Neural rhythmic symphony of human walking observation: Upside-down and Uncoordinated condition on cortical theta, alpha, beta and gamma oscillations

Abstract

Biological motion observation has been recognized to produce dynamic change in sensorimotor activation according to the observed kinematics. Physical plausibility of the spatial-kinematic relationship of human movement may play a major role in the top-down processing of human motion recognition. Here, we investigated the time course of scalp activation during observation of human gait in order to extract and use it on future integrated brain-computer interface using virtual reality (VR). We analyzed event related potentials (ERP), the event related spectral perturbation (ERSP) and the inter-trial coherence (ITC) from high-density EEG recording during video display onset (−200–600 ms) and the steady state visual evoked potentials (SSVEP) inside the video of human walking 3D-animation in three conditions: Normal; Upside-down (inverted images); and Uncoordinated (pseudo-randomly mixed images). We found that early visual evoked response P120 was decreased in Upside-down condition. The N170 and P300b amplitudes were decreased in Uncoordinated condition. In Upside-down and Uncoordinated conditions, we found decreased alpha power and theta phase-locking. As regards gamma oscillation, power was increased during the Upside-down animation and decreased during the Uncoordinated animation. An SSVEP-like response oscillating at about 10 Hz was also described showing that the oscillating pattern is enhanced 300 ms after the heel strike event only in the Normal but not in the Upside-down condition. Our results are consistent with most of previous point-light display studies, further supporting possible use of virtual reality for neurofeedback applications.

Oscillations in the human brain during walking execution, imagination and observation

“…This has resulted in much convergence in results but also some divergent evidence within this literature. Neurophysiological, neuroimaging and behavioral data have demonstrated a high sensitivity to kinematics of human movement [120,121] including walking [122,123] as in a selfimage mirror walking or virtual environment [63], reference frame [122,[124][125][126]. It is well known that shape and motion information are treated separately by ventral and dorsal visual streams, and converge to the posterior portion of superior temporal sulcus [111,127,128].…”

On the neural basis of sensory weighting: Alpha, beta and gamma modulations during complex movements

“…Contributing to a higher level of sensory information processing, gamma oscillations are considered as neural markers of unimodal and multimodal sensory binding (Engel et al, 2012;Ghazanfar et al, 2008;Krebber et al, 2015;Maier et al, 2008;Wang, 2010). For instance, gamma response in the occipital cortex is observed following the presentation of two coherent visual stimuli (Tallon-Baudry et al, 1996;Zarka et al, 2014). This response is absent when a visual stimulus is presented simultaneously with incongruent visual (TallonBaudry et al, 1996;Zarka et al, 2014) or non-visual stimuli Krebber et al, 2015;Maier et al, 2008).…”

“…For instance, gamma response in the occipital cortex is observed following the presentation of two coherent visual stimuli (Tallon-Baudry et al, 1996;Zarka et al, 2014). This response is absent when a visual stimulus is presented simultaneously with incongruent visual (TallonBaudry et al, 1996;Zarka et al, 2014) or non-visual stimuli Krebber et al, 2015;Maier et al, 2008). In the case of incongruent visuo-tactile stimulation, this decrease of gamma power is not only observed over the visual cortex but is also found centrally, over the somatosensory cortex (Krebber et al, 2015).…”

Sensorimotor and cognitive involvement of the beta–gamma oscillation in the frontal N30 component of somatosensory evoked potentials

“…The oscillatory approach is particularly attractive because it provides a wider scope to the study of brain function through the interaction between ERP and ongoing cortical activity (Klimesch, 1999(Klimesch, , 2012Fries, 2005;Zarka et al, 2014;Gruber et al, 2014). While the earlier thalamic P14 and the parietal N20 remain stable, the N30 amplitude is highly sensitive to concurrent input from the periphery, such as superficial and deep muscle massage (Cheron and Borenstein, 1991) or centrally generated as motor execution, motor preparation and movement imagery (Rushton et al, 1981;Cheron andBorenstein, 1987, 1992;Rossini et al, 1999).…”

“…In humans, as in monkeys, these neurons are distributed in a complex mirror neuron network (MNN) (Fabbri-Destro and Rizzolatti, 2008;Fadiga et al, 2005;Grèzes et al, 2001;Iacoboni et al, 2005). Numerous studies have been made of the visual processes involved in the recognition of other peoples' movements (Blake and Shiffrar, 2007;Avanzini et al, 2013;Di Dio et al, 2013;McAleer et al, 2014;Zarka et al, 2014), prediction (Csibra and Gergely, 2007;Kilner et al, 2007), and the implications for social cognition (Jacob and Jeannerod, 2005;Schütz-Bosbach and Prinz, 2007;Heyes, 2010;Press et al, 2011). However, the contribution of the MNN to somatosensory information has not been thoroughly investigated.…”