Direct mapping rather than motor prediction subserves modulation of corticospinal excitability during observation of actions in real time

Abstract

Gueugneau N, Mc Cabe SI, Villalta JI, Grafton ST, DellaMaggiore V. Direct mapping rather than motor prediction subserves modulation of corticospinal excitability during observation of actions in real time. J Neurophysiol 113: 3700 -3707, 2015. First published March 25, 2015 doi:10.1152/jn.00416.2014.-Motor facilitation refers to the specific increment in corticospinal excitability (CSE) elicited by the observation of actions performed by others. To date, the precise nature of the mechanism at the basis of this phenomenon is unknown. One possibility is that motor facilitation is driven by a predictive process reminiscent of the role of forward models in motor control. Alternatively, motor facilitation may result from a model-free mechanism by which the basic elements of the observed action are directly mapped onto their cortical representations. Our study was designed to discern these alternatives. To this aim, we recorded the time course of CSE for the first dorsal interosseous (FDI) and the abductor digiti minimi (ADM) during observation of three grasping actions in real time, two of which strongly diverged in kinematics from their natural (invariant) form. Although artificially slow movements used in most action observation studies might enhance the observer's discrimination performance, the use of videos in real time is crucial to maintain the time course of CSE within the physiological range of daily actions. CSE was measured at 4 time points within a 240-ms window that best captured the kinematic divergence from the invariant form. Our results show that CSE of the FDI, not the ADM, closely follows the functional role of the muscle despite the mismatch between the natural and the divergent kinematics. We propose that motor facilitation during observation of actions performed in real time reflects the model-free coding of perceived movement following a direct mapping mechanism.

Observing Without Acting: A Balance of Excitation and Suppression in the Human Corticospinal Pathway?

“…In particular there was no evidence of a muscle-specific modulation of MEPs during the precision grip observation compared to the intra-task baseline. Whilst numerous other studies have established muscle-specific effects during action observation (e.g., Alaerts et al, 2009 ; Gueugneau et al, 2015 ; Bunday et al, 2016 ; Hilt et al, 2017 ; see also Naish et al, 2014 for a review), we note that sometimes these results stem from muscle by movement interactions (i.e., comparisons across movement conditions) that do not consider whether there has actually been a change relative to some other time point or baseline (Alaerts et al, 2009 ; Bunday et al, 2016 ).…”

“…Both non-invasive and invasive studies have since pointed to the existence of similar, mirror-like activity in the human motor system, including in the primary motor cortex (M1) (Fadiga et al, 1995 ; Hari et al, 1998 ) and supplementary motor area (Mukamel et al, 2010 ). Transcranial magnetic stimulation (TMS) studies have shown that the corticospinal pathway is facilitated during action observation (Fadiga et al, 1995 ; Gangitano et al, 2001 ; Maeda et al, 2002 ; Labruna et al, 2011 ; Gueugneau et al, 2015 ), which seems consistent with the increased activity in primate premotor areas (di Pellegrino et al, 1992 ; Gallese et al, 1996 ; Kraskov et al, 2009 ), with direct cortico-cortical connections to M1, and in M1 itself (Vigneswaran et al, 2013 ; Kraskov et al, 2014 ). However, since some of those neurons in M1 included pyramidal tract neurons, the majority of which project directly to the spinal cord (Lemon, 2008 ), it remains unclear how the increased activity in the motor system during observation is prevented from producing overt movement.…”

Time-dependent modulation of spinal excitability during action observation in the macaque monkey

“…This facilitation was most prominent during Hand Shaping before the grasp, and just after the grasp itself. Previous findings in humans suggest that corticospinal excitability modulations peak at the time of observed maximal hand aperture (Gangitano et al 2001), while dynamic stages of the action are ongoing (Urgesi et al 2006(Urgesi et al , 2010, or at the time when grasp is achieved (Gueugneau et al 2015), and the peak of the observation response in macaque mirror neurons often occurs prior to, or around, the grasp (Vigneswaran et al 2013).…”

Development of a Non-invasive Brain Computer Interface for Neurorehabilitation

“…Moreover, recent studies have shown that MI increases M1 excitability, resulting in motor learning by mental practice [84], [86], [87]. In other words, motor learning can be achieved by MI practice, leading to the development of neuroplasticity in the human primary cortex (M1).…”