Publications by authors named "Antonino Naro"

169 Publications

Is intensive gait training feasible and effective at old age? A retrospective case-control study on the use of Lokomat Free-D in patients with chronic stroke.

J Clin Neurosci 2021 Oct 23;92:159-164. Epub 2021 Aug 23.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy. Electronic address:

Background: In the last decade, the number of people over 60 has increased, leading to various healthcare problems. The aim of this retrospective study is to evaluate the effects of robotic rehabilitation in elderly patients as well as their perception of usability and adaptation to intensive robotic neurorehabilitation.

Methods: This is a retrospective case-control study. Eighty elderly stroke patients were included in the analysis using an electronic data retrieval system. The enrolled patients were divided into two groups: the experimental group (EG) underwent rehabilitation training with Lokomat FreeD, equipped with a VR screen, while the control group (CG) performed traditional rehabilitation training. The two groups matched for age, sex, education, brain injury, stroke interval. The rehabilitation protocol included a total of 40 training sessions.

Results: Both types of rehabilitation led to an improvement in the perceived level of disability (FIM) and in the performance in gait and balance (TT), highlighting a significant improvement especially in the EG. However, only in the EG, Lokomat training had induced an increase in the distance covered in 10 min (10 m walk test), and a significant improvement in mood (HRS-D). Moreover, Lokomat-FreeD was well tolerated by patients with high levels of usability.

Conclusions: Our results suggest that elderly patients may benefit from high-intensity robotic neurorehabilitation using the Lokomat-Pro FreeD.
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http://dx.doi.org/10.1016/j.jocn.2021.08.013DOI Listing
October 2021

Beyond motor recovery after stroke: The role of hand robotic rehabilitation plus virtual reality in improving cognitive function.

J Clin Neurosci 2021 Oct 31;92:11-16. Epub 2021 Jul 31.

IRCCS Centro Neurolesi, Bonino Pulejo, Messina, Italy. Electronic address:

Robot-assisted hand training adopting end-effector devices results in an additional reduction of motor impairment in comparison to usual care alone in different stages of stroke recovery. These devices often allow the patient to perform practical, attentive, and visual-spatial tasks in a semi-virtual reality (VR) setting. We aimed to investigate whether the hand end-effector robotic device Amadeo could improve cognitive performance, beyond the motor deficit, as compared to the same amount of occupational treatment focused on the hand. Forty-eight patients (aged 54.3 ± 10.5 years, 62.5% female) affected by either ischemic or hemorrhagic stroke in the chronic phase were enrolled in the study. The experimental group (EG) underwent Amadeo robotic training, while the control group (CG) performed occupational therapy involving the upper limb. Patients were assessed at the beginning and at the end of the rehabilitation protocol using a specific neuropsychological battery, as well as motor function tests. The EG showed greater improvements in different cognitive domains, including attentive abilities and executive functions, as well as in hand motor function, as compared to CG. Our study showed that task-oriented VR-based robotic rehabilitation enhanced not only motor function in the paretic arm but also global and specific cognitive abilities in post-stroke patients. We may argue that the hand robotic plus VR-based training may provide patients with an integration of cognitive and motor skill rehabilitation, thus amplifying the functional outcome achievement.
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http://dx.doi.org/10.1016/j.jocn.2021.07.053DOI Listing
October 2021

Paving the way for a better management of pain in patients with spinal cord injury: An exploratory study on the use of Functional Electric Stimulation(FES)-cycling.

J Spinal Cord Med 2021 Aug 9:1-11. Epub 2021 Aug 9.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy.

Context/objective: Chronic pain is common in patients with spinal cord injury (SCI), for whom it negatively affects quality of life, and its treatment requires an integrated approach. To this end, lower limb functional electrical stimulation (FES) cycling holds promise.

Objective: To investigate pain reduction in a sample of patients with SCI by means of lower limb rehabilitation using FES cycling.

Design, Setting And Participants: Sixteen patients with incomplete and complete SCIs, attending the Neurorobotic Unit of our research institute and reporting pain at or below the level of their SCI were recruited to this exploratory study.

Interventions: Patients undertook two daily sessions of FES cycling, six times weekly, for 6 weeks.

Outcome Measures: Pain outcomes were measured using the 0-10 numerical rating scale (NRS), the Multidimensional Pain Inventory for SCI (MPI-SCI), and the 36-Item Short Form Survey (SF-36). Finally, we assessed the features of dorsal laser-evoked potentials (LEPs) to objectively evaluate Aδ fiber pathways.

Results: All participants tolerated the intervention well, and completed the training without side effects. Statistically significant changes were found in pain-NRS, MPI-SCI, and SF-36 scores, and LEP amplitudes. Following treatment, we found that three patients experienced high pain relief (an NRS decrease of at least 80%), six individuals achieved moderate pain relief (an NRS decrease of about 30-70%), and five participants had mild pain relief (an NRS decrease of less than 30%).

Conclusion: Our preliminary results suggest that FES cycling training is capable of reducing the pain reported by patients with SCI, regardless of American Spinal Injury Association scoring, pain level, or the neurological level of injury. The neurophysiological mechanisms underlying such effects are likely to be both spinal and supraspinal.
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http://dx.doi.org/10.1080/10790268.2021.1961050DOI Listing
August 2021

Does cybersickness affect virtual reality training using the Computer Assisted Rehabilitation Environment (CAREN)? Preliminary results from a case-control study in Parkinson's disease.

Physiother Theory Pract 2021 Aug 7:1-9. Epub 2021 Aug 7.

Neurorehab Unit, IRCCS Centro Neurolesi "Bonino-Pulejo, Messina, Italy.

This pilot study aimed to evaluate whether and to what extent cybersickness (CS) may affect a rehabilitation program using the Computer-assisted Rehabilitation Environment (CAREN), a virtual reality (VR) computer-assisted device for clinical rehabilitation. The study was carried out on 30 subjects, 15 patients with Parkinson's Disease (PD) and 15 healthy controls (HC), which underwent a set of four exergames programmed by our team for PD rehabilitation training. All participants completed the Motion Sickness Susceptibility Questionnaire Short-form (MSSQ) before the training and the Motion Symptoms Assessment Questionnaire (MSAQ) immediately after a single CAREN session. Overall, mean MSAQ scores remained low after the session, suggesting that the users did not experience severe discomfort. We found no significant difference in MSAQ scores between the two groups, while there was a statistically significant difference for the subsection of MSAQ regarding the peripheral symptoms (i.e. sweating, cold sweating, feeling warm), which were higher in HC. Moreover, the results highlighted some correlation between MSSQ and MSAQ. Gastrointestinal symptoms in PD, as well as MSSQ and sopite-related symptoms in HC, were also correlated with susceptibility to CS. As CS is rarely reported after CAREN, this and similar devices may be considered comfortable and safe for patients' rehabilitation involving VR training, including PD persons.
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http://dx.doi.org/10.1080/09593985.2021.1964117DOI Listing
August 2021

Cognitive recovery in people with relapsing/remitting multiple sclerosis: A randomized clinical trial on virtual reality-based neurorehabilitation.

Clin Neurol Neurosurg 2021 Sep 21;208:106828. Epub 2021 Jul 21.

IRCCS Centro Neurolesi "Bonino Pulejo", Messina, Italy.

Background: Multiple sclerosis (MS) can adversely affect several domains of cognitive function, including attention, information processing, memory and learning, executive functions and visuospatial skills. In recent years, technological innovations have proven effective in improving motor and cognitive impairment in neurological patients, including those affected by MS.

Objective: The study aims to evaluate cognitive outcomes after rehabilitation training with the Virtual Reality rehabilitation system (VRRS) in patients suffering from MS.

Methods: All patients were randomized into either the control group (CG: 15 patients) receiving conventional cognitive rehab or the experimental group (EG) using virtual reality (VR) (15 patients). Both groups underwent the same amount of cognitive training, 3 times a week for 8 weeks. They were submitted to neuropsychological assessment before (T0) and after the rehabilitation treatment (T1).

Results: Our data showed that both conventional and VR cognitive rehabilitation approaches improved mood (p < 0.001) and visuospatial skills. However, only in the EG a significant improvement in specific cognitive domains (p < 0.001), including learning ability, short-term verbal memory, lexical access ability, as well as quality of life related to mental states, was found.

Conclusions: The present study demonstrated that VR can be a motivational and effective tool for cognitive recovery in MS patients.
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http://dx.doi.org/10.1016/j.clineuro.2021.106828DOI Listing
September 2021

Rehabilitation of somatoparaphrenia with misoplegia: insights from a single case-pilot study.

J Integr Neurosci 2021 Jun;20(2):439-447

Istituto di Ricerca e Cura a carattere Scientifico Centro Neurolesi "Bonino Pulejo", 98158 Messina, Italy.

Somatoparaphrenia lacka ownership of a paralyzed limb, i.e., the illusion that one's limbs belong to someone else. Somatoparaphrenia is one of the many forms of body misperceptions. We report a case of somatoparaphrenia with misoplegia, characterized by the absence of anosognosia for hemiplegia and personal neglect, following a surgical operation for left parietal meningioma. The patient received a novel multidisciplinary treatment, including motor rehabilitation training, traditional physiotherapy and robotic rehabilitation using the Hunova Movendo Technology and psychological counseling. At the end of the training, the patient improved in global cognitive functioning, mood, motor abilities, and the perception of herself and her body, reducing the sense of estrangement and repulsion in the lower right limb. Our result showed the importance of a specific neuropsychological assessment in patients with parietal brain lesions and the usefulness of an integrated psychological and motor approach in rehabilitating patients with somatoparaphrenia, primarily when associated with misoplegia.
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http://dx.doi.org/10.31083/j.jin2002046DOI Listing
June 2021

Pain Perception in Disorder of Consciousness: A Scoping Review on Current Knowledge, Clinical Applications, and Future Perspective.

Brain Sci 2021 May 20;11(5). Epub 2021 May 20.

Department of Clinical and Experimental Medicine, University of Messina, 98124 Messina, Italy.

Pain perception in individuals with prolonged disorders of consciousness (PDOC) is still a matter of debate. Advanced neuroimaging studies suggest some cortical activations even in patients with unresponsive wakefulness syndrome (UWS) compared to those with a minimally conscious state (MCS). Therefore, pain perception has to be considered even in individuals with UWS. However, advanced neuroimaging assessment can be challenging to conduct, and its findings are sometimes difficult to be interpreted. Conversely, multichannel electroencephalography (EEG) and laser-evoked potentials (LEPs) can be carried out quickly and are more adaptable to the clinical needs. In this scoping review, we dealt with the neurophysiological basis underpinning pain in PDOC, pointing out how pain perception assessment in these individuals might help in reducing the misdiagnosis rate. The available literature data suggest that patients with UWS show a more severe functional connectivity breakdown among the pain-related brain areas compared to individuals in MCS, pointing out that pain perception increases with the level of consciousness. However, there are noteworthy exceptions, because some UWS patients show pain-related cortical activations that partially overlap those observed in MCS individuals. This suggests that some patients with UWS may have residual brain functional connectivity supporting the somatosensory, affective, and cognitive aspects of pain processing (i.e., a conscious experience of the unpleasantness of pain), rather than only being able to show autonomic responses to potentially harmful stimuli. Therefore, the significance of the neurophysiological approach to pain perception in PDOC seems to be clear, and despite some methodological caveats (including intensity of stimulation, multimodal paradigms, and active vs. passive stimulation protocols), remain to be solved. To summarize, an accurate clinical and neurophysiological assessment should always be performed for a better understanding of pain perception neurophysiological underpinnings, a more precise differential diagnosis at the level of individual cases as well as group comparisons, and patient-tailored management.
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http://dx.doi.org/10.3390/brainsci11050665DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8161058PMC
May 2021

How patients with mild dementia living in a nursing home benefit from dementia cafés: a case-control study focusing on psychological and behavioural symptoms and caregiver burden.

Psychogeriatrics 2021 Jul 18;21(4):612-617. Epub 2021 May 18.

IRCCS Centro Neurolesi Bonino-Pulejo, Messina, Italy.

Background: Dementia is a syndrome, mainly due to neurodegeneration, affecting cognition, behaviour, feelings and relationships. Pharmacological treatment is still challenging and thus different ways to improve/slow down the disease are necessary.

Methods: Twenty-five subjects with mild dementia, living in a nursing home, and their relatives were invited to attend a dementia cafe, a community group which provides support for families affected by dementia. Each patient was evaluated by a neuropsychologist, through the administration of a specific neuropsychological battery, before and at the end of the study. Their outcomes were compared to a matched group of patients with dementia receiving psycho-counselling.

Results: After the dementia cafe meetings, patients showed higher significant changes in mood (P < 0.01), behavioural symptoms (P < 0.001), quality of life (P < 0.001), and caregiver burden (P < 0.001). The control group significantly improved only in quality of life with a reduction of caregiver burden.

Conclusions: Our findings confirm that patients with dementia may benefit from the dementia cafe, especially concerning behavioural symptoms. Moreover, caregivers find these cafés to be welcoming, relaxed places to socialise and access support and information. Future dementia cafés should create programs and comfortable environments answering to the different needs of the patients.
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http://dx.doi.org/10.1111/psyg.12721DOI Listing
July 2021

An action-observation/motor-imagery based approach to differentiate disorders of consciousness: what is beneath the tip of the iceberg?

Restor Neurol Neurosci 2021 ;39(3):181-197

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy.

Background: The evaluation of motor imagery in persons with prolonged Disorders of Consciousness (pDOC) is a practical approach to differentiate between patients with Minimally Conscious State (MCS) and Unresponsive Wakefulness Syndrome (UWS) and to identify residual awareness even in individuals with UWS. Investigating the influence of motor observation on motor imagery could be helpful in this regard.

Objective: In order to corroborate the clinical diagnosis and identify misdiagnosed individuals, we used EEG recordings, to assess the influence of the low-level perceptual and motoric mechanisms on motor observation on motor imagery, taking into account the role of the high-level cognitive mechanisms in patients with pDOC.

Methods: We assessed the influence of motor observation of walking in first-person or third-person view (by a video provision) on motor imagery of walking in the first-person view on the visual N190 (expression of motor observation processing), the readiness potential (RP) (expressing motor preparation), and the P3 component (high-level cognitive processes) in a sample of 10 persons with MCS, 10 with UWS, and 10 healthy controls (CG). Specifically, the video showed a first-view or third-view walk down the street while the participants were asked to imagine a first-view walking down the street.

Results: CG showed greater N190 response (low-level sensorimotor processing) in the non-matching than in the matching condition. Conversely, the P3 and RP responses (high-level sensorimotor processing) were greater in the matching than in the non-matching condition. Remarkably, 6 out of 10 patients with MCS showed the preservation of both high- and low-level sensorimotor processing. One UWS patient showed responses similar to those six patients, suggesting a preservation of cognitively-mediated sensorimotor processing despite a detrimental motor preparation process. The remaining patients with MCS did not show diversified EEG responses, suggesting limited cognitive functioning.

Conclusions: Our study suggests that identifying the low-level visual and high-level motor preparation processes in response to a simple influence of motor observation of motor imagery tasks potentially supports the clinical differential diagnosis of with MCS and UWS. This might help identify UWS patients which were misdiagnosed and who deserve more sophisticated diagnoses.
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http://dx.doi.org/10.3233/RNN-201130DOI Listing
January 2021

Hippotherapy in neurodevelopmental disorders: a narrative review focusing on cognitive and behavioral outcomes.

Appl Neuropsychol Child 2020 Dec 1:1-8. Epub 2020 Dec 1.

IRCCS Centro Neurolesi "Bonino-Pulejo", Messina, Italy.

Hippotherapy (HT) is a rehabilitative tool inducing psychological and motor improvements using human-horse interaction. HT provides sensory stimulation to the rider through the rhythmic and repetitive movements of the horse, facilitating communication between patients and healthcare professionals, favoring the establishment of a therapeutic alliance. The purpose of this review is to evaluate the effects of HT treatment on cognitive-behavioral processes in neurodevelopmental disorders. We screened studies published between 2002 and 2020 on PubMed, Scopus, Cochrane, and Web of Sciences databases. The search combined the following terms: "hippotherapy"; "horseback riding"; "equine-assisted therapy"; "developmental disorder"; "autism spectrum disorder"; "dyspraxia"; "infantile cerebral palsy"; and "attention-deficit/hyperactivity disorder". This review shows that HT can be a valuable tool for the treatment of developmental disorders. The psychological, cognitive and relational areas could benefit from the animal-child interaction to promote child autonomy, self-esteem, self-efficacy and openness to others. Physical, motor and psychosocial benefits were found in adolescents with anxiety and/or depression disorders, in autism spectrum disorders, dyspraxia, as well as in infantile cerebral palsy and attention deficit hyperactivity disorder. HT could be considered an alternative therapeutic tool thanks to the relationship between patient-horse-instructor and to the sensory-motor and cognitive stimulation that enforce learning processes.
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http://dx.doi.org/10.1080/21622965.2020.1852084DOI Listing
December 2020

A narrative review on non-invasive stimulation of the cerebellum in neurological diseases.

Neurol Sci 2021 Jun 23;42(6):2191-2209. Epub 2021 Mar 23.

IRCCS Centro Neurolesi Bonino Pulejo, via Palermo, SS113, Ctr. Casazza, 98124, Messina, Italy.

Importance: The cerebellum plays an important role in motor, cognitive, and affective functions owing to its dense interconnections with basal ganglia and cerebral cortex. This review aimed at summarizing the non-invasive cerebellar stimulation (NICS) approaches used to modulate cerebellar output and treat cerebellar dysfunction in the motor domain.

Observation: The utility of NICS in the treatment of cerebellar and non-cerebellar neurological diseases (including Parkinson's disease, dementia, cerebellar ataxia, and stroke) is discussed. NICS induces meaningful clinical effects from repeated sessions alone in both cerebellar and non-cerebellar diseases. However, there are no conclusive data on this issue and several concerns need to be still addressed before NICS could be considered a valuable, standard therapeutic tool.

Conclusions And Relevance: Even though some challenges must be overcome to adopt NICS in a wider clinical setting, this tool might become a useful strategy to help patients with lesions in the cerebellum and cerebral areas that are connected with the cerebellum whether one could enhance cerebellar activity with the intention of facilitating the cerebellum and the entire, related network, rather than attempting to facilitate a partially damaged cortical region or inhibiting the homologs' contralateral area. The different outcome of each approach would depend on the residual functional reserve of the cerebellum, which is confirmed as a critical element to be probed preliminary in order to define the best patient-tailored NICS.
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http://dx.doi.org/10.1007/s10072-021-05187-1DOI Listing
June 2021

Does embodied cognition allow a better management of neurological diseases? A review on the link between cognitive language processing and motor function.

Appl Neuropsychol Adult 2021 Mar 8:1-12. Epub 2021 Mar 8.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy.

Embodied cognition (EC) refers to the interplay occurring in thinking among individual's sensorimotor capacities (i.e., the ability of the body to respond to its senses with movement), the body itself, and the environment. The aim of the present narrative review is to provide an overall understanding of whether and how motor training could lead to language recovery, consistently with EC theories (action-perception cycle, mirror neuron systems -MNS-, and embodied semantics). We therefore reviewed the works dealing with EC in terms of the link between language processing, mirror neuron system (MNS), and motor function, evaluating the potential clinical implications for better managing neurological deficits. Connections between body and mind were found, as body states influence cognitive functions, such as perception and reasoning, as well as language processing, especially in neurological disorders. In fact, abnormalities in "embodied language" were found in movement disorders and neurodegenerative diseases, negatively affecting patients' rehabilitation outcomes. Understanding the link between language processing and motor outcomes is fundamental in the rehabilitation field, given that EC can be targeted to improve patients' functional recovery and quality of life.
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http://dx.doi.org/10.1080/23279095.2021.1890595DOI Listing
March 2021

Improvement of brain functional connectivity in autism spectrum disorder: an exploratory study on the potential use of virtual reality.

J Neural Transm (Vienna) 2021 03 6;128(3):371-380. Epub 2021 Mar 6.

IRCCS Centro Neurolesi Bonino Pulejo, via Palermo, C.da Casazza, SS113, 98124, Messina, Italy.

Patients with Autism Spectrum Disorder (ASD) need to be provided with behavioral, psychological, educational, or skill-building interventions as early as possible. Cognitive Behavior Therapy has proven useful to manage such problems. There is also growing evidence on the usefulness of Virtual Reality Therapy (VRT) in treating various functional deficits in ASD. This exploratory study is aimed at assessing the changes in cognitive functions in children with ASD, and the putative subtending neurophysiological mechanisms, following the provision of rehab training using an innovative VRT system. Twenty patients with ASD, aged 6-15 years, were provided with 24 sessions of VRT by using the pediatric module of the BTS NIRVANA System. Neuropsychological and EEG evaluations were carried out before and at the end of the training. After VRT, all patients showed a significant improvement in their cognitive-behavioral problems concerning attention processes, visuospatial cognition, and anxiety. These findings were paralleled by an evident reshape of frontoparietal connectivity in the alpha and theta frequency range. Our study suggests that VRT could be a useful and promising tool to improve ASD neurorehabilitation outcomes. This improvement is likely to occur through changes in frontoparietal network connectivity following VRT.
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http://dx.doi.org/10.1007/s00702-021-02321-3DOI Listing
March 2021

Effects of Robotic Neurorehabilitation on Body Representation in Individuals with Stroke: A Preliminary Study Focusing on an EEG-Based Approach.

Brain Topogr 2021 05 4;34(3):348-362. Epub 2021 Mar 4.

IRCCS Centro Neurolesi Bonino Pulejo - Piemonte, via Palermo, SS113, Ctr. Casazza, 98124, Messina, Italy.

Patients with stroke can experience a drastic change in their body representation (BR), beyond the physical and psychological consequences of stroke itself. Noteworthy, the misperception of BR could affect patients' motor performance even more. Our study aimed at evaluating the usefulness of a robot-aided gait training (RAGT) equipped with augmented visuomotor feedback, expected to target BR (RAGT + VR) in improving lower limb sensorimotor function, gait performance (using Fugl-Meyer Assessment scale for lower extremities, FMA-LE), and BR (using the Body Esteem Scale-BES- and the Body Uneasiness Test-BUT), as compared to RAGT - VR. We also assessed the neurophysiologic basis putatively subtending the BR-based motor function recovery, using EEG recording during RAGT. Forty-five patients with stroke were enrolled in this study and randomized with a 1:2 ratio into either the RAGT + VR (n = 30) or the RAGT - VR (n = 15) group. The former group carried out rehabilitation training with the Lokomat©Pro; whereas, the latter used the Lokomat©Nanos. The rehabilitation protocol consisted of 40 one-hour training sessions. At the end of the training, the RAGT + VR improved in FMA-LE (p < 0.001) and BR (as per BES, (p < 0.001), and BUT, (p < 0.001)) more than the RAGT- did (p < 0.001). These differences in clinical outcomes were paralleled by a greater strengthening of visuomotor connectivity and corticomotor excitability (as detected at the EEG analyses) in the RAGT + VR than in the RAGT - VR (all comparisons p < 0.001), corresponding to an improved motor programming and execution in the former group.We may argue that BR recovery was important concerning functional motor improvement by its integration with the motor control system. This likely occurred through the activation of the Mirror Neuron System secondary to the visuomotor feedback provision, resembling virtual reality. Last, our data further confirm the important role of visuomotor feedback in post-stroke rehabilitation, which can achieve better patient-tailored improvement in functional gait by means of RAGT + VR targeting BR.
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http://dx.doi.org/10.1007/s10548-021-00825-5DOI Listing
May 2021

Toward improving functional recovery in spinal cord injury using robotics: a pilot study focusing on ankle rehabilitation.

Expert Rev Med Devices 2021 Mar 5:1-13. Epub 2021 Mar 5.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy.

Conventional physical therapy interventions are strongly recommended to improve ambulation potential and upright mobility in persons with incomplete spinal cord injury (iSCI). Ankle rehabilitation plays a significant role, as it aims to stem drop foot consequences. This pilot study aimed to assess the neurophysiological underpinnings of robot-aided ankle rehabilitation (using a platform robot) compared to conventional physiotherapy and its efficacy in improving gait performance and balance in persons with iSCI. Ten individuals with subacute/chronic iSCI (six males and four females, 39 ± 13 years, time since injury 8 ± 4 months, ASIA impairment scale grade C-D) were provided with one-month intensive training for robot-aided ankle rehabilitation (24 sessions, 1 h daily, six times a week). Clinical (10-Meter Walk Test (10MWT), 6-Minute Walk Test (6MWT), and Timed Up and Go test (TUG)), and electrophysiological aftereffects (surface-EMG from tibialis anterior and medial gastrocnemius muscles to estimate muscle activation patterns; and corticomuscular coherence-CMC-to assess functional synchronization between sensorimotor cortex and muscles, i.e. the functional integrity of corticospinal output) were assessed at baseline (PRE) and after the trial completion (POST). The experimental group (EG) data were compared with those coming from a retrospective control group (CG; n = 10) matched for clinical-demographic characteristics, who previously underwent conventional ankle rehabilitation. the EG achieved a greater improvement in balance and gait as compared to the CG (TUG EG from 70 ± 18 to 45 ± 15 s, p = 0.002; CG from 68 ± 21 to 48 ± 18 s, p = 0.01; group-comparison p = 0.001; 10MWT EG from 0.43 ± 0.11 to 0.51 ± 0.09 m/s, p = 0.006; CG from 0.4 ± 0.13 to 0.45 ± 0.12, p = 0.01; group-comparison p = 0.006; 6 MWT EG from 231 ± 13 to 274 ± 15 m, p < 0.001; CG from 236 ± 13 to 262 ± 15 m, p = 0.003; group-comparison p = 0.01). Furthermore, the EG showed a retraining of muscle activation (an increase within proper movements, with a reduction of co-contractions) and CMC (beta frequency increase within proper movements, i.e. in a framework of preserved motor coordination). The improvements in CMC, gait, balance, and muscle activation were not correlated with each other. Robot-aided ankle rehabilitation improved gait performance by selectively ameliorating CMC, muscle activation patterns, and, lastly, gait balance and speed. Despite CMC, gait, balance, and muscle activation were not correlated, this pilot study suggests that robot-aided ankle rehabilitation may favor a better communication between above-SCI and below-SCI structures. This communication improvement may depend on a more synchronized corticospinal output (as per CMC increase) and a better responsiveness of below-SCI motorneurons to corticospinal output (as per specific and ankle movement focused muscle activation increases at the surface EMG), thus favoring greater recruitment of spinal motor units and, ultimately, improving muscle activation pattern and strength. Adopting robot-aided ankle rehabilitation protocols for persons with iSCI in the subacute/chronic phase may allow achieving a clinically significant improvement in gait performance.
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http://dx.doi.org/10.1080/17434440.2021.1894125DOI Listing
March 2021

'Online therapy' to reduce caregiver's distress and to stimulate post-severe acquired brain injury motor and cognitive recovery: A Sicilian hospital experience in the COVID era.

J Telemed Telecare 2021 Feb 3:1357633X21990195. Epub 2021 Feb 3.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy.

Introduction: Severe acquired brain injury(SABI) often results in the deterioration of physical, cognitive and emotional functions in the patient and a significant caregiver's distress syndrome, which is now amplified by the social isolation, depression and financial difficulties related to the COVID-19 pandemic. The use of web-based online-therapy has been shown to be useful to overcome caregiver's distress syndrome and further stimulate cognitive-motor recovery of SABI-patients. Our study aimed to investigate whether a systematic online Skype-therapy(OLST) may be of support in favoring global cognitive and sensory-motor recovery in SABI-patients and reducing caregiver distress.

Methods: Twenty-five SABI-subjects in inpatient regimen were provided with intensive OLST with the caregiver for 12 weeks in addition to standard neurorehabilitation. Each subject and caregiver was evaluated before and after the treatment by administering an ad hoc battery. Furthermore, 18 of 27 patients were provided with EEG recording in resting state.

Results: We found a significant reduction in caregiver's anxiety (p<0.0001) and burden(p<0.0001). Patients showed significant improvement in trunk control (p<0.0001), functional independence (p = 0.005), functional (p = 0.01) and global communication (p = 0.004), cognitive functioning (p = 0.001), and behavioral responsiveness (p = 0.0004). The training yielded a significant connectivity change within the fronto-centro-parietal areas in the delta frequency band (p<0.0001) and the centro-parieto-occipital areas in the alpha range (p = 0.004).

Discussion: OLST may be a useful and complementary treatment to optimize global cognitive and functional recovery in SABI-subjects and reduce caregivers' concerns in the Covid-era. OLST can foster cognitive-motor recovery potentially by favoring the plasticity-dependent functional recovery. Therefore, OLST could be proposed as a tool allowing social conversations also in the hospital setting.
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http://dx.doi.org/10.1177/1357633X21990195DOI Listing
February 2021

Can powered exoskeletons improve gait and balance in multiple sclerosis? A retrospective study.

Int J Rehabil Res 2021 06;44(2):126-130

IRCCS Centro Neurolesi 'Bonino Pulejo'.

Multiple sclerosis (MS) is a progressive neurologic disorder that can profoundly influence mobility, independence and quality of life. Gait dysfunction in MS is common, resulting in an increased risk of losing walking ability. Robotic exoskeletons have been developed to offer a new form of locomotor training. The aim of our study was to investigate the effectiveness of the powered exoskeleton (Ekso) in improving gait and balance in patients affected by MS. Twenty patients with MS (mean ± SD: age = 43.7 ± 10.3 years; 66.7% male) were enrolled in this retrospective study. They were divided into two groups, matched for demographic data (age and sex) and medical characteristics (disease duration and Expanded Disability Status Scale), but differing for the type of rehabilitation training performed. Group 1 [experimental group (EG)] received gait training with the Ekso device, whereas group 2 (control group) performed traditional gait training. Although both trainings led to a significant improvement in the ability to walk and balance, only in the EG a significant improvement in walking speed (10 Meter Walk test; P = 0.002), in person's mobility (Timed Up and Go test; P = 0.002), and in the perception of mental well-being (MSQoL-M; P = 0.004), with a good usability and acceptance of the device, was found. Powered exoskeletons could be considered a valuable tool to improve functional outcomes and get the therapeutic goal in patients with MS.
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http://dx.doi.org/10.1097/MRR.0000000000000459DOI Listing
June 2021

FRONTIERS IN DETECTING CONSCIOUSNESS: THE GROWING USE OF EEG ANALYSIS.

Innov Clin Neurosci 2020 Jul;17(7-9):8-9

IRCCS Centro Neurolesi Bonino Pulejo Messina, Italy.

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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7839660PMC
July 2020

How may patients with MS benefit from using music assisted therapy? A case-control feasability study investigating motor outcomes and beyond.

Mult Scler Relat Disord 2021 Feb 24;48:102713. Epub 2020 Dec 24.

IRCCS Centro Neurolesi "Bonino Pulejo", Messina, Italy. Electronic address:

Motor impairment is the most common symptom in multiple sclerosis (MS), as gait and balance dysfunction are reported in more than 85% of the patients, with considerable consequences on the patient's activities of daily living and psychological status. This study aimed at evaluating the feasibility and potential efficacy of a novel treatment involving music plus treadmill in patients with MS. Ten patients affected by secondary progressive MS were submitted to a specific training using the Gait Trainer (GT) 3, a platform that integrates gait training via a treadmill and rhythmic auditory stimulation. The 30 minutes training was performed three times per week for eight weeks (24 sessions in total). The enrolled patients were compared with a control group (CG) of 10 patients with MS matched for age, gender, disease duration, and EDSS stage. The CG received the same amount of treatment, but using conventional overground gait training. All patients completed the training without reporting any side effects. At the end of the training, CG improved in static and dynamic balance and in mood. Instead, in the EG a significant improvement in static and dynamic balance, walking speed, and mobility, as well as in mood, and perception of quality of life (QoL), both for physical and mental well-being, was found. This exploratory study suggests that GT3 might be a feasible and potentially useful approach for MS gait rehabilitation, thanks to patients' high motivation and good acceptance of the music assisted therapy.
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http://dx.doi.org/10.1016/j.msard.2020.102713DOI Listing
February 2021

Does overground robotic gait training improve non-motor outcomes in patients with chronic stroke? Findings from a pilot study.

J Clin Neurosci 2020 Nov 15;81:240-245. Epub 2020 Oct 15.

IRCCS Centro Neurolesi Bonino Pulejo - Piemonte, Messina, Italy. Electronic address:

Stroke is the leading cause of disability among the elderly in the industrialized world. No more than 40% of stroke survivors walk independently, and only after receiving appropriate rehabilitation treatment; many stroke patients have also non-motor symptoms. The aim of this pilot study is to evaluate the effects of Ekso-training on non-motor outcomes, including gastrointestinal function and psychological well-being, in post stroke patients. We enrolled 30 post-stroke subjects, which were randomized into two groups in order of recruitment: 15 patients were trained with the overground exoskeleton Ekso-GT (experimental group, EG), whereas 15 patients were submitted to a standard gait training (control group, CG). Both the groups underwent the same amount of physiotherapy. At the end of the training, only in the EG we observed a significant improvement in constipation, mood, and coping strategies, with regard to social support, as well as in the perception of quality of life (as per SF-12). According to these preliminary data, overground robotic gait training can be considered a valuable tool in improving non-motor symptoms, including constipation and behavioral disorders in patients with chronic stroke.
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http://dx.doi.org/10.1016/j.jocn.2020.09.070DOI Listing
November 2020

Breaking the ice to improve motor outcomes in patients with chronic stroke: a retrospective clinical study on neuromodulation plus robotics.

Neurol Sci 2021 Jul 6;42(7):2785-2793. Epub 2020 Nov 6.

IRCCS Centro Neurolesi Bonino Pulejo, via Palermo, SS 113, ctr. Casazza, 98124, Messina, Italy.

Background: Stroke is one of the main causes of impairment affecting daily activities and quality of life. There is a growing effort to potentiate the recovery of functional gait and to enable stroke patients to walk independently.

Aim: To estimate the effects of dual-site transcranial direct current stimulation (dstDCS) on gait recovery in chronic stroke patients provided with robot-aided gait training (RAGT).

Methods: Thirty-seven patients were included in this retrospective clinical study. Nine patients were provided with dstDCS during the first 10 min of RAGT by using Lokomat®Pro (on-RAGT), 15 patients immediately after RAGT (post-RAGT), and 13 patients immediately before RAGT (pre-RAGT).

Results: Each group improved over time concerning disability burden and lower limb strength. on-RAGT and post-RAGT experienced better improvement in balance (p < 0.001) and, moderately, gait endurance (p = 0.04) as compared to pre-RAGT. Furthermore, all treatments decreased the facilitation of the unaffected hemisphere (p < 0.001) and the inhibition of the affected hemisphere (p < 0.001). The duration of such aftereffects was found to be greater for post-RAGT.

Discussion And Conclusion: This is the first trial with dstDCS coupled with RAGT in chronic stroke patients with gait impairment. When timely coupled with RAGT, dstDCS may be considered an effective tool for the recovery of lower limb function in patients with first unilateral stroke in the chronic phase. Moreover, our data suggest the ductility of dstDCS concerning RAGT timing, thus making this intervention suitable in a neurorehabilitation setting and well adaptable to patients' needs.
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http://dx.doi.org/10.1007/s10072-020-04875-8DOI Listing
July 2021

Towards New Diagnostic Approaches in Disorders of Consciousness: A Proof of Concept Study on the Promising Use of Imagery Visuomotor Task.

Brain Sci 2020 Oct 17;10(10). Epub 2020 Oct 17.

IRCCS Centro Neurolesi Bonino Pulejo, SS113 C.da Casazza, 98124 Messina, Italy.

Background: advanced paraclinical approaches using functional neuroimaging and electroencephalography (EEG) allow identifying patients who are covertly aware despite being diagnosed as unresponsive wakefulness syndrome (UWS). Bedside detection of covert awareness employing motor imagery tasks (MI), which is a universally accepted clinical indicator of awareness in the absence of overt behavior, may miss some of these patients, as they could still have a certain level of awareness. We aimed at assessing covert awareness in patients with UWS using a visuomotor-guided motor imagery task (VMI) during EEG recording.

Methods: nine patients in a minimally conscious state (MCS), 11 patients in a UWS, and 15 healthy individuals (control group-CG) were provided with an VMI (imagine dancing while watching a group dance video to command), a simple-MI (imagine squeezing their right hand to command), and an advanced-MI (imagine dancing without watching a group dance video to command) to detect command-following. We analyzed the command-specific EEG responses (event-related synchronization/desynchronization-ERS/ERD) of each patient, assessing whether these responses were appropriate, consistent, and statistically similar to those elicited in the CG, as reliable markers of motor imagery.

Results: All patients in MCS, all healthy individuals and one patient in UWS repeatedly and reliably generated appropriate EEG responses to distinct commands of motor imagery with a classification accuracy of 60-80%.

Conclusions: VMI outperformed significantly MI tasks. Therefore, patients in UWS may be still misdiagnosed despite a rigorous clinical assessment and an appropriate MI assessment. It is thus possible to suggest that motor imagery tasks should be delivered to patients with chronic disorders of consciousness in visuomotor-aided modality (also in the rehabilitation setting) to greatly entrain patient's participation. In this regard, the EEG approach we described has the clear advantage of being cheap, portable, widely available, and objective. It may be thus considered as, at least, a screening tool to identify the patients who deserve further, advanced paraclinical approaches.
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http://dx.doi.org/10.3390/brainsci10100746DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7603054PMC
October 2020

Can patients with severe traumatic brain injury be trained with cognitive telerehabilitation? An inpatient feasibility and usability study.

J Clin Neurosci 2020 Sep 17;79:246-250. Epub 2020 Aug 17.

IRCCS Centro Neurolesi "Bonino Pulejo", Messina, Italy. Electronic address:

Traumatic Brain Injury (TBI) is the most common cause of long-term disability and death among young adults. Innovation technology, with regard to telerehabilitation, may be of help in managing these frail patients. The aim of the study is to evaluate whether TBI patients and caregivers are able to properly use a Tele-rehabilitation device during hospitalization. Ten TBI subjects (5 males and 5 females; mean age of 45.7 ± 14.4 years), and their caregivers (6 males and 4 females; mean age of 43.7 ± 13.5 years) were consecutively recruited in this preliminary study. After 3 meetings with the telemedicine operators aimed to provide both patients and caregivers with the basic information for the proper use of the device, patients were submitted to 6 training sessions, provided 3 times per week for two weeks, each session lasting about one hour. The telerehabilitation simulation was carried out using the tele-cockpit station and the VRRS-Tablet, used either in the patient's room or in the institute's Family Room. The motivation during training was positive, as per the Intrinsic Motivation Inventory score: 202.6 for patients and 216 for caregivers. Participants also presented positive usability scores, as per the System Usability Scale score: 68 for patients and 69 for caregivers. Our feasibility and usability study supports the idea that in-patients with severe TBI could benefit from cognitive telerehabilitation performed in the pre-discharge phase, in order to get a higher level of adherence to the home tele-treatment and potentially better outcomes.
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http://dx.doi.org/10.1016/j.jocn.2020.07.063DOI Listing
September 2020

Multiplex and Multilayer Network EEG Analyses: A Novel Strategy in the Differential Diagnosis of Patients with Chronic Disorders of Consciousness.

Int J Neural Syst 2021 Feb 9;31(2):2050052. Epub 2020 Oct 9.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy, Via Palermo, SS 113, Contrada Casazza, 98124 Messina, Italy.

The deterioration of specific topological network measures that quantify different features of whole-brain functional network organization can be considered a marker for awareness impairment. Such topological measures reflect the functional interactions of multiple brain structures, which support the integration of different sensorimotor information subtending awareness. However, conventional, single-layer, graph theoretical analysis (GTA)-based approaches cannot always reliably differentiate patients with Disorders of Consciousness (DoC). Using multiplex and multilayer network analyses of frequency-specific and area-specific networks, we investigated functional connectivity during resting-state EEG in 17 patients with Unresponsive Wakefulness Syndrome (UWS) and 15 with Minimally Conscious State (MCS). Multiplex and multilayer network metrics indicated the deterioration and heterogeneity of functional networks and, particularly, the frontal-parietal (FP), as the discriminant between patients with MCS and UWS. These data were not appreciable when considering each individual frequency-specific network. The distinctive properties of multiplex/multilayer network metrics and individual frequency-specific network metrics further suggest the value of integrating the networks as opposed to analyzing frequency-specific network metrics one at a time. The hub vulnerability of these regions was positively correlated with the behavioral responsiveness, thus strengthening the clinically-based differential diagnosis. Therefore, it may be beneficial to adopt both multiplex and multilayer network analyses when expanding the conventional GTA-based analyses in the differential diagnosis of patients with DoC. Multiplex analysis differentiated patients at a group level, whereas the multilayer analysis offered complementary information to differentiate patients with DoC individually. Although further studies are necessary to confirm our preliminary findings, these results contribute to the issue of DoC differential diagnosis and may help in guiding patient-tailored management.
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http://dx.doi.org/10.1142/S0129065720500525DOI Listing
February 2021

Effectiveness of high-frequency cervical spinal cord stimulation in the treatment of refractory trigeminal neuropathy: A case report.

Medicine (Baltimore) 2020 Oct;99(40):e22304

Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Centro Neurolesi Bonino-Pulejo, Messina, Italy.

Rationale: Treatment of chronic neuropathic pain in the head and face regions presents a challenge for pain specialists due to the lack of reliable medical and surgical approaches.

Patient Concerns: A 62-year-old patient came to our attention for an intense facial pain secondary to a lesion of the right trigeminal nerve (all branches) due to a petroclival meningioma.

Diagnoses: The patient also presented with gait impairment as well as a deficit of the right facial, auditory, trochlear and abducens cranial nerves.

Interventions: Conventional medical management (CMM) as well as tonic SCS were already adopted but they all dramatically failed. We intervened with the use of high-frequency (10 kHz) spinal cord stimulation (HFSCS) at the cervicomedullary junction (CMJ). The patient was thus provided with HFSCS at the CMJ. Pain and quality of life (QoL) were assessed 1 and 3 months after implantation. We also tested the trigeminal-facial reflex responses.

Outcomes: HFSCS led to a full relief from the debilitating electric shocks like pain in the right hemiface, even though a background dull pain appeared. The gradual addition of pregabalin helped in fully relieving the painful symptomatology, with a significant improvement in QoL. Moreover, sensitivity amelioration on the inner portion of the mouth allowed the patient to start feeding again also using that side of the mouth. These findings were paralleled by a significant reshape of trigeminal-facial reflex responses suggesting an inhibition of nociceptive sensory inputs at brainstem level following HFSCS.

Lessons: This is the first report suggesting the usefulness of HFSCS at the CMJ in neuropathic pain due to trigeminal nerve neuropathy non-responsive to tonic SCS and CMM.
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http://dx.doi.org/10.1097/MD.0000000000022304DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7535548PMC
October 2020

Robotic Rehabilitation in Spinal Cord Injury: A Pilot Study on End-Effectors and Neurophysiological Outcomes.

Ann Biomed Eng 2021 Feb 11;49(2):732-745. Epub 2020 Sep 11.

IRCCS Centro Neurolesi Bonino Pulejo, via Palermo, Ctr. Casazza SS113, 98124, Messina, Italy.

Robot-aided gait training (RAGT) has been implemented to provide patients with spinal cord injury (SCI) with a physiological limb activation during gait, cognitive engagement, and an appropriate stimulation of peripheral receptors, which are essential to entrain neuroplasticity mechanisms supporting functional recovery. We aimed at assessing whether RAGT by means of an end-effector device equipped with body weight support could improve functional ambulation in patients with subacute, motor incomplete SCI. In this pilot study, 15 patients were provided with six RAGT sessions per week for eight consecutive weeks. The outcome measures were muscle strength, ambulation, going upstairs, and disease burden. Furthermore, we estimated the activation patterns of lower limb muscles during RAGT by means of surface electromyography and the resting state networks' functional connectivity (RSN-FC) before and after RAGT. Patients achieved a clinically significant improvement in the clinical outcome measures substantially up to six months post-treatment. These data were paralleled by an improvement in the stair-climbing cycle and a potentiating of frequency-specific and area-specific RSN-FC patterns. Therefore, RAGT, by means of an end-effector device equipped with body weight support, is promising in improving gait in patients with subacute, motor incomplete SCI, and it could produce additive benefit for the neuromuscular reeducation to gait in SCI when combined with conventional physiotherapy.
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http://dx.doi.org/10.1007/s10439-020-02611-zDOI Listing
February 2021

A Case-Controlled Pilot Study on Rhythmic Auditory Stimulation-Assisted Gait Training and Conventional Physiotherapy in Patients With Parkinson's Disease Submitted to Deep Brain Stimulation.

Front Neurol 2020 4;11:794. Epub 2020 Aug 4.

IRCCS Centro Neurolesi Bonino Pulejo - Piemonte, Messina, Italy.

Deep brain stimulation (DBS) is indicated when motor disturbances in patients with idiopathic Parkinson's disease (PD) are refractory to current treatment options and significantly impair quality of life. However, post-DBS rehabilitation is essential, with particular regard to gait. Rhythmic auditory stimulation (RAS)-assisted treadmill gait rehabilitation within conventional physiotherapy program plays a major role in gait recovery. We explored the effects of a monthly RAS-assisted treadmill training within a conventional physiotherapy program on gait performance and gait-related EEG dynamics (while walking on the RAS-aided treadmill) in PD patients with ( = 10) and without DBS ( = 10). Patients with DBS achieved superior results than those without DBS concerning gait velocity, overall motor performance, and the timed velocity and self-confidence in balance, sit-to-stand (and vice versa) and walking, whereas both groups improved in dynamic and static balance, overall cognitive performance, and the fear of falling. The difference in motor outcomes between the two groups was paralleled by a stronger remodulation of gait cycle-related beta oscillations in patients with DBS as compared to those without DBS. Our work suggests that RAS-assisted gait training plus conventional physiotherapy is a useful strategy to improve gait performance in PD patients with and without DBS. Interestingly, patients with DBS may benefit more from this approach owing to a more focused and dynamic re-configuration of sensorimotor network beta oscillations related to gait secondary to the association between RAS-treadmill, conventional physiotherapy, and DBS. Actually, the coupling of these approaches may help restoring a residually altered beta-band response profile despite DBS intervention, thus better tailoring the gait rehabilitation of these PD patients.
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http://dx.doi.org/10.3389/fneur.2020.00794DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7417712PMC
August 2020

A Case of Psychogenic Myoclonus Responding to a Novel Transcranial Magnetic Stimulation Approach: Rationale, Feasibility, and Possible Neurophysiological Basis.

Front Hum Neurosci 2020 17;14:292. Epub 2020 Jul 17.

IRCCS Centro Neurolesi Bonino Pulejo, Messina, Italy.

Repetitive transcranial magnetic stimulation (rTMS) can relieve motor symptoms related to psychogenic movement disorders (PMDs), but the subtending neurophysiological basis is unclear. We report on a 50-year-old woman with a diagnosis of psychogenic myoclonus in the right lower limb, who was treated with a daily session (in the late morning/early afternoon) of 1 Hz rTMS over the left premotor cortex (PMC), five times a week for 6 weeks. Clinical data and EEG at rest were collected before and immediately and 2-month after the rTMS protocol completion. The patient reported a significant reduction of involuntary movement frequency and intensity and the related disability burden up to the follow-up. In parallel, any abnormality in terms of source current density within and connectivity between the frontal and parietal areas was reset. The short follow-up period, the lack of extensive neurophysiological measures, and the lack of control treatment represent the main limitation of the study. However, low-frequency rTMS over PMC seems a safe and promising approach for the management of psychogenic myoclonus owing to the combination of cortical neuromodulation and non-specific mechanisms suggesting cognitive-behavioral effects.
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http://dx.doi.org/10.3389/fnhum.2020.00292DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7396578PMC
July 2020
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