosov Moscow State University

Email: ymikadze@yandex.ru
ORCID iD: 0000-0001-8137-9611
SPIN-code: 7799-8969

PhD, Professor

Russian Federation, Moscow; Moscow

Mikhai N Gordeev

Federal Center of Brain Research and Neurotechnologies; Milton Erickson Moscow Institute of Psychology and Psychotherapy

Email: mngordeev@yandex.ru
ORCID iD: 0000-0002-5126-4132

MD, PhD, Professor

Russian Federation, Moscow; Moscow

Galina E. Ivanova

Federal Center of Brain Research and Neurotechnologies; The Russian National Research Medical University named after N.I. Pirogov

Email: reabilivanova@mail.ru
ORCID iD: 0000-0003-3180-5525
SPIN-code: 4049-4581

MD, PhD, Professor

Russian Federation, Moscow; Moscow

Alexandra K. Dorozhkina

Federal Center of Brain Research and Neurotechnologies

Email: trofimova@fccps.ru
ORCID iD: 0000-0001-6521-9503
SPIN-code: 2607-9136
Russian Federation, Moscow

References

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