Changes in event-related potentials during dual task walking in aging and Parkinson's disease
Introduction
It has been theorized that walking in everyday life conditions requires higher cognitive processes that utilizes a complex neural network that incorporates cognitive and motor information (Woollacott and Shumway-Cook, 2002, Yogev-Seligmann et al., 2008). Most evidence supporting this notion relies on behavioral studies stemming from dual-task paradigms during walking to increase cognitive demands. These studies show that adding a simultaneous task to walking taxes executive function and attention and leads to changes in gait performance (Hausdorff et al., 2008, Yogev-Seligmann et al., 2008). This effect is exacerbated with ageing and neurodegenerative diseases such as Parkinson's disease (PD) (Segev-Jacubovski et al., 2011, Woollacott and Shumway-Cook, 2002, Yogev-Seligmann et al., 2008) and is related to falls (Segev-Jacubovski et al., 2011) providing indirect evidence of the importance of the interconnection between motor and cognitive functions during walking. In recent years, various neuroimaging techniques were used to study the role of cognitive resources during walking. fMRI studies used motor imagery (Maidan et al., 2016b, Peterson et al., 2014) and alternating movements of feet (Nieuwhof et al., 2017, Shine et al., 2013) to mimic gait in the scanner. These studies reported increased activation in various frontal regions related to the attentional networks (Maidan et al., 2016b, Peterson et al., 2014, Shine et al., 2013), however these findings are limited as they do not directly capture actual gait.
Recent studies using functional Near Infrared Spectroscopy (fNIRS), a neuroimaging technique measuring blood oxygenation levels from the brain convexity during actual walking, showed increased activation of the prefrontal cortex (PFC) in healthy young and older adults during dual task walking, as compared to usual walking (Holtzer et al., 2015, Metzger et al., 2017, Mirelman et al., 2017). Patients with PD presented similar findings but also showed increased activation already during usual walking (Maidan et al., 2016a) suggesting a reliance on cognitive resources already during simple tasks. However, similar to fMRI, the temporal resolution of the fNIRS is low and it measures hemodynamic responses only in specific superficial areas of interest, unable to distinguish isolated effects from network function (Ferrari and Quaresima, 2012).
Spontaneous electroencephalographic (EEG) recording as well as event-related potentials (ERPs) are direct measurements of neuronal activity, with high temporal resolution, that can be applied during walking. Variations in ERP responses including amplitude, polarity, distribution, and latency have been associated with various cognitive measures (Duncan et al., 2009, Picton et al., 2000, Woodman, 2010). Changes were mainly observed in P300, the most studied ERP related to attention and cognitive decline, elicited using the “oddball” task. Task in which a random sequence of stimuli is presented and subjects are required to mentally count the rare target events (Polich, 2004). Accumulating evidence from EEG and fMRI studies show that P300 generation stems from the connection between frontal lobe and hippocampal/temporal-parietal function (Huang et al., 2015, Kiehl et al., 2001, Knight, 1996). It has been suggested that frontal areas account for the attention mechanism that directs neural responsivity to a new stimulus (Daffner et al., 2000a, Daffner et al., 2000b), whereas the tempo-parietal regions correspond to the attentional resources used to maintain memory entries (Berti et al., 2004, Huang et al., 2015). Patients with PD have decreased P300 amplitude and increased peak latency during sitting tasks as compared to healthy older adults and as the severity of cognitive dysfunction increases (Yilmaz et al., 2017). Although these changes in P300 were highly sensitive to cognitive decline and attentional impairments (Batterink et al., 2012), they were also observed in other pathologies such as Alzheimer's disease (Benz et al., 2014) showing low specificity.
As demonstrated previously (Yogev-Seligmann et al., 2008), PD involves deficits in motor and cognitive functions that are often exacerbated during dual-task in which motor and cognitive tasks are performed simultaneously. In this study, we combined the oddball task with walking to evaluate the dual-task effect of an attentional demanding task while walking in healthy young adults, healthy older adults and patients with PD. Using this approach, we aimed to reveal specific changes in P300 while walking and dual-tasking in older adults and patients with PD. We hypothesized that P300 latency will increase and amplitude will decrease during dual-task walking because of the additional attentional load, and that these changes will be more pronounced with aging and disease.
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Participants
Thirty-one subjects, i.e., 11 healthy young adults, 10 healthy older adults, and 10 patients with PD, participated in this study. Recruitment was performed by reaching out to the geriatric and neurology outpatient clinics in Tel Aviv Medical Center. Participants were excluded if they had: MOCA ≤ 21, a history of neurological disorder other than PD that could affect their performance, inability to walk at least 5 minutes, unstable medical condition including cardio-vascular instability, hearing
Participants
Participant characteristics are presented in Table 1. Healthy older adults and patients with PD were similar in age (p = 0.227). MOCA, gait speed, and CTT scores were significantly lower in patients with PD, compared to healthy young (Table 1).
Oddball task performance and P300 evaluation
All participants were engaged in the oddball task and demonstrated high accuracy of performance during standing (healthy young 100 ± 0.0%, healthy older adults 98 ± 1.7%, and patients with PD 97.4 ± 1.1%) and during walking (healthy young 99.2 ± 0.4%,
Discussion
P300 is an index of stimulus processing which has been considered a motor free measure of cognitive function (Magliero et al., 1984, Polich, 2004). In this study, we aimed to elucidate specific changes in P300 associated with dual tasking in older adults and patients with PD using EEG. Our findings demonstrate (1) prolonged P300 latency during walking is more pronounced in aging and PD, (2) there is an association between P300 latency and reduced cognitive function as measured by CTT and motor
Conclusions
To our knowledge, this study is the first to report on alterations in neuronal activity using EEG during dual task oddball walking in patients with PD. These high temporal resolution EEG findings provide an additional layer to our knowledge regarding executive function deficits in aging and PD demonstrating new direct evidence of the physiological recruitment of attentional networks during walking and their impact by ageing and disease.
Conflict of interest
None of the authors have potential conflicts of interest to be disclosed.
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