Cortical Correlates of Gait Compensation Strategies in Parkinson Disease

Tosserams, Anouk; Weerdesteyn, Vivian; Bal, Tess; Bloem, Bastiaan R.; Solis‐Escalante, Teodoro; Nonnekes, Jorik

doi:10.1002/ana.26306

Cited by 26 publications

(25 citation statements)

References 60 publications

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“…These results provide evidence for the notion that application of a cognitive movement strategy poses attentional demands. Furthermore, this finding strengthens recent reports that indicated that different cortical mechanisms underlie external cueing and cognitive movement compensatory strategies ( Stuart and Mancini, 2020 ; Tosserams et al, 2022 ).…”

Section: Discussionsupporting

confidence: 90%

Compensatory movement strategies differentially affect attention allocation and gait parameters in persons with Parkinson’s disease

Yogev‐Seligmann

Krasovsky

Kafri

2022

Front. Hum. Neurosci.

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Persons with Parkinson’s disease (PwP) are advised to use compensatory strategies such as external cues or cognitive movement strategies to overcome gait disturbances. It is suggested that external cues involve the processing of sensory stimulation, while cognitive-movement strategies use attention allocation. This study aimed to compare over time changes in attention allocation in PwP between prolonged walking with cognitive movement strategy and external cues; to compare the effect of cognitive movement strategies and external cues on gait parameters; and evaluate whether these changes depend on cognitive function. Eleven PwP participated in a single-group pilot study. Participants walked for 10 min under each of three conditions: natural walking, using external cuing, using a cognitive movement strategy. Attention and gait variables were extracted from a single-channel electroencephalogram and accelerometers recordings, respectively. Attention allocation was assessed by the% of Brain Engagement Index (BEI) signals within an attentive engagement range. Cognitive function was assessed using a neuropsychological battery. The walk was divided into 2-min time segments, and the results from each 2-min segment were used to determine the effects of time and condition. Associations between cognitive function and BEI signals were tested. Findings show that in the cognitive movement strategy condition, there was a reduction in the % of BEI signals within the attentive engagement range after the first 2 min of walking. Despite this reduction the BEI did not consistently differ from natural and metronome walking. Spatiotemporal gait variables were better in the cognitive movement strategy condition relative to the other conditions. Global cognitive and information processing scores were significantly associated with the BEI only when the cognitive movement strategy was applied. In conclusion, the study shows that a cognitive movement strategy has positive effects on gait variables but may impose a higher attentional load. Furthermore, when walking using a cognitive movement strategy, persons with higher cognitive function showed elevated attentive engagement. The findings support the idea that cognitive and attentional resources are required for cognitive movement strategies in PwP. Additionally, this study provides support for using single-channel EEG to explore mechanistic aspects of clinical interventions.

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Section: Discussionsupporting

confidence: 90%

Compensatory movement strategies differentially affect attention allocation and gait parameters in persons with Parkinson’s disease

Yogev‐Seligmann

Krasovsky

Kafri

2022

Front. Hum. Neurosci.

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“…Only the gamma band power of the parieto-occipital region decreased in non-responders. These findings support the results of previous interventions for PD showing that transcranial alternating current stimulation (tACS) (Del Felic et al, 2019) and the use of gait compensation strategies (Tosserams et al, 2022) to improve PD motor symptoms were closely related to decreased beta oscillation.…”

Section: Discussionsupporting

confidence: 88%

Characterizing cortical responses to short-term multidisciplinary intensive rehabilitation treatment in patients with Parkinson’s disease: A transcranial magnetic stimulation and electroencephalography study

Pei

Liu

Huang

et al. 2022

Front. Aging Neurosci.

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Combined transcranial magnetic stimulation and electroencephalography (TMS-EEG) is a powerful non-invasive tool for qualifying the neurophysiological effects of interventions by recording TMS-induced cortical activation with high temporal resolution and generates reproducible and reliable waves of activity without participant cooperation. Cortical dysfunction contributes to the pathogenesis of the clinical symptoms of Parkinson’s disease (PD). Here, we examined changes in cortical activity in patients with PD following multidisciplinary intensive rehabilitation treatment (MIRT). Forty-eight patients with PD received 2 weeks of MIRT. The cortical response was examined following single-pulse TMS over the primary motor cortex by 64-channel EEG, and clinical symptoms were assessed before and after MIRT. TMS-evoked potentials were quantified by the global mean field power, as well as oscillatory power in theta, alpha, beta, and gamma bands, and their clinical correlations were calculated. After MIRT, motor and non-motor symptoms improved in 22 responders, and only non-motor function was enhanced in 26 non-responders. Primary motor cortex stimulation reduced global mean field power amplitudes in responders but not significantly in non-responders. Oscillations exhibited attenuated power in the theta, beta, and gamma bands in responders but only reduced gamma power in non-responders. Associations were observed between beta oscillations and motor function and between gamma oscillations and non-motor symptoms. Our results suggest that motor function enhancement by MIRT may be due to beta oscillatory power modulation and that alterations in cortical plasticity in the primary motor cortex contribute to PD recovery.

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“…Adequate gait control therefore not only relies on the integrity and function of corticostriatal motor loops, but on compensatory input from cognitive, sensory and limbic systems as well (Fig. 2 ) [ 47 – 50 ]. Reinforcing the integration of these different neural networks may consequently facilitate optimal compensation for the PD-related loss of function in the motor circuitries.…”

Section: Discussionmentioning

confidence: 99%

Modulating arousal to overcome gait impairments in Parkinson’s disease: how the noradrenergic system may act as a double-edged sword

Tosserams

Bloem

Martens

et al. 2023

Transl Neurodegener

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In stressful or anxiety-provoking situations, most people with Parkinson’s disease (PD) experience a general worsening of motor symptoms, including their gait impairments. However, a proportion of patients actually report benefits from experiencing—or even purposely inducing—stressful or high-arousal situations. Using data from a large-scale international survey study among 4324 people with PD and gait impairments within the online Fox Insight (USA) and ParkinsonNEXT (NL) cohorts, we demonstrate that individuals with PD deploy an array of mental state alteration strategies to cope with their gait impairment. Crucially, these strategies differ along an axis of arousal—some act to heighten, whereas others diminish, overall sympathetic tone. Together, our observations suggest that arousal may act as a double-edged sword for gait control in PD. We propose a theoretical, neurobiological framework to explain why heightened arousal can have detrimental effects on the occurrence and severity of gait impairments in some individuals, while alleviating them in others. Specifically, we postulate that this seemingly contradictory phenomenon is explained by the inherent features of the ascending arousal system: namely, that arousal is related to task performance by an inverted u-shaped curve (the so-called Yerkes and Dodson relationship). We propose that the noradrenergic locus coeruleus plays an important role in modulating PD symptom severity and expression, by regulating arousal and by mediating network-level functional integration across the brain. The ability of the locus coeruleus to facilitate dynamic ‘cross-talk’ between distinct, otherwise largely segregated brain regions may facilitate the necessary cerebral compensation for gait impairments in PD. In the presence of suboptimal arousal, compensatory networks may be too segregated to allow for adequate compensation. Conversely, with supraoptimal arousal, increased cross-talk between competing inputs of these complementary networks may emerge and become dysfunctional. Because the locus coeruleus degenerates with disease progression, finetuning of this delicate balance becomes increasingly difficult, heightening the need for mental strategies to self-modulate arousal and facilitate shifting from a sub- or supraoptimal state of arousal to improve gait performance. Recognition of this underlying mechanism emphasises the importance of PD-specific rehabilitation strategies to alleviate gait disability.

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Cortical Correlates of Gait Compensation Strategies in Parkinson Disease

Cited by 26 publications

References 60 publications

Compensatory movement strategies differentially affect attention allocation and gait parameters in persons with Parkinson’s disease

Compensatory movement strategies differentially affect attention allocation and gait parameters in persons with Parkinson’s disease

Characterizing cortical responses to short-term multidisciplinary intensive rehabilitation treatment in patients with Parkinson’s disease: A transcranial magnetic stimulation and electroencephalography study

Modulating arousal to overcome gait impairments in Parkinson’s disease: how the noradrenergic system may act as a double-edged sword

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