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Movement-related EEG signatures associated with freezing of gait in Parkinson's disease: an integrative analysis.

ABSTRACT: Freezing of gait is the most severe gait deficit associated with Parkinson's disease and significantly affects patients' independence and consequently their quality of life. The lack of a clear understanding of its underlying neurophysiological mechanism has resulted in limited effectiveness of the current treatment options. In this study, we investigated EEG features over (pre-)supplementary motor area and primary motor cortex during a simple cue-based ankle dorsiflexion movement. These features include movement-related cortical potentials (0.05-5 Hz) and brain oscillations (1-50 Hz). Electromyogram signal from the tibialis anterior muscle of the dominant foot was used to determine the movement onset. The EEG features before, during and following the onset of the movement were compared among three groups of participants: patients with freezing (N = 14, 11 males), patients without freezing (N = 14, 13 males) and healthy age-matched controls (N = 13, 10 males) with 15 recorded trials for each individual. Additionally, Parkinson's disease patients with freezing of gait were separated into mild (N = 7) and severe cases (N = 5), so that EEG features associated with freezing severity could be investigated. The results indicated significant differences between patients with severe freezing of gait compared to healthy controls and patients without freezing of gait. In addition, patients with mild and severe freezing represented cortical activity differences. For patients with freezing, the initial component of movement-related cortical potential is significantly lower than that of the healthy controls (P = 0.002) and is affected by the severity of freezing. Furthermore, a striking absence of beta frequency band (12-35 Hz) desynchronization was observed in patients with freezing, especially low-beta frequency band over Cz, before the movement, which was also associated with the severity of the freezing of gait. Low-beta (13-20 Hz) and high-beta (21-35 Hz) frequency band activities represented unique features for each group. Beta event-related desynchronization over Cz present in healthy controls prior to movement onset, was partially replaced by the theta band (4-8 Hz) synchrony in patients with freezing. Patients with severe freezing also represented some level of theta band synchronization over contralateral supplementary motor area. This suggests the involvement of cognitive processing over the motor cortex in controlling cue-based voluntary movement as a compensatory mechanism associated with freezing of gait. The EEG features identified in this study are indicative of important freezing of gait clinical characteristics such as severity and contribute to a better understanding of the underlying neurophysiology of the mysterious phenomenon of freezing of gait.

SUBMITTER: Karimi F

PROVIDER: S-EPMC8643573 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Freezing of gait (FOG) is arguably the most severe symptom associated with Parkinson's disease (PD), and often occurs while performing dual tasks or approaching narrowed and cluttered spaces. While it is well known that visual cues alleviate FOG, it is not clear if this effect may be the result of cognitive or sensorimotor mechanisms. Nevertheless, the role of vision may be a critical link that might allow us to disentangle this question. Gaze behaviour has yet to be carefully investigated while freezers approach narrow spaces, thus the overall objective of this study was to explore the interaction between cognitive and sensory-perceptual influences on FOG. In experiment #1, if cognitive load is the underlying factor leading to FOG, then one might expect that a dual-task would elicit FOG episodes even in the presence of visual cues, since the load on attention would interfere with utilization of visual cues. Alternatively, if visual cues alleviate gait despite performance of a dual-task, then it may be more probable that sensory mechanisms are at play. In compliment to this, the aim of experiment#2 was to further challenge the sensory systems, by removing vision of the lower-limbs and thereby forcing participants to rely on other forms of sensory feedback rather than vision while walking toward the narrow space. Spatiotemporal aspects of gait, percentage of gaze fixation frequency and duration, as well as skin conductance levels were measured in freezers and non-freezers across both experiments. Results from experiment#1 indicated that although freezers and non-freezers both walked with worse gait while performing the dual-task, in freezers, gait was relieved by visual cues regardless of whether the cognitive demands of the dual-task were present. At baseline and while dual-tasking, freezers demonstrated a gaze behaviour that neglected the doorway and instead focused primarily on the pathway, a strategy that non-freezers adopted only when performing the dual-task. Interestingly, with the combination of visual cues and dual-task, freezers increased the frequency and duration of fixations toward the doorway, compared to non-freezers. These results suggest that although increasing demand on attention does significantly deteriorate gait in freezers, an increase in cognitive demand is not exclusively responsible for freezing (since visual cues were able to overcome any interference elicited by the dual-task). When vision of the lower limbs was removed in experiment#2, only the freezers' gait was affected. However, when visual cues were present, freezers' gait improved regardless of the dual-task. This gait behaviour was accompanied by greater amount of time spent looking at the visual cues irrespective of the dual-task. Since removing vision of the lower-limbs hindered gait even under low attentional demand, restricted sensory feedback may be an important factor to the mechanisms underlying FOG.

Project description:Background:Freezing of gait (FOG) is a common, disabling symptom of Parkinson's disease (PD), but the mechanisms and treatments of FOG remain great challenges for clinicians and researchers. The main focus of this review is to summarize the possible mechanisms underlying FOG, the risk factors for screening and predicting the onset of FOG, and the clinical trials involving various therapeutic strategies. In addition, the limitations and recommendations for future research design are also discussed. Main body:In the mechanism section, we briefly introduced the physiological process of gait control and hypotheses about the mechanism of FOG. In the risk factor section, gait disorders, PIGD phenotype, lower striatal DAT uptake were found to be independent risk factors of FOG with consistent evidence. In the treatment section, we summarized the clinical trials of pharmacological and non-pharmacological treatments. Despite the limited effectiveness of current medications for FOG, especially levodopa resistant FOG, there were some drugs that showed promise such as istradefylline and rasagiline. Non-pharmacological treatments encompass invasive brain and spinal cord stimulation, noninvasive repetitive transcranial magnetic stimulation (rTMS) or transcranial direct current stimulation (tDCS) and vagus nerve stimulation (VNS), and physiotherapeutic approaches including cues and other training strategies. Several novel therapeutic strategies seem to be effective, such as rTMS over supplementary motor area (SMA), dual-site DBS, spinal cord stimulation (SCS) and VNS. Of physiotherapy, wearable cueing devices seem to be generally effective and promising. Conclusion:FOG model hypotheses are helpful for better understanding and characterizing FOG and they provide clues for further research exploration. Several risk factors of FOG have been identified, but need combinatorial optimization for predicting FOG more precisely. Although firm conclusions cannot be drawn on therapeutic efficacy, the literature suggested that some therapeutic strategies showed promise.

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Movement-related EEG signatures associated with freezing of gait in Parkinson's disease: an integrative analysis.

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