Clinical NeuroscienceThe measurement of visual sampling during real-world activity in Parkinson's disease and healthy controls: A structured literature review
Introduction
Visual sampling (VS) is the combination of fixations and saccades that are required to gather information about our environment when performing a real-world activity. VS has been assessed using a variety of methods since the 1700s, evolving from simple photographic technology to more recently the use of mobile infra-red eye-tracking (Land, 2006, Porterfield, 1752). Eye-tracking involves two distinguishable movements of the eye; activity that stabilises the fovea (fixations) on areas of interest (AOI), and activity that rapidly shifts the fovea to bring AOI into high visual acuity (saccades) (Anderson and MacAskill, 2013). A combination of fixations and saccades provide the mechanisms through which we sample our visual environment (McPeek et al., 2000, Deubel, 2003, Tatler, 2009). Advancements in eye-tracking technology have enabled VS to be monitored during real-world activity (e.g. walking, obstacle crossing, driving). This progress is vital as VS is a critical feature of motor control, which is task-dependent and relates to specific goals (Marigold and Patla, 2007). For example: during locomotion over even ground in healthy control subjects long fixation durations are not necessarily required, yet saccadic frequency, amplitude and duration of fixations increase in healthy subjects when walking over uneven terrain (Land, 2006, Patla and Greig, 2006). The co-ordination of the eyes, head, trunk and other body segments during real-world activity requires visuomotor control to guide and organise linked-segment interactions. Motor control and visual mechanisms are also inter-linked with attentional networks, which are governed by cognitive (‘top-down’) processes (Botha and Carr, 2012). Therefore, disease-specific impairments of motor control (Joti et al., 2007, Konczak et al., 2009) and cognition (Archibald et al., 2013) potentially mediate visual function.
Parkinson's disease (PD) is a progressive neurodegenerative disease associated with impaired motor control (Konczak et al., 2009) and a range of cognitive and visual deficits. Motor symptoms such as bradykinesia (slow movement) and akinesia (impaired movement) are evident in limb and eye movements in PD during real-world activity. For example, bradykinesia can affect reaching (Schettino et al., 2006), pointing (Adamovich et al., 2001, Bekkering et al., 2001, Boisseau et al., 2002, Klockgether and Dichgans, 1994) and force control (Vaillancourt et al., 2001b, Vaillancourt et al., 2001a). In addition, impaired visuo-perceptual and basic visual functions such as reduced contrast sensitivity are reported by up to 81% (Verbaan et al., 2007) and 78% (Davidsdottir et al., 2005) of PD subjects respectively. These symptoms are seen at an early stage in PD and are associated with functional decline, freezing of gait (FOG) and falls. Investigation into VS during real-world activity in PD is warranted, to further clarify the links between these motor, cognitive and visual impairments. Eye-tracking technology has been used to further understand the visual strategies of PD subjects since the 1960's (Terao et al., 2011, van Stockum et al., 2012), demonstrating VS impairments, such as hypometric voluntary (van Stockum et al., 2012, Anderson and MacAskill, 2013) and variable reflexive (Chambers and Prescott, 2010) saccades. However until recently most research using eye-trackers involved small sample sizes (Anderson and MacAskill, 2013). Similarly most PD studies of VS are limited to static examination of eye movements alone or involve simple single-segment motor tasks (e.g. mouse clicks). Of the PD studies investigating VS during real-world activity, a wide range of protocols has been used indicating a lack of standardisation, which limits VS interpretation. Investigators who want to conduct similar research are left with the choice between numerous protocols, which differ in many respects. In the process of developing robust protocols it is often helpful to have evidence-based recommendations. We therefore examined previous work that assessed VS during real-world activities in PD and healthy control (HC) participants, in order to provide some guidance regarding the selection of appropriate methodology.
We focused the review on the following: (1) VS instrumentation used during real-world activities involving both PD and HC; (2) commonly reported VS outcomes; (3) PD specific influences on these visual outcomes; and, (4) recommendations concerning protocol. For the purpose of this review a real-world activity was considered to be a goal-orientated motor task, which involved more than one body segment (such as walking, reaching, turning etc.).
Section snippets
Search strategy
The key terms were “Parkinson's disease”, “visual sampling” and a “motor task”. A list of synonyms was created for each key term (Fig. 1). Key terms were matched and exploded with medical subject headings (MeSH) in each separate database where appropriate. Databases searched included Medline (from 1950), Embase (from 1974), PsychInfo (from 1806), Scopus, Web of Knowledge (from 1900), PubMed (from 1950) and the Cochrane library (from 1800) to February 2013. Studies were relevant if they
The evidence base
The search strategy yielded 2814 articles, excluding duplicates (Fig. 2 – adapted from Moher et al., 2009). An initial screening resulted in 287 articles of interest of which 14 were identified for inclusion by the first reviewer (SS) and 20 by the second reviewer (LA), with 6 disagreements. A consensus was made for inclusion of 15 articles for review after consultation with the third reviewer (SL).
Reasons for exclusion were: performance of a simple motor task (n = 3) (Shimizu et al., 1981,
Discussion
This review examined 15 studies reporting VS in PD subjects during real-world activities. Explicitly reviewing; (i) how VS was measured; (ii) the specific outcomes assessed and how they were defined; and (iii) the differences reported between PD and HC subjects in these outcomes during real-world activities. This review has demonstrated that the measurement of VS during real-world activities in PD is emerging, but further work is warranted to establish the validity and reliability of VS
Conclusions
The functional implications of VS during real-world activities remain unclear, but research in this area is emerging. Precise quantitative measures of VS during real-world activities are essential for characterising the VS impairments involved in PD. However, no single measure or combination of outcomes has been established as the most informative indicator of these processes. Although mobile infra-red eye–trackers are the most comprehensive method available to date, the validity and
Acknowledgements
The authors thank Erika Gavillet, Medical Librarian at Newcastle University, for her contribution to the articles search strategy. The research was supported/funded by the National Institute for Health Research (NIHR) Newcastle Biomedical Research Unit based at Newcastle upon Tyne Hospitals NHS Foundation Trust and Newcastle University. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health.
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