The influence of vestibular training on dynamic visual acuity in primary school students with learning difficulties.

Efimova Viktoriya Leonidovna ORCID: 0000-0001-7029-9317 Doctor of Psychology Associate Professor of the Department of Developmental Psychology and Pedagogy of the Family, "Russian State Pedagogical University named after A.I. Herzen" 191186, Russia, Leningrad region, Saint Petersburg, nab. Moika River, 48 prefish@ya.ru Other publications by this author     Nikolaeva Elena Ivanovna ORCID: 0000-0001-8363-8496 Doctor of Biology Professor, Head of the Department of Age Pedagogy and Family Psychology "Russian State Pedagogical University named after A.I. Herzen" 191186, Russia, Leningrad region, Saint Petersburg, nab. Moika River, 48 klemtina@yandex.ru Other publications by this author     Buinov Leonid Gennad'evich ORCID: 0000-0002-6203-4324 Doctor of Medicine Professor, Department of Medical and Valeological Disciplines, Faculty of Life Sciences, Russian State Pedagogical University, Russian State Pedagogical University. A.I. Herzen 191186, Russia, Leningrad region, St. Petersburg, Moika River Embankment, 48 buynoff@yandex.ru Vergunov Evgenii Gennad'evich ORCID: 0000-0002-8352-5368 PhD in Psychology Senior Researcher, Laboratory of Body Functional Reserves, Research Institute of Neurosciences and Medicine 630117, Russia, Novosibirsk region, Novosibirsk, ul. Timakova, 4 vergounov@gmail.com Nikolaeva Natal'ya Olegovna ORCID: 0000-0002-2270-8320 PhD in Medicine Lecturer, Department of Developmental Psychology and Pedagogy of the Family, Russian State Pedagogical University. A.I. Herzen 191186, Russia, Leningrad region, Saint Petersburg, Moika River embankment, 48 nikolaeva.n.o@yandex.ru Khasnutdinova Antonina Leonidovna ORCID: 0009-0000-5628-3482 PhD in Psychology Assistant, Department of the Department of Developmental Psychology and Pedagogy of the Family, Russian State Pedagogical University. A.I. Herzen 191186, Russia, Leningrad region, St. Petersburg, Moika River Embankment, 48 ant.khasnutdinova@yandex.ru

Mazurova Irina Sergeevna ORCID: 0000-0001-5908-3216 Psychologist, Prognoz LLC 191014, Russia, Leningrad region, Saint Petersburg, 3 Paradnaya str., Building 2 irina.1998list.ru@yandex.ru Other publications by this author

The number of students with learning difficulties is increasing every year in all countries. In this regard, studies of the psychophysiological mechanisms underlying these difficulties are relevant.

In recent decades, the hypothesis has been confirmed that one of the causes of difficulties in mastering reading and writing in elementary school may be reduced sensory reactivity of the vestibular system. If earlier motor and cognitive processes were considered by science in isolation from each other, now the relationship between the development of the vestibular system and the cognitive development of children is shown ^{[6,7,14,15,22,26]}.

            There is evidence that a decrease in sensory reactivity of the vestibular system may be the cause of reading disorders in children ^[15].

At the time of birth, the vestibular system is one of the most functionally mature sensory systems, but its development continues throughout childhood under the influence of motor experience.  It is possible that the increase in the number of younger schoolchildren with learning difficulties and concomitant functional immaturity of the vestibular system, which has been noted by researchers in recent decades, is the result of a change in the lifestyle of modern children, whose motor activity is significantly lower than 20-30 years ago.

The vestibular system performs two functions that are closely related to the ability to learn: vestibulospinal: control of muscle tone, posture, gravitational confidence; and vestibulocular: compensatory movements of the eyeballs, during rapid movements of the head in space, ensuring the stability of the image on the retina.  Compensatory eye movements, in turn, provide the necessary dynamic visual acuity - the ability to clearly see objects in a situation when the head changes its position in space.

Features of vestibulocular functions have been studied to a greater extent in adults with various neurological disorders, such as Parkinson's disease, chronic cerebrovascular disorders, cerebellar tumors, etc. ^[1,10,11,12].

            The study of the relationship between the vestibular and visual systems in healthy people is relevant for aerospace medicine ^[9].

Studies of the features of the vestibulocular reflex in children are significantly less ^[2,3,13].

Since the vestibular system in children functionally mature much earlier than the cortical areas involved in the development of reading and writing, it is possible that classes with children with a combination of vestibular dysfunctions and learning difficulties, it is advisable to start with the normalization of sensory reactivity of the vestibular system, taking into account the results of the assessment of the vestibulocular reflex, the duration of post-rotational nystagmus and cervical vestibular potentials. 

This determined the goals of the work:

1.                  Study of dynamic visual acuity in children with learning difficulties

2.                  Evaluation of the possibility of using vestibular training to normalize dynamic acuity in such children.

3.                  Determination of prognostic capabilities of initial neurological diagnoses and instrumental diagnostic indicators in relation to the results of vestibular training.

MethodologyThe study involved 35 children aged 7-11 years with learning difficulties.

Criteria for inclusion in the group: the presence of difficulties in mastering reading and writing. Exclusion criteria: hearing impairment.

All study participants were consulted by a neurologist. Diagnoses were established: 2 children – F48 (other neurotic disorders), 13 children - F80.0 (specific disorder of speech articulation), 8 children - F80.1 (specific disorder of expressive speech), 8 - F81.0 (specific reading disorder), 1 child - F81.3(mixed disorder learning skills), 7 - F83 (mixed specific disorders of psychological development), 4 - F90.0 (impaired activity and attention), 1 - F90.1 (hyperkinetic behavior disorder), 3 - F95 (tics), 1 - F98.5 (stuttering), 1 - G91.1 (obstructive hydrocephalus), 3 - G93.4 (encephalopathy not specified), 2 - with G93.8 (other unspecified brain lesions), 1 - with Q85 (phacomatoses not classified elsewhere) and 4 children with astheno-neurotic syndrome. 

 Instrumental studies of the vestibular system were carried out according to the appointment of a neurologist, training was assigned based on the results of diagnosis.  The presence of a decrease in sensory reactivity of the vestibular system was established using instrumental studies. 

The functions of the otolith part of the vestibular apparatus were evaluated by the cVMVP method (Cervical vestibular evoked potentials). cVMVP was recorded on a neuromedifier Neuro-MVP-4 (Neurosoft, Ivanovo) in response to sound stimulation. The latency of the peak P13 of the cVMVP recorded at the time of the sacculocervical reflex on the side of the stimulus presentation (clicks) was evaluated.  Sound stimuli of 130 dB with a duration of 0.5 ms were presented using headsets.  Averaged from 4 to 20 VMVP in 5-15 series with subsequent superposition. During the study, the child sat in a chair with his head turned to the side as much as possible to cause tonic tension of the sternocleidomastoideus muscle. Then the study was repeated with the head turning in the opposite direction.

The functions of the horizontal channels of the vestibular apparatus were evaluated by measuring the duration of post-rotational nystagmus (PVN). Registration was carried out using a psychophysiological telemetry device "Reakor-T" manufactured by LLC NPKF "Medikom-MTD" (Taganrog) in the PMO "Encephalan-SA". The subject was located in a sitting position in a chair Barani. The head was installed in an inclined position forward at an angle of 30 degrees. The chair was rotated at a speed of 10 revolutions in 20 seconds, the eyes of the subject were closed. The chair was stopped and the duration of post-rotational nystagmus was assessed by recording an electrooculogram (EOG). The horizontal component of the EOG was recorded using two EOG leads (electrodes at the outer corners of the eyes).

The vestibulocular reflex was evaluated before and after vestibular training by measuring dynamic visual acuity (DOSES) using the standard Sivtsev table. Static visual acuity was assessed using a standard technique in sitting and standing positions. When assessing the doses, the subjects called letters, with simultaneous activation of the horizontal semicircular channels of the vestibular apparatus, for this purpose rapid low-amplitude movements of the head from side to side were performed. The assessment was carried out sitting and standing. Children with visual impairments were examined with glasses. The norm was the difference between static and dynamic visual acuity of no more than 1 row according to the Sivtsev table.

            Vestibular training based on biofeedback (BOS) was conducted on a Fortis riding simulator that accurately reproduces the movements of a horse.  The child was sitting astride a saddle on a life-size horse simulator, and controlled movements with the help of reins, solving visual game tasks on a large monitor screen and receiving visual feedback. The duration of the training is 15 days, daily classes of 20 minutes.

            Methods of data analysis.To build models, such a tool of the partial least squares method (PLS) was used

as 2B-PLS (Two-Block PLS) from the JACOBI 4 software package (Polunin 2019).

One block contains the measurement results after normalization for the scope (predictors), the other block contains the questions asked to the model (binary signs, responses). After that, simultaneous rotation of the blocks occurs, and the angle that gives the maximum covariance between the score matrices of both blocks after rotation is considered optimal for rotation. This is achieved by identifying the most contrasting subgroups of indicators.

Thus, 2B-PLS allows you to formulate questions that teach the model such a rotation angle that will give the most informative (maximum variance) answer to them. At the same time, the purpose of the model is to identify new orthogonal axes – independent latent structures (another name is 2B-PLS –Two-Block Projection to Latent Structure), which will be the mechanisms of the studied phenomena. The resulting mechanisms are described using load matrices (loadings) of both blocks and contain the rotation parameters of the source blocks (correlation coefficients between the source blocks and the account matrices), and the number of responses may be greater than the number of predictors, and all variables may have a close correlation (Rohlf 2000; R?nnar 1994).

2B-PLS models allow us to describe and study the influence of mechanisms by highlighting areas of interest (ROI, Regions of Interest) on graphs of variable loads. Latent structure analysis is widely used to study mechanisms in interdisciplinary research in recent years in the field of psychophysiology (Nikolaeva 2022; Krivoshchekov 2022), neuroscience (Savostyanov 2022), biology (Kovaleva 2019), psychology (Vergunov 2022), genetics (Polunin 2019).

Results The result of the multidimensional analysis was a 2B-PLS model, the blocks of which included (Table 1) predictors (7 normalized variables, Block 1) and a series of question signs (19 binary variables, block 2).

Accordingly, the 2B-PLS model describes 7 latent structures (a minimum of variables from both blocks), the same for both predictors and responses.

With the help of block 2 (responses), we set the rotation for block 1 (predictors) – we train him to find the most informative answers to the questions from block 2.

Table 1. Variable blocks for 2B-PLS

Notes: indicators with a "+" sign were included in the predictor block, and with a "-" sign were fictitiously built on graphs for the convenience of ROI analysis

As follows from the 2B-PLS scree graph (Fig. 1), 6 latent structures showed statistical significance. Structures 1 and 2 (the first segment of the graph) describe general features (almost 48.9% of the total variance), structures 3 and 4 (the second segment of the graph) describe particular specifics (almost 29.8% of the total variance), and structures 5 and 6 (part of the third segment of the graph) describe even more particular specifics (18.2% of the total variance). Below, according to the objectives of the study, ROI, which are formed by the effects of the vestibulocular reflex, will be considered.

Figure 1. Scree plot of latent structures 2B-PLS. Below the red dotted line – going beyond the border of statistical significance

According to Fig. 2, the ROI with reduced dynamic visual acuity in standing samples includes the diagnosis of F80.1 (specific disorder of expressive speech), while the ROI with normal dynamic visual acuity in standing samples does not have any factors controlled in the study. The ROI with reduced dynamic visual acuity in sitting tests includes a diagnosis of F98.5 (stuttering), and this is typical for the situation before the training (after the training, the situation may be arbitrary). The ROI with normal dynamic visual acuity in sitting tests initially includes the diagnosis of F90.0 (impaired activity and attention) and the symptoms of astheno-neurotic syndrome, which is characteristic of the situation after the training (before the training, the situation may be arbitrary). Thus, the situation described in Fig. 2 refers to the general features of the sample and shows that with the diagnosis of F90.0 (impaired activity and attention) and the symptoms of astheno-neurotic syndrome, normalization of dynamic visual acuity is observed in sitting samples after training.

Figure 2. ROI for loads 2B-PLS visualization for variables (structures 1 and 2). For symbols, see Table. 1. Red circles with equal radii show the boundaries of ROI with centers at the points of indicators of the vestibulocular reflex

A particular specificity that takes into account the symmetry of cervical vestibular evoked potentials and the severity of their asymmetry on the left, as well as the symmetry of the duration of post-rotational nystagmus, is given in the following ROI (Fig. 3):

- reduced dynamic visual acuity in standing tests accompanies the diagnosis of G 93.4 (encephalopathy is not specified), a decrease in the latency of the peak of cervical vestibular evoked potentials on the left up to the equality of indicators on the left and right;

- normative indicators of dynamic visual acuity in standing tests accompany the diagnosis of F81.0 (specific reading disorder), a decrease in the latency of the peak of cervical vestibular evoked potentials on the left and equality of the duration of post-rotational nystagmus on the left and right;

- impaired indicators of dynamic visual acuity in sitting tests accompany the diagnoses of F95 (tics), F80.1 (specific disorder of expressive speech), F98.5 (stuttering), G 91.1 (obstructive hydrocephalus), Q 85 (phacomatoses not classified elsewhere), which is typical for the situation before the training (after the training situation can be arbitrary).

- impaired indicators of dynamic visual acuity in sitting tests after the training accompany the initial diagnoses of F81.3 (mixed learning skills disorder) and G 93.8 (other unspecified brain lesions) (before the training, the situation may be arbitrary).

Figure 3. ROI for loads 2B-PLS visualization for variables (structures 3 and 4). The symbols correspond to those for Fig. 2

Discussion            

Our study allows us to conclude that in a group of children with certain neurological diagnoses, after vestibular training on a riding simulator, the indicators of dynamic visual acuity significantly improve. Individual prediction of the training results is difficult, since some subjects did not have an improvement in their indicators (but they did not worsen either).

            Indicators of dynamic acuity significantly improved in hyperactive and emaciated children, and in samples in a sitting position. The fact that dynamic visual acuity improves more often in a sitting position can be explained by the fact that the support area in this position is larger than standing. In a standing position, any person, even with a normally functioning vestibular system, makes small fluctuations in the body. In people with impaired vestibular reactivity, these fluctuations may manifest themselves more than necessary, or less. Therefore, the indicators of dynamic visual acuity in standing tests are associated with the results of evaluation of vestibular function by instrumental methods: cervical vestibular myogenic evoked potentials and evaluation of the duration of post-rotational nystagmus.       

Our study showed that the prognosis of the effectiveness of vestibular training on a riding simulator can be made, taking into account the diagnosis of the child, as well as the presence of asymmetry in the indicators of cervical vestibular myogenic evoked potentials and the duration of post-rotational nystagmus on the left and right.

The mechanism of dynamic visual acuity is associated with the fact that part of the impulses from the vestibular apparatus in the inner ear through the vestibular nuclei in the brain stem does not enter the cortex, but directly to the oculomotor muscles. This impulse initiates automatic compensatory eye movements, which allow the image to stay longer on the retina with rapid head movements, which creates optimal conditions for image processing by the visual areas of the cerebral cortex. The vestibulocular reflex, which is the result of the interaction of the vestibular and oculomotor systems, provides the ability to clearly see stationary and moving objects during head movements ^[27].

Since the child's head rarely remains completely motionless in real life, the insufficiency of compensatory eye movements can negatively affect the development of cognitive functions and hinder the full development of educational skills, in particular reading and writing.

Children with a violation of the vestibulocular reflex may experience unpleasant subjective sensations while reading and writing: letters or words on a sheet seem to move, change their position or become clouded. If a child informs his parents about this, they usually turn to an optometrist. But since the oculist evaluates visual acuity in static, in conditions when the vestibular system is not activated (motionless head), the insufficiency of the vestibulocular reflex is not detected.

Various tests are used to assess doses. During some of them, the subject is sitting or standing, making head movements; another option is to assess dynamic visual acuity while walking, for example, on a treadmill ^[17,24].

It is shown that the dynamic visual acuity test with stimulation of horizontal semicircular channels can be carried out for children from the age of three.

             Another paper shows the possibility of conducting this test for typically developing children over 5 years of age. The necessity of research into the possibility of using the test for children with various developmental disorders is discussed ^[25].

We have found that children with learning difficulties can often reveal various manifestations of functional immaturity of the vestibular system, including violations of dynamic visual acuity ^[8].

Studies by other authors have shown that dose reduction is typical for children with hearing impairments ^[19].

            There is evidence of the connection of vestibular dysfunctions not only with the insufficiency of compensatory eye movements, but also with memory.  The work of Wiener-Vacher and co-authors describes the connections between the vestibular apparatus in the inner ear and the hippocampus, which is responsible for transferring short-term memories into long-term memory. Thus, memory is associated with our movements in space, since the hippocampus receives impulses from the vestibular system only with certain movements of the head in space ^[21,23,26].

            Perhaps this explains the observations that some children memorize learning material better when they have the ability to move rather than sit still ^[4,5].

The experimental data obtained by us that vestibular training can contribute to the normalization of dynamic visual acuity are consistent with the results of studies by other authors.

So, in the work of Calgani and co-authors, it was shown that short vestibular training in combination with cognitive training increases reading speed in children with dyslexia. Positive changes persisted a month after the training ^[16].

A study by Lofty and co-authors shows the effectiveness of vestibular training for children with attention deficit hyperactivity disorder (ADHD), which is combined with vestibular disorders. The study involved 54 children with ADHD who were randomly divided into two groups. The experimental group of children underwent training, which included balance exercises and oculomotor exercises and exercises for hand-eye coordination. Children of the control group did not participate in vestibular training. Testing before and after the training using a battery of CANTAB tests showed an improvement in cognitive performance after the training, which includes vestibular exercises ^[18,20].

Conclusion. In children with learning difficulties, reduced reactivity of the vestibular system may be detected, which affects the vestibulocular function.  The conducted experimental study showed that vestibular training on a riding simulator significantly improves dynamic visual acuity in a group of children with hyperactivity and symptoms of astheno-neurotic syndrome. The prognosis of the effectiveness of such training is also favorable for children, in whom, according to the results of an instrumental study of the vestibular function, an asymmetry of sensory reactivity of the channel and otolith sections of the vestibular apparatus is revealed.