Influence of visual cues on gait in Parkinson's disease: Contribution to attention or sensory dependence?

doi:10.1016/j.jns.2006.05.008

Journal of the Neurological Sciences

Volume 248, Issues 1–2, 25 October 2006, Pages 192-195

https://doi.org/10.1016/j.jns.2006.05.008 Get rights and content

Abstract

Sensory cueing is used for a long time to improve gait in patients with Parkinson's disease. This has been established for visual cues such as stripes on floor and for rhythmic auditory cues. Concerning visual cueing two main mechanisms of action have been suggested and may be suitable depending on the instruction given to the patients. Stripes placed on the walking surface may draw attention to the stepping process if patients are talked to put their feet on the stripes. In another paradigm, the stripes on floor are just used to enhance the optical flow and the motion of the stripes is essential to improve gait. These findings are not found in normal controls suggesting that patients with Parkinson's disease are more dependent on dynamic visual cues for gait control than controls. Several common characteristics exist between attention and sensory contribution in gait control. First, their potential beneficial effect may be contre-balanced by a negative influence: visual information may be helpful for gait in patients or may disrupt locomotion and induce freezing (for example passing a door). Attention focused on gait allows a partial correction of the troubles by intentional modulation of the stride length but a dual task flowing attention away produces deterioration. Another point is that both strategies are probably used by the central nervous system to compensate deficits: visual dependence to compensate an impaired kinesthetic feed-back and attentional processing to alleviate automaticity in locomotion and so, to by-pass the deficit of internal cueing.

Introduction

Several studies have shown that sensory and attentional stimuli play important role in gait. A common paradigm was used (stripes on floor) in different works to demonstrate both effects. We will review the main experimental results demonstrating the role of each factor and will try to show the possible imbalance that may exist between sensory inputs and attention.

Section snippets

Gait in Parkinson's disease

Gait in Parkinson's disease (PD) belong to the group of hypokinetic gait characterized by a decreased stride length which is probably the most frequent gait trouble representing 35% of all the gait disorders [1]. Normal pressure hydrocephalus and PD are the two main diseases of this group, the others being progressive supranuclear palsy, artherioclerotic encephalopathy, Alzheimer's disease. The common findings in this group are a reduced stride length and a reduced velocity. In PD, some more

Attention and locomotion

External visual cues may act to focus attention on the stride length process. In this case, people are asked to walk on the stripes to normalize their stride length. Patients with PD are able to do so even if they are not able when relying on internal cues, and they normalize also their cadence and their velocity demonstrating that the internal regulation of stride length is the fundamental deficit in gait hypokinesia [7]. Moreover, when patients are trained with visual cues or with a mental

Visual control of locomotion

During locomotion, it is possible to differentiate static visual cues that are available in a single flash of stroboscopic light, namely position and orientation visual cues, from dynamic visual cues that are perceptible under permanent illumination and are involved in the visual perception of movement produced by the subject's own actions (16), also called optic flow. Dynamic visual cues have been shown to provide an important contribution to body balance, in standing [15] as well as in

Common mechanisms between sensory integration and attention

It appears from these different experiments that external visual cueing may be effective to improve locomotion in PD because it may compensate 2 different deficits depending on the experimental paradigm: normalization of the deficit of internal cueing when patients are instructed to step on the markers because the visual cues draw attention to the stepping process and reduce the degree of automaticity of locomotion or compensation of a deficit of proprioceptive integration when visual cues

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An executive dysfunction is supposed to contribute to freezing of gait (FoG) in Parkinson’s disease. We aimed to investigate at a behavioral and cortical levels whether an attentional load (particularly, a conflicting situation) can specifically impact preparation and execution phases of step initiation in parkinsonian patients with FoG.
Fifteen patients with FoG, 16 without and 15 controls performed an adapted version of the Attention Network Test, with step initiation as response instead of the standard manual keypress. Kinetic and kinematic features of gait initiation as well as high-resolution electroencephalography were recorded during the task.
Patients with FoG presented an impaired executive control. Step execution time was longer in parkinsonian patients. However, the executive control effect on step execution time was not different between all groups. Compared to patients, controls showed a shorter step initiation-locked alpha desynchronization, and an earlier, more intense and shorter beta desynchronization over the sensorimotor cortex. Even though controls were faster, the induced alpha and beta activity associated with the effect of executive control didn’t differ between patients and controls.
Tasks of conflict resolution lead to a comparable alteration of step initiation and its underlying brain activity in all groups. Links between executive control, gait initiation and FoG seem more complex than expected.
This study questions the cognitive hypothesis in the pathophysiology of freezing of gait. Executive dysfunction is associated with FoG but is not the main causal mechanism since the interaction between attention and motor preparation didn’t provoke FoG.
Imaging the neural underpinnings of freezing of gait in Parkinson's disease
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Freezing of gait (FoG) is a paroxysmal and sporadic gait impairment that severely affects PD patients’ quality of life. This review summarizes current neuroimaging investigations that characterize the neural underpinnings of FoG in PD. The review presents and discusses the latest advances across multiple methodological domains that shed light on structural correlates, connectivity changes, and activation patterns associated with the different pathophysiological models of FoG in PD. Resting-state fMRI studies mainly report cortico-striatal decoupling and disruptions in connectivity along the dorsal stream of visuomotor processing, thus supporting the ‘interference’ and the ‘perceptual dysfunction’ models of FoG. Task-based MRI studies employing virtual reality and motor imagery paradigms reveal a disruption in functional connectivity between cortical and subcortical regions and an increased recruitment of parieto-occipital regions, thus corroborating the ‘interference’ and ‘perceptual dysfunction’ models of FoG. The main findings of fNIRS studies of actual gait primarily reveal increased recruitment of frontal areas during gait, supporting the ‘executive dysfunction’ model of FoG. Finally, we discuss how identifying the neural substrates of FoG may open new avenues to develop efficient treatment strategies.
Effects of rhythmic visual cues on cognitive resources allocation characterized by electroencephalographic (EEG) features during human gait initiation
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Rhythmic visual cues are beneficial in gait initiation (GI) in Parkinson's disease patients with freezing of gait (FOG), however, the underlying neurophysiological mechanism remains poorly understood. The cognitive control modulated by visual cues during GI has been investigated and considered as a potential factor influencing automatic motor actions, but it is unclear how rhythmic visual cues affect cognitive resources demands during GI. The purpose of this study was to explore the effect of rhythmic visual cues on cognitive resources allocation by recording the anticipatory cerebral cortex electroencephalographic (EEG) activity during GI. Twenty healthy participants initiated gait in response to the rhythmic and non-rhythmic visual cues of stimulus presentation. We assessed the contingent negative variation (CNV) of averaged EEG data over 32 electrode positions during GI preparation, the results of which showed that the CNV was induced over prefrontal, frontal, central, and parietal regions in both rhythmic conditions and non-rhythmic conditions. Overall, different visual cues modulated the amplitude of CNV in the early and late stages of the GI preparation. Compared with the non-rhythmic condition, the CNV amplitude was lower in rhythmic condition over displayed regions precede the GI onset. In the late stage of GI preparation, it showed significant differences between the two conditions in prefrontal, frontal, and central regions, and the amplitude of CNV was lower under rhythmic condition. More to the point, the differences were more obvious in the late stage of GI preparation between the two conditions, which was closely associated with the cognitive resources. Therefore, the results indicate that less cognitive resources allocation is required to trigger GI under rhythmic visual cues compared with non-rhythmic visual cues. This study may provide a new insight into why rhythmic visual cues are more effective in improving GI ability compared to non-rhythmic visual cues.
Sensory reweighting in frail aged adults: Are the balance deficiencies mainly compensated by visual or podal dependences?
2021, Neuroscience Letters
Citation Excerpt :
People who have suffered a stroke are increasingly visually dependent when controlling their posture. In the field of pathological aging, visual dependence is documented in people with Parkinson's disease [8]. However, normal aging leads to potential alterations in the three main sources of sensory information: a reduction in the functional capacities of vision, an impairment of vestibular reflexes and somaesthetic mechanoreceptors.
Postural control is based on the integration of different sensory inputs. The process of scaling the relative importance of these sensory cues (visual, vestibular and proprioceptive) depends on individuals and creates sensory preferences, leading to sensory dependences when one particular source is preponderant. In this context, the literature showed a frequent visual dependence (visual inputs weighting) in aged adults. However, the somaesthetic inputs can also be prioritised in a podal-dependent profile. In the frail aged adults, none study has shown the distribution of these two dependences.
Which sensory orientation profile is preferentially adopted by frail aged males and females?
In this cross-sectional study, we compared 33 frail aged adults to 16 non frail aged adults during a static postural control task in three conditions on a force platform: i) a standard condition, ii) a no-vision condition and iii) a foam condition. An analysis with the factor sex was also performed in each group of participants.
The analysis of stabilometric parameters (mean velocity and mean velocity variance) highlighted a significant difference in no-vision or foam conditions when compared to the standard condition in frail aged males and only in the foam condition when compared to the standard condition for females in the frail group. No significant difference was observed between conditions in the control group.
Our study showed the predominance of both visual and podal information in frail aged adults when controlling their posture. Considering the sex factor, frail males were more dependents to their visual cues than frail females. This result should be used when designing the rehabilitation programs in this population.
The neuropathological basis of anxiety in Parkinson's disease
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Evidence suggests that 24.5%–46.7% (mean 31%) of patients with Parkinson’s disease experience an anxiety disorder, a much higher prevalence than in controls. Anxiety does not appear to be a consequence of diagnosis or the motoric symptoms of the disorder and can manifest as Generalised Anxiety Disorder, phobias or panic attacks. At present, the neural underpinnings of anxiety disorders in Parkinson’s disease is unknown. Here, we make the novel proposal that the superior colliculus (SC), one component of a rapid, reflexive threat detection system in the brain, consisting of the colliculus, pulvinar and amygdala, becomes hyper-responsive to sensory stimuli following dopamine denervation of the striatum in Parkinson’s disease. This in turn leads to heightened responses to existing threat-related stimuli (giving rise to phobias and panic attacks), and heightened responses to anticipated threats (giving rise to Generalised Anxiety Disorder). This proposal is supported by a range of evidence, in particular elevated visual responses in the SC in an animal model of Parkinson’s disease and in Parkinson’s disease itself. Also facilitated saccadic eye movements (prosaccades, express saccades and fixational saccades) and increased distractibility in Parkinson’s disease, both of which involve the SC. Identifying one potential locus of change in the brain in Parkinson’s disease relevant to anxiety gives a potential target for interventions to combat a non-motor symptom that has a substantial negative effect on quality of life in the disorder.
Linking anxiety, cognitive and sensory deficits to gait and balance deficits in Parkinson’s disease
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Deficits of gait and balance have a dramatic impact on quality of life and independence and hence are arguably the most debilitating symptoms associated with Parkinson's disease (PD). Perhaps more importantly, these deficits can serve as a valuable model that sheds light on mechanisms underlying all motor symptoms in PD and other movement disorders. This chapter will systematically consider important factors that likely interact to impact gait, posture, and other motor impairments in PD. One example is the so-called “freezing phenomena,” where patients report that their feet are glued to the ground, unable to initiate their next step, leading to much greater risk of falls and injury. This makes “freezing” one of the most severe gait and balance issues associated with advanced PD. Understanding the underlying mechanisms of these impairments has the potential to uncover new therapeutic interventions for PD.

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Influence of visual cues on gait in Parkinson's disease: Contribution to attention or sensory dependence?

Abstract

Introduction

Section snippets

Gait in Parkinson's disease

Attention and locomotion

Visual control of locomotion

Common mechanisms between sensory integration and attention

Arch Phys Med Rehabil

Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson's disease

J Neurol Neurosurg Psychiatry

Ability to modulate walking cadence remains intact in Parkinson's disease

J Neurol Neurosurg Psychiatry

Verbal fluency task affects gait in Parkinson's disease with motor freezing

J Geriatr Psychiatry Neurol

Dual task interference during gait in people with Parkinson disease: effects of motor versus cognitive secondary tasks

Phys Ther

The basal ganglia and posture

Is parkinsonian gait caused by a regression to an immature walking pattern?

Adv Neurol

The pathogenesis of gait hypokinesia in Parkinson's disease

Brain

Analyse cinématique de la marche du parkinsonien: effet de la levodopa et de stimulations visuelles

Rev Neurol

Motor function of the monkey globus pallidus. Neuronal discharge and parameters of movement

Brain

An evaluation of the role of internal cues in the pathogenesis of parkinsonian hypokinesia

Brain

Impaired simultaneous cognitive task performance in Parkinson's disease: a dopamine-related dysfunction

Neurology