Recalibration of inhibitory control systems during walking-related dual-task interference: A Mobile Brain-Body Imaging (MOBI) Study

Highlights

• Dual-task performance during active walking was explored.

• High-density brain electrical activity was recorded from freely walking individuals.

• Mobile Brain-Body Imaging (MOBI) allows for neural measures in naturalistic settings.

• Cognitive control networks reconfigure to manage dual-task walking interference.

• Stride timing patterns are significantly lengthened by cognitive load.

Abstract

Walking while simultaneously performing cognitively demanding tasks such as talking or texting are typical complex behaviors in our daily routines. Little is known about neural mechanisms underlying cortical resource allocation during such mobile actions, largely due to portability limitations of conventional neuroimaging technologies. We applied an EEG-based Mobile Brain-Body Imaging (MOBI) system that integrates high-density event-related potential (ERP) recordings with simultaneously acquired foot-force sensor data to monitor gait patterns and brain activity. We compared behavioral and ERP measures associated with performing a Go/NoGo response-inhibition task under conditions where participants (N = 18) sat in a stationary way, walked deliberately or walked briskly. This allowed for assessment of effects of increasing dual-task load (i.e. walking speed) on neural indices of inhibitory control. Stride time and variability were also measured during inhibitory task performance and compared to stride parameters without task performance, thereby assessing reciprocal dual-task effects on gait parameters. There were no task performance differences between sitting and either walking condition, indicating that participants could perform both tasks simultaneously without suffering dual-task costs. However, participants took longer strides under dual-task load, likely indicating an adaptive mechanism to reduce inter-task competition for cortical resources. We found robust differences in amplitude, latency and topography of ERP components (N2 and P3) associated with inhibitory control between the sitting and walking conditions. Considering that participants showed no dual-task performance costs, we suggest that observed neural alterations under increasing task-load represent adaptive recalibration of the inhibitory network towards a more controlled and effortful processing mode, thereby optimizing performance under dual-task situations.

Introduction

Humans continuously process sensory and cognitive events while engaged in everyday activities such as walking. For example, we successfully navigate the aisles of a shopping center as we rehearse a shopping list and contemplate the necessary ingredients for that evening's dinner. Most everyday situations require this type of multitasking and brain processes have evolved to handle concurrent processing of cognitive and motor functions. However, research on multitask performance has provided clear evidence for costs, indicating that cognitive-motor interference (CMI) can compromise performance in one or both domains (Al-Yahya et al., 2011, Woollacott and Shumway-Cook, 2002). This is particularly the case for older individuals (Al-Yahya et al., 2011) where performing cognitively demanding tasks while walking greatly increases the risk of falling. As such, revealing the neural bases of CMI has important clinical implications and the development of objective brain measures of increased cognitive-motor interference could well provide biomarkers that predict increased risk of falls, allowing for early detection and intervention. In turn, these measures may serve as early risk indicators (i.e. endophenotypes) for those who will go on to develop clinically significant cognitive impairments such as Alzheimer's disease.

Behavioral dual-task studies have provided robust evidence for a mutual influence suggesting that motor and cognitive functions are supported in part by common neural processes (Woollacott and Shumway-Cook, 2002). Postural stability during walking varies depending on the complexity of the cognitive task (Woollacott and Shumway-Cook, 2002) and strong associations between age and speed reduction under dual-task conditions have been reported (Al-Yahya et al., 2011). At the same time, walking impinges on cognitive performance with studies showing impaired spatial memory capacity, and target detection time (Lajoie et al., 1993). More specifically, Lajoie and colleagues showed that detection time increased during the single-support phase (i.e. one foot in swing) of the gait cycle, suggesting that attentional demands co-vary with differences in balance requirements during the gait cycle (Lajoie et al., 1993).

While behavioral evidence suggests reliance on common brain processes, only a few studies have directly assessed cortical involvement during walking with (Doi et al., 2012, Holtzer et al., 2011, Uehara et al., 2011) and without (Gramann et al., 2011, Gwin et al., 2011, Harada et al., 2009, Kurz et al., 2012, Suzuki et al., 2008) engagement in a secondary task. Studies using functional magnetic resonance imaging (fMRI) have identified relevant cortical regions, showing activations during preparation and execution of rhythmic foot and leg movements in frontal and primary motor cortex (Heuninckx et al., 2005, Heuninckx et al., 2008, Sahyoun et al., 2004). Obviously these studies are limited by the lack of realistic mobility of the participants. Studies using functional near-infrared spectroscopy (fNIRS) assessing oxygenated hemoglobin (oxyHb) have reported increased oxyHb levels in the prefrontal and premotor cortices of participants who were preparing to walk (Suzuki et al., 2008), and that inter-individual variations in stride-time interval correlated positively with oxyHb response within the pre-central gyrus and supplementary motor area (Kurz et al., 2012). In a dual-task study by Holtzer and colleagues, oxyHb levels in prefrontal cortical (PFC) regions increased during a “walking and talking” dual-task scenario in contrast to a walking-alone condition, especially in young participants. An association between trunk stability under dual-task conditions and gray matter atrophy has been established (Doi et al., 2012), and a transcranial magnetic stimulation (TMS) study showed that the excitability of the primary motor cortex during a dual motor task varied as a function of gait speed (Uehara et al., 2011).

Neuroimaging studies have been successful in defining relevant cortical areas and related changes in activity under dual-task conditions (Holtzer et al., 2011). However, hemodynamic imaging methods lack the temporal resolution necessary to determine and dissociate the susceptibility of specific processing stages to CMI. Broader susceptibility with interference that affects multiple processing levels of the secondary task might be related to increased dual-task costs. Event-related potentials (ERP) provide temporally precise measures of information processing that are very well-suited to dissociate between sensory-perceptual, cognitive and motor processing stages. Work by our group (De Sanctis et al., 2012, Nolan et al., 2009, Nolan et al., 2011, Nolan et al., 2012) and others (Bulea et al., 2013, Duvinage et al., 2013, Gramann et al., 2010, Gramann et al., 2011, Gwin et al., 2010, Gwin et al., 2011; Gwin et al., 2011) has demonstrated the feasibility of acquiring high-density EEG to investigate evoked potentials related to perceptual and cognitive processes during active and passive self-motion. For example, participants standing or walking on a treadmill while performing a visual oddball task produced entirely typical ERP components with excellent signal-to-noise characteristics (Gramann et al., 2010).

Here, we deployed high-density scalp EEG recordings while participants performed a taxing visual Go/NoGo response inhibition task, which requires subjects to overcome a potent response tendency established by frequent Go stimuli to successfully inhibit response execution to NoGo stimuli. We also used force sensors attached to the sole of each foot to measure duration and variability of the gait cycle while participants walked on a treadmill (Fig. 1). To assess the influence of walking load on response inhibition, we compared participants′ Go/NoGo task performance under three activity conditions: 1) sitting, 2) walking deliberately (2.4 km/h) and 3) walking briskly (5.0 km/h). We predicted that walking, particularly at higher speed, would compromise inhibitory control abilities. To assess the influence of response inhibition load on gait, we compared duration and variability of the gait cycle while participants walked on the treadmill with and without performance of the Go/NoGo inhibition task.

EEG based studies identifying specific phases of inhibitory network activity have distinguished relatively early automatic processes, as represented by the N2 component (250–350 ms), from late controlled processes, as represented by the P3 component (400–550 ms) (Eimer, 1993, Falkenstein et al., 1995, Falkenstein et al., 1999). We set out to investigate walking-related effects on the N2 and P3 components, allowing us to assess the susceptibility of different inhibitory processing stages to CMI. Furthermore, effects of CMI at the sensory-perceptual processing level were assessed by considering the visual-evoked potential (VEP) to the NoGo stimulus. Based on preliminary results by our group (De Sanctis et al., 2012), which showed that CMI strongly modulated the N2 component, we predicted increased susceptibility of early and automatic processing stages of inhibitory control to motor load. Furthermore, we predicted an increase in stride-to-stride variability while participants perform the inhibitory task, indicative of dual-task costs in the form of less stable gait patterns.