Translingual Neurostimulation in Late Residual Stage Cerebral Palsy

Children Treatment Affects Functional Brain Networks

A. Yu. Efimtsev

, T. S. Ignatova

, A. G. Trufanov

, A. G. Levchuk

, G. E. Trufanov

E. N. Kondratyeva

, N. Yu. Shmedyk

, A. M. Sarana

2,5

, S. G. Shcherbak

2,5

and Yu. P. Danilov

The Almazov National Medical Research Centre, St. Petersburg, Russian Federation

St. Petersburg State Healthcare Institution “City Hospital No. 40”, 197706, Borisova str., 9, St. Petersburg, Russia

Military Medical Academy n.a. S. M. Kirov, Akademika Lebedeva str., 6, St. Petersburg, Russia

Institute of Physiology n.a. I.P. Pavlov, Russian Academy of Sciences, Makarova Embankment, 6, St. Petersburg, Russia

St. Petersburg University, University Embankment 7-9, St. Petersburg, Russia

Keywords: Neuro-electrostimulation, Neuroimaging, Functional MRI, Cerebral Palsy.

Abstract: Management of cerebral palsy is an actual problem of modern medicine. A new direction of

neurorehabilitation, intensively discussed in modern science and practice, includes various types of electrical

stimulation. Constant stimulation of the nervous system is one of the most popular ways to activate neural

networks to activate the brain and initiate neuroplasticity processes. Participants in the experiment were

children with cerebral palsy, spastic diplegia form at the age of 6 to 19 (n = 6) (mean age - 17,9 ± 5,6 years).

All subjects underwent standard treatment, including massage, therapeutic gymnastics simulators, robotic

mechanotherapy, etc., which lasted 20-25 minutes with neurostimulation of the brain (using a PoNS device).

All subjects underwent a resting state functional MRI once before and twice - after neurostimulation course.

Results indicate positive dynamics in all subjects: most of them learned walking without aids, obtained

decreased muscle tonus and improvement in balance, coordination function were noted. Neurostimulation

with the PoNS device combined with curative gymnastics (focused exercises), improves the efficiency of

motor functions and the development of motor skills. Resting state functional MRI showed improvement in

brain networks. If performed properly, it can be an auxiliary method of objective control of treatment

effectiveness.

1 INTRODUCTION

In subjects with cerebral palsy, there are apparent

violations of equilibrium, the position of motion,

retention of the pose in space. Each function of the

human body is based on well-organized complex

neural networks, including numerous interconnected

structures (cortex, nuclei, neural clusters) located in

different levels of brain and spinal cord.

Collaboration and synchronization of human

performance in behavioral, cognitive and autonomic

functions. This close integration is especially

important in complex sensory and motor functions,

such as vision, hearing, balance, gait, speech.

Neurorehabilitation of children with cerebral

palsy is multicomponent and includes physiotherapy,

special massage therapy, treatment, special limb

treatment with different stitches, the use of fixing

devices for walking, special, facilitating the motor

activity of the child, and costumes. In modern

medicine, the problems of rehabilitation of children

with cerebral palsy are given particular attention. A

new direction of neurorehabilitation, intensively

discussed in contemporary science and practice, is the

use of various types of electrostimulation, as well as

their use in or in combination with existing

procedures. The most common among them - are

electrical stimulation of muscles and nerves, as well

as the spinal cord. Electrical stimulation was used to

treat spastic Erb-Duchenne paralysis in 1871. Since

the treatment of patients with spasticity by electrical

stimulation of the muscles and nerve structures, skin,

subcutaneous, epidural electrodes, as well as peroneal

implantations have been used (Morenko et al., 2015).

Despite the positive results achieved by an integrated

approach of treatment, the problem of rehabilitation

of children with cerebral palsy in the late residual

stage with persistent stereotypes remains unresolved.

Eﬁmtsev, A., Ignatova, T., Trufanov, A., Levchuk, A., Trufanov, G., Kondratyeva, E., Shmedyk, N., Sarana, A., Shcherbak, S. and Danilov, Y.

Translingual Neurostimulation in Late Residual Stage Cerebral Palsy Children Treatment Affects Functional Brain Networks.

DOI: 10.5220/0007698205490556

In Proceedings of the 12th International Joint Conference on Biomedical Engineering Systems and Technologies (BIOSTEC 2019), pages 549-556

ISBN: 978-989-758-353-7

549

The issue of restoring muscle control and complex

sensorimotor integration (balance, movement

coordination, body retention in space) has not been

given the necessary attention so far. Artificial

stimulation of the nervous system is one of the most

popular ways to activate neural networks to activate

the brain and initiate neuroplasticity processes

(Danilov et al., 2006).

2 MATERIALS AND METHODS

2.1 Neurostimulation

An innovative alternative method of using peripheral

neurostimulation for neurorehabilitation was

presented by Yu. P. Danilov at the World Congress

on Psychophysiology in St. Petersburg in 2010. This

method was developed at the University of

Wisconsin, USA, in a laboratory headed by the

famous scientist Paul Bach-Rita, one of the founders

of the modern concept of neuroplasticity. In the

laboratory of haptic communication and

neurorehabilitation (TCNL), a device was developed

for electro-tactile stimulation of human skin, and in

the most densely innervated tactile region, the tongue

(Danilov et al., 2008). Electrotactic stimulation of the

tongue is, at the moment, the most effective and safest

stimulation of the central nervous system. The tongue

is the thinnest part relative to other surfaces of the

skin, saturated with various types of mechanical,

thermal and taste receptors, with the addition of free

nerve endings. This zone has a maximum density of

mechanoreceptors per unit area and has a minimum

two-point discrimination threshold: 0.5-1 mm for

mechanical stimulation and 0.25-0.5 mm for

electrical stimulation (Danilov et al., 2007). Two

main cranial nerves (branches of the trigeminal,

20,000-22,000 nerve fibers and the facial nerve,

3,000-6,000 nerve fibers) from the front surface of the

tongue transmit nerve impulses directly to the brain

stem structures. They activate the complex of the

trigeminal nerve (mesencephalic, sensory and spinal)

the largest nuclei of the trunk) and simultaneously

along the branch of the facial nerve the adjacent

nucleus of the solitary tract is stimulated. The

cochlear nuclei, the structures of the medulla and the

upper sections of the cervical spine (C2 and C3) are

activated directly also. The reticular formation of the

brain stem, the complex of vestibular nuclei and the

ventral part of the cerebellum fall into the zone of

secondary activation (Barbara et al., 2009). As you

know, the brain stem area has a massive accumulation

of neural nuclei (86), some of them are engaged in

autonomous regulation (blood circulation,

respiration), the other part - sensorimotor integration.

It is not necessary to exclude the possible secondary

activation of several common systems of

neurochemical regulation of brain activity, the nuclei

of which are located in the brain stem - noradrenergic,

dopaminergic, serotonergic and acetylcholinergic.

Descending paths regulating the activity of spinal

cord motoneurons, namely: the trigeminal-spinal,

solitary-spinal, and three vestibulo-spinal, directly

involved in the regulation of the activity of the lower

limbs and walking, come from the same area

(Mitchele et al., 2009). Intensive rhythmic

stimulation of existing neurons leads to the

corresponding activation of synaptic contacts and

axons, including the whole complex of pre- and

postsynaptic neurochemical mechanisms (Ignatova et

al., 2018). Phenomena such as long-term potentiation

or depression of neural networks may underlie the

effects observed when using electro-tactile

stimulation of the tongue. Long-term potentiation

(Long-term potentiation, LTP), as well as long-term

depression (Long-term inhibition, LTI), is the

enhancement or suppression of synaptic transmission

between two neurons that persists for a long time after

exposure to the synaptic pathway. LTP is involved in

the mechanisms of synaptic plasticity, providing the

nervous system of a living organism with the ability

to adapt to changing environmental conditions

(Patriat et al., 2013). Most neurophysiological

theorists believe that long-term potentiation together

with long-term depression underlies the cellular

mechanisms of memory and learning (Lomo, 2003).

At the moment, the device for electrotactile

stimulation is called PoNS (Portable

Neurostimulator), and its use for stimulation of the

brain in children with cerebral palsy is a new direction

in neurorehabilitation. The matrix, in which are the

electrodes of irregular shape; optimized to stimulate

the most sensitive areas of language. The matrix itself

includes 143 electrodes divided into nine 16 -

electrode sectors (Fig.1). Within each segment, only

one electrode is active at a given time, and the rest are

grounded. Stimulation through one electrode occurs

simultaneously in nine sectors. The electrodes are

alternated with a frequency of 50 Hz. The incentive is

a triplet of rectangular pulses of microsecond

duration.

Regular stimulation from the PoNS device,

activating vast areas of the brain, increases the

efficiency of existing neural networks, increases the

likelihood of the formation of new synaptic contacts

(synaptogenesis), enhances the brain's innate ability

to improve motor function. The goal of successful

NNSNT 2019 - Special Session on Non-invaisive Neuro-stimulation in Neurorehabilitation Tasks

550

neurorehabilitation with such stimulation is to restore

motor function or to teach new motor skills, achieved

by combining specialized exercises with extensive

brain activation using the PoNS device.

Figure 1: The PoNS device (Portable Neurostimulator), the

close-up of the matrix.

Figure 2: The PoNS device (Portable Neurostimulator).

The studies were conducted in patients with

peripheral and central vestibular disorders (Badke et

al., 2011; Chisholm et al., 2014; Bach-y-Rita, 2008;

Wildenberg et al., 2013) multiple sclerosis, stroke

(Wildenberg et al., 2011), TBI and spinal injuries

(Joseph et al., 2011; Kublanov, 2008; Kublanov et al.,

2018). The high efficiency of peripheral

neurostimulation was shown in combination with

specialized physiotherapy in restoring general motor

control of the body, balance, walking, speech, eye

movements, various aspects of sensorimotor

integration. Additional studies, using functional MRI,

unequivocally confirmed the presence of potent

activation of the brain stem and the ventral part of the

cerebellum during stimulation of the tongue, as well

as the presence of long-lasting aftereffect, the

preservation of foci of activity in the brain of subjects

for hours and even days after the last stimulation

(Efimtcev et al., 2018). Additional data analysis

showed that simultaneously with the activation of the

subcortical structures of the brain, the coefficients of

communication between the cortex areas of the brain

involved in integrative training processes also change

(Petrenko et al., 2017).

2.2 Participants

This study involved six children with a cerebrally

palsy, form of spastic diplegia. Patients with intact

intellect, no seizures in anamnesis. All children

obtained standard treatment, including massage,

medical gymnastics with simulators, robotic

mechanotherapy, hydrotherapy, and 10 daily sessions

of physical therapy, which lasted for 20-25 minutes

and neurostimulation of the brain (using the PoNS

device). Patients underwent functional MRI of the

brain before the start of and at the end of the course

of treatment using neurostimulation. The patients

were aged 8 to 14 years. Patients were evaluated by

standard scales GMFSC Scale (gross motor skills),

FMS (functional motor scale), Berg balance scale, the

Ashworth scale (spasticity).

All patients underwent resting state fMRI at three

timepoints - before the course of neurostimulation,

within 3 days after the end of the course of

neurostimulation, and in 1 month after

neurostimulation. The parameters of the pulse

sequence were: BOLD technique, repetition time

(TR) - 3000 ms, echo time (TE) - 30 ms, spin rotation

angle (FA) - 90°, FOV - 192 mm, matrix - 64 × 64,

slice thickness - 4.5 mm, the number of slices - 29,

the number of repetitions - 120, the scan time - 6

minutes. Patients were instructed to lie with their eyes

open (do not sleep), without fixing their gaze. Thus,

for all subjects, there were identical conditions of a

state of rest, and this had a minimal impact on the

visual and aural working networks of the brain.

Also, all patients underwent structural MRI with

obtaining T1 and T2 weighted images and FLAIR

(Fluid attenuated inversion-recovery) to exclude

brain tumors and other pathological morphological

changes. The T1-weighted gradient echo MP-RAGE

(Magnetization Prepared Rapid Acquired Gradient

Echoes) pulse sequence — a gradient echo with

magnetization preparation and fast collection — was

used to align fMRI images with the anatomical

structures of the brain. The main feature of this

sequence is its high resolution and isotropic voxel

with a volume of 1.2 mm

Translingual Neurostimulation in Late Residual Stage Cerebral Palsy Children Treatment Affects Functional Brain Networks

551

The parameters of the MP-RAGE pulse sequence

were: repetition time (TR) - 2300 ms, echo time (TE)

- 3 ms, spin rotation angle (FA) - 9 °, FOV - 240 ×

256 mm, matrix - 256 × 240, slice thickness - 1.2 mm,

the number of slices - 160, the number of repetitions

- 1, scanning time - 9 minutes. Details of the

parameters of all pulse sequences are presented in

Table 1.

Table 1: MRI Examination Protocol.

Pulse

sequence

Scan time Parameters

T2 TSE

(axial plane)

2 m. 30 s.

FOV – 220×220 mm, slice

thickness – 4.0 мм, TR –

6000 ms, ТЕ – 93 ms,

matrix – 320×320, slice

number

–

T2 TIRM

(axial plane)

4 m. 30 s.

FOV –199×220 mm, slice

thickness – 4.0 мм, TR –

9000 ms, ТЕ – 93 ms,

matrix – 256×232, slice

number

–

MPRAGE 9 m

FOV – 240×256 mm, slice

thickness – 1.2 мм, TR –

2300 ms, ТЕ – 3 ms, matrix

– 256×240, slice number –

160

BOLD FRMI

(resting state)

6 m

FOV – 192×192 mm, slice

thickness – 4.5 мм, TR –

3000 ms, ТЕ – 30 ms,

matrix – 64×64, slice

number

–

Statistical processing and evaluation of the results

of neuroimaging studies of each patient individually

and their group (rest fMRI data) was carried out using

the software package CONN v.18 (Functional

connectivity toolbox). The software was designed to

determine the relationships between various brain

regions, including the dynamic mode, statistical

mapping of activation zones, identifying the structure

of multiple rest networks and working functional

networks of the brain. We used analysis based on the

choice of the region of interest (ROI-to-ROI and

Seed-to-Voxel), as well as analysis based on graph

theory (Fig. 3).

3 RESULTS

The first patient before the course of treatment could

walk using multi-support canes within the room, and

used walkers for longer distances (500 meters or

more), after the course of treatment he mastered

walking using one single-support cane within the

room and at school, for longer distances uses multi

support sticks. Before the treatment, the second

patient used multi-support canes for walking within

Figure 3: Graphical representation of the results of

intergroup statistical analysis based on the choice of the

zone of interest (ROI-to-ROI): a - maps with a schematic

representation, combined with an anatomical atlas of the

brain; b - 3D reconstruction of the map of positive and

negative functional connections, combined with the

anatomical atlas of the brain.

the room, and on the street, the patient could not stand

on his own without support, after finishing the course

of treatment he learned to walk independently on a

flat surface (within the room), the patient can stand

on his own without a support and on the street uses

one single support cane. The third patient, before the

NNSNT 2019 - Special Session on Non-invaisive Neuro-stimulation in Neurorehabilitation Tasks

552

start of the course of treatment, used a walker within

the room to walk, a stroller was used at school and for

longer distances. After completing the course of

treatment, the patient has mastered multi-support

canes within the room, the walker is using at school

and can walk to the playground, and an active type

stroller is used for longer distances. Before the

treatment, the fourth patient walked using two single-

support canes within the premises and on the street,

could stand for several seconds without support, at the

end of the course of treatment he learned to walk

independently on a flat surface, he stands alone on the

street, using one single-bearing cane on the street.

The fifth patient, before the course of treatment, used

multi-support canes for walking, at the end of the

treatment course, he mastered walking within the

premises, relying on one single-bearing cane, and

using multi-support canes for longer distances.

One patient with the level of GMFSC

development 4, before the course of treatment, could

move around with the walker within the room, an

active type of stroller was used at school and on the

street. At the end of the course of treatment the patient

learned to walk using multi-support canes within the

room and at school for more long distance confidently

uses walkers. Also, all patients showed a decrease in

muscle tone and an improvement in balance and

coordinating function. The equilibrium

improvements estimated on the Berg scale ranged

from 2 to 7 units (4.5 on average), and as a percentage

of the initial state, the improvement was observed

from 12 to 70% (31% on average) (Fig. 4).

Figure 4: Berg scale (patients data).

As the result of intergroup statistical analysis

(two-sample t-test, comparing the resting state in the

first and second timepoints), we noticed the

enhancement of the functional connections (FC) and

the interaction of the MPFC with the posterior

parietal cortex on the right, frontoparietal cortex,

anterior sections of cingulate cortex (ACC),

supramarginal and angular gyri on the left. All of

them are parts of a default mode network (DMN). At

the same time, we found decreased FC of MPFC and

the cerebellar worm (p FDR-corr. <0.05) (Fig. 5,

Table 2).

(a)

(b)

Figure 5: The result of a group comparison of patients in the

second and first timepoints. The areas of statistically

significant differences are shown: increase and decrease of

the functional connectivity in diagram (a) and on the 3D

model (b) (cont.).

When performing intergroup statistical analysis

(two-sample t-test, comparing the state of rest in the

first and third timepoints), the changes were less

expressed. The MPFC FC with the paracingulate gyri

on the right and the ACC intensified even more, and

the FC with the posterior occipital cortex on the left

decreased (p FDR-corr. <0.04) (Fig. 6, Table 3).

Translingual Neurostimulation in Late Residual Stage Cerebral Palsy Children Treatment Affects Functional Brain Networks

553

Table 2: The results of a group comparison of patients in

the second and first timepoint.

(a)

(b)

Figure 6: The result of a group comparison of patients in the

third and first timepoint. The areas of statistically

significant differences are shown: increase and decrease of

the functional connectivity in diagram (a) and on the 3D

model (b).

Table 3: The results of group comparison of patients in the

second and first timepoint.

When performing analysis based on graph theory,

global efficiency has become more expressed at the

second and third timepoints, compared to the first

timepoint (p FDR-corr.<0.05 for each time point)

(Fig. 7).

a b

Figure 7: The result of the analysis based on graph theory

at different timepoints: a – the first timepoint (before the

course of treatment), b – the second timepoint (immediately

after the course of treatment), c – the third timepoint

(delayed study).

4 DISCUSSION

The simultaneous combination of TLNS with

specialized exercises allows to influence all

components of motor activity: central (cortical),

Brain area

Hemis

phere

T Voxels

% of

atlas

Volume

MNI

coordinates

(x,y,z)

atlas.Ver12 (Vermis 1 2)

-4.23

41 87 328 1,-40,-11

atlas.PaCiG r (Paracingulate Gy*ght)

3.96

213 16 1704 7,37,23

networks.Salience.SMG (L) (-

60,*,31)

3.73

416 44 3328 -60,-39,-31

atlas.AG r (Angular Gyrus Right)

2.98

630 43 5040 54,-50,-17

atlas.pSMG l (Supramarginal

Gyr*eft)

2.63

431 41 3448 -55,-46,33

networks.Salience.ACC (0,22,35)

2.52

147 6 1176 0,21,-15

atlas.AG l (Angular Gyrus Left)

2.42

334 35 2672 -50,-56,30

networks.FrontalParietal.PPC

(R)*,45)

2.37

52,-52,32

Brain area

Hemisp

here

T Voxels

% of

atlas

Volume

MNI

coordinates

(x,y,z)

atlas.PaCiG r (Paracingulate

Gy*ght)

3.76

102 8 816 7,37,23

networks.Salience.ACC

(0,22,35)

2.74

250 10 2000 0,22,35

atlas.OP l (Occipital Pole Left) l

-2.66

171 6 1368 -17,-97,7

NNSNT 2019 - Special Session on Non-invaisive Neuro-stimulation in Neurorehabilitation Tasks

554

subcortical (basal ganglia, cerebellum, brain stem),

spinal cord centers. Thus, multilevel

neurostimulation allows activating not only muscle

control (decrease in tone) but also such complex

sensorimotor functions as balance and movement

coordination when walking, which, in combination

with physical rehabilitation, helps to master and

develop new motor skills quickly.

The positive effects persisted (or decreased, but

slightly) during the many months of interruption (up

to one year) between the courses of therapy, which is

confirmed by our fMRI study. It shows that the

dynamical changes in brain during the course are

obvious, and there were also improvements a month

later, though they were not so significant compared to

the second one, the clinical condition of the patients

confirms this fact. They did not have negative

dynamics. This allowed us to consistently improve

the symptoms, being studied, with each subsequent

course, i.e. neurostimulation gives to rehabilitation a

cumulative (accumulative) effect.

It is traditionally considered that a child with

cerebral palsy reaches half of its potential to develop

motor skills by the age of 5 years and the maximum

possible development by 7 years. The potential

achieved remains at the same level or may even

worsen with age. In our experiments, all children

were over the age of 7 years. These results can

significantly expand both the scope of this technology

in the rehabilitation of children with cerebral palsy

and improve the prediction of the effectiveness of the

therapy used for older children.

Brain TLNS enhances the effect of physical

rehabilitation, activating vast areas of the brain,

increases the efficiency of existing neural networks,

increases the likelihood of new synaptic contacts

(synaptogenesis), enhances the brain's innate ability

to improve motor function. The fMRI data alone

confirms that the human brain is plastic at any age and

is capable of an amazing reorganization, the

mechanisms of which we are just beginning to

explore. The dynamics of changes in DMN and

functional connections between the first and second

timepoints turned out to be more vivid than between

the first and third timepoints. That probably indicates

a delayed rehabilitation effect.

5 CONCLUSION

Taking into the attention the limited and minimal

intensity of training, the main task of the study was

limited to the formation of new motor skills. The

patient in 10 sessions had to form a new motor skill,

consolidate it and use it in everyday life. Based on

these considerations, it is clear why the index of

general motor control (FMS scale) has statistically

significantly improved. Since the development of

motor control skills was the task of training, besides

general improvement in functional connectivity,

certain parts of motor neural networks improved their

level of functional activity as a result of

neurostimulation. This technique is innovative in the

field of neurostimulation, non-invasive, safe and easy

to use. Indeed, the daily 20-minute stimulation of the

tongue for two weeks increases the innate ability of

the brain to improve motor function, contributes to

the formation of new motor skills.

The use of neurostimulation using the PoNS

device, in combination with therapeutic exercises

(targeted exercises), can improve the efficiency of the

recovery of motor functions and the development of

motor skills.

The use of resting state functional MRI allows to

obtain data without having to perform special tasks

for children, which simplifies the method of objective

monitoring, as well as it provides better and more

detailed information about the functional state of the

brain than with task-based fMRI. This pilot study data

allows to consider the fMRI technology as the

objective tool for the neuro-electrostimulation

mechanisms investigation. The data could also form

new treatment techniques of the non-invasive multi-

electrode neck neural structures neurostimulation

application for treatment of the psychiatric and

neurological disorders, exactly – disorders

accompanied by the neurodegeneration (Alzheimer

disease, Parkinson disease, dementia), consequences

of the brain traumas, neurotoxic actions, depressive

and anxiety disorders, strokes.

ACKNOWLEDGEMENTS

The work was supported by Act 211 Government of

the Russian Federation, contract № 02.A03.21.0006.

The authors thank Ivan Brak, Elena Filimonova and

Eugenia Kobeleva for participation in the data

processing.

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