Enhanced Obstacle Contrast to Promote Visual Scanning in Fallers with Parkinson’s Disease: Role of Executive Function

Highlights

• PD approached the low contrast obstacle slower than controls.

• PD spent longer looking at the obstacle compared to controls regardless of contrast.

• PD looked at the ground beyond the low contrast obstacle less than controls.

• Gaze location was associated with executive function and not visual function in PD.

• Enhancing obstacle contrast may improve online processing of environmental cues.

Abstract

The ability to perceive differences in environmental contrast is critical for navigating complex environments safely. People with Parkinson’s disease (PD) report a multitude of visual and cognitive deficits which may impede safe obstacle negotiation and increase fall risk. Enhancing obstacle contrast may influence the content of visual information acquired within complex environments and thus target environmental fall risk factors. 17 PD with a history of falls and 18 controls walked over an obstacle covered in a high and low contrast material in separate trials whilst eye movements were recorded. Measures of visual function and cognition were obtained. Gaze location was extracted during the approach phase. PD spent longer looking at the obstacle compared to controls regardless of contrast (p < .05), however group differences were largest for the low contrast obstacle. When accounting for group differences in approach time, PD spent longer looking at the low contrast obstacle and less time looking at the ground beyond the low contrast obstacle compared to controls (p < .05). The response to obstacle contrast in PD (high-low) was significantly associated with executive function. Better executive function was associated with spending longer looking at the low contrast obstacle and at the ground beyond the high contrast obstacle. Enhancing the contrast of ground-based trip hazards may improve visual processing of environmental cues in PD, particularly for individuals with better executive function. Manipulating contrast to attract visual attention is already in use in the public domain, however its utility for reducing fall risk in PD is yet to be formally tested in habitual settings.

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.