Overground Walking Decreases Alpha Activity and Entrains Eye Movements in Humans

Abstract

Experiments in animal models have shown that running increases neuronal activity in early visual areas in light as well as in darkness. This suggests that visual processing is influenced by locomotion independent of visual input. Combining mobile electroencephalography, motion- and eye-tracking, we investigated the influence of overground free walking on cortical alpha activity (~10 Hz) and eye movements in healthy humans. Alpha activity has been considered a valuable marker of inhibition of sensory processing and shown to negatively correlate with neuronal firing rates. We found that walking led to a decrease in alpha activity over occipital cortex compared to standing. This decrease was present during walking in darkness as well as during light. Importantly, eye movements could not explain the change in alpha activity. Nevertheless, we found that walking and eye related movements were linked. While the blink rate increased with increasing walking speed independent of light or darkness, saccade rate was only significantly linked to walking speed in the light. Pupil size, on the other hand, was larger during darkness than during light, but only showed a modulation by walking in darkness. Analyzing the effect of walking with respect to the stride cycle, we further found that blinks and saccades preferentially occurred during the double support phase of walking. Alpha power, as shown previously, was lower during the swing phase than during the double support phase. We however could exclude the possibility that the alpha modulation was introduced by a walking movement induced change in electrode impedance. Overall, our work indicates that the human visual system is influenced by the current locomotion state of the body. This influence affects eye movement pattern as well as neuronal activity in sensory areas and might form part of an implicit strategy to optimally extract sensory information during locomotion.

Visual Demands of Walking Are Reflected in Eye-Blink-Evoked EEG-Activity

“…Finally, walking on complex ground is often accompanied by decreased head movements [24], presumably to stabilize gaze behavior. In spite of this, many studies on information processing during walking are restricted to walking on a flat indoor surface or a treadmill with constant velocity [23,[25][26][27]. Some real-world EEG studies have indirectly verified the involvement of cognitive processes during walking [12,13,26,28,29] or while riding a bicycle [30,31].…”

“…In spite of this, many studies on information processing during walking are restricted to walking on a flat indoor surface or a treadmill with constant velocity [23,[25][26][27]. Some real-world EEG studies have indirectly verified the involvement of cognitive processes during walking [12,13,26,28,29] or while riding a bicycle [30,31]. Typically, these experiments are designed to require mobile and unrestricted participants to perform a cognitive task that is unrelated to their locomotion.…”

Saccade and Fixation Eye Movements During Walking in People With Mild Traumatic Brain Injury

“…We limited gait metric comparisons between groups to gait velocity because of the variable's ability to differentiate between groups from previous studies (Fino, 2016;Howell et al, 2018). However, other components of gait, specifically percent of time spent in double support, have also been shown to be different in those with chronic symptoms of mTBI (Cao et al, 2020). This variable is of particular interest because saccade frequency increases during the double support phase of gait.…”

Perceptual Awareness of Optic Flows Paced Optimally and Non-optimally to Walking Speed

“…Moreover, recent studies in mice have demonstrated complex locomotion-driven modulations in the primary visual cortex (V1), with an overall effect of strongly increased firing rates (Clancy et al., 2019; Fu et al., 2014; Niell & Stryker, 2010; Savier et al., 2019) independent of the influence of arousal (Vinck et al., 2015; for comparable findings in humans i.e., a decrease in alpha activity suggesting disinhibition in the occipital cortex with locomotion see Cao et al., 2020; Cao & Händel, 2019). Interestingly, a sizable fraction of V1 neurons have been shown to be tuned specifically for locomotor speed, even if the animals are running in complete darkness (i.e., in the absence of visual flow; Dipoppa et al., 2018; Erisken et al., 2014; Saleem et al., 2013).…”