Research ArticleEnhanced Obstacle Contrast to Promote Visual Scanning in Fallers with Parkinson’s Disease: Role of Executive Function
Introduction
Visual complaints are common in older adults with Parkinson’s disease (PD) with three in every four people with PD reporting visual disturbance (Davidsdottir et al., 2005). Ocular deficits arise from deposition of α-synuclein and dopamine deficiency in the retina reflecting underlying PD pathology (Guo et al., 2018) as well as age-related pathology. Visual impairments are evident throughout the visual pathway (Biousse et al., 2004, Davidsdottir et al., 2005, Weil et al., 2016, Ekker et al., 2017) ranging from movement of the eye and eye lid (bradykinesia and saccadic hypokinesia, impaired convergence and inhibition of return), to the retina (impaired contrast sensitivity and colour discrimination) through to the optic nerve, the lateral geniculate and visual cortex (glaucoma, hallucinations and poor visuo-spatial ability) (Ekker et al., 2017). Of particular importance is contrast sensitivity, which represents the ability to differentiate objects from their background. Adequate contrast sensitivity serves as a critical visual function that may also be influenced by external factors such as the time of day (poorer luminance at night), weather conditions (fog, heavy rain), inadequate lighting or interior design (colour scheme with little contrast variation). Contrast sensitivity is important for identifying objects, judging their locality and evaluating depth and distance ultimately to facilitate safe and effective navigation of complex environments, and is frequently impaired in PD compared to age-matched controls (Pieri et al., 2000, Nowacka et al., 2014).
Negotiating a ground-based obstacle safely requires online visual input and sensory feedback enabling adaptive feedforward control of dynamic balance (Patla and Greig, 2006). Acquisition of visual information from the environment, termed exteroreceptive input (Patla, 1998), is important during obstacle crossing in people with PD (Pieruccini-Faria et al., 2014b, Vitório et al., 2012, Vitório et al., 2013). Almost a third of all falls in people with PD occur as a result of a trip (Stolze et al., 2004) and over 80% of people with PD who fall have impaired vision (Wood et al., 2002). Thus measuring gaze behaviour during complex tasks, such as obstacle crossing which may be particularly hazardous for people with PD, is important for understanding fall risk and developing effective interventions.
A key contributing factor to visual control in people with PD is cognitive deficit which is evident even in early disease (Getz and Levin, 2017). Visuospatial function, attention and executive function are primarily affected (Dubois and Pillon, 1996) and associated with increased fall risk (Hausdorff et al., 2006, Allcock et al., 2009). Cognitive impairment impacts on visual search as well as retrieval and interpretation of visual information in a ‘top down’ manner (Connor et al., 2004, Possin, 2010). Evidence from studies using paper- and computer-based tests report slower processing speeds, reduced set-shifting ability (executive function), and attentional deficit including reduced attentional capacity, an inability to sustain attention and difficulty allocating attentional resources appropriately in people with PD (Richards et al., 1993, Sawamoto et al., 2002, Zgaljardic et al., 2003, Kudlicka et al., 2011). Competition for attentional resources increases in natural settings where other factors increase task complexity (i.e. a greater number of visual stimuli exist within cluttered environments and when engaging in cognitive-motor dual tasks, such as having a conversation and negotiating obstacles concurrently).
One approach to optimising obstacle negotiation is to direct attention to the obstacle by increasing obstacle saliency. This may prompt preparatory motor planning and improve interpretation of obstacle parameters (shape, size, vicinity) which is particularly relevant for people with PD who demonstrate reduced visual exploration when interpreting environmental cues compared to controls (Vitório et al., 2014, Vitório et al., 2016). Previous work reports a significant association between obstacle visibility and risk of obstacle contact, even in young adults with normal visual function (Rietdyk and Rhea, 2011), suggesting the strategy is broadly adopted. Artificially creating a low environmental contrast serves as a proxy for inducing similar visual conditions experienced by people with PD. Using such a paradigm is informative for understanding the visuo-motor strategies used by healthy older adults when negotiating low contrast obstacles. It also provides the opportunity to examine the effect of enhanced obstacle contrast on performance in people with and without PD.
The primary aim of this study was to explore gaze behaviour in people with PD and controls when approaching obstacles of high and low contrast. We hypothesised that people with PD would spend longer looking at the obstacle compared to controls and that these differences would be more pronounced when approaching the low contrast obstacle due to limited salience. A secondary aim was to investigate the relationship between visual and cognitive function and gaze location when approaching a high and low contrast obstacle.
Section snippets
Participants
Seventeen people with PD who presented with a history of falls (n = 17) participated. Participants with PD were included provided they: reported at least two falls in the 6-months prior to participation; were aged 60–90 years; had adequate hearing and vision; and had stable medication in the month prior to recruitment. Exclusion criteria included moderate-to-severe cognitive impairment (defined as Mini Mental State Exam score <21/30; MMSE (Folstein et al., 1975)), considerable visual or
Results
The PD group were older and had an increased body mass compared to the control group, and also experienced poorer visual function (contrast sensitivity) (Table 1; p < .05). Despite evidence of visual impairment, the PD group were considered to be of mild to moderate disease severity with 72% of the sample categorised as Hoehn & Yahr stage II and less than half reporting FOG (Table 2). No freezing episodes were observed during the gait assessment.
Discussion
This study investigated the differences in gaze behaviour when approaching obstacles of high and low contrast in a group of people with PD with a history of falls. Disease-specific differences in gaze behaviour were quantified using a group of non-falling, cognitively intact older adults with no visual impairments as our reference group. Our findings suggest that enhancing obstacle contrast alters the content of visual information acquired. PD approached the low contrast obstacle more
CRediT authorship contribution statement
Lisa Alcock: Conceptualization, Writing - original draft, Visualization. Brook Galna: Writing - review & editing. Jeffrey M. Hausdorff: Writing - review & editing. Sue Lord: Writing - review & editing. Lynn Rochester: Writing - review & editing.
Acknowledgements
The research was supported by the National Institute for Health Research (NIHR) Newcastle Biomedical Research Unit based at Newcastle Hospitals NHS Foundation Trust and Newcastle University. The research was also supported by NIHR Newcastle CRF Infrastructure funding. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. This work was funded by a European Union 7th Framework Programme (FP7) under the Health theme (FP7 – 278169,
Declarations of interest
None.
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