Corticospinal Facilitation during Observation of Graspable Objects: A Transcranial Magnetic Stimulation Study

Abstract

In 1979, Gibson first advanced the idea that the sight of graspable objects automatically activates in the observer the repertoire of actions necessary to interact with them, even in the absence of any intention to act (“affordance effect”). The neurophysiological substrate of this effect was later identified in a class of bimodal neurons, the so-called "canonical" neurons, located within monkey premotor cortex. In humans, even if different behavioral studies supported the existence of affordance effect, neurophysiological investigations exploring its neural substrates showed contradictory results. Here, by means of Transcranial Magnetic Stimulation (TMS), we explored the time-course of the “affordance effect” elicited by the observation of everyday-life graspable objects on motor cortex of resting observers. We recorded motor evoked potentials (MEP) from three intrinsic hand muscles (two "synergic" for grasping, OP and FDI and one "neutral", ADM). We found that objects’ vision determined an increased excitability at 120 milliseconds after their presentation. Moreover, this modulation was proved to be specific to the cortical representations of synergic muscles. From an evolutionary perspective, this timing perfectly fits with a fast recruitment of the motor system aimed at rapidly and accurately choosing the appropriate motor plans in a competitive environment filled with different opportunities.

A central component of the N1 event-related brain potential could index the early and automatic inhibition of the actions systematically activated by objects

“…Indeed, these systematic activations occur extremely early. For instance, when participants are observing graspable objects, the increase in muscle excitability starts as early as 120 ms after the onset of the presentation (Franca et al, 2012). Similar delays were obtained in a study where participants learned to associate the contraction of the tibialis anterior muscle of each ankle in responses to an auditory cue (Schneider et al, 2004) or when measuring facial action (i.e., spontaneous mimicry) in response to the presentation of happy and neutral faces (Korb, Grangean and Sherer, 2010).…”

Corticospinal Excitability in the Hand Muscles is Decreased During Eye Movement with Visual Occlusion

“…Accordingly, the inconsistent finding between the two studies is explained by a view that visual feedback eliminates the decrease in corticospinal excitability during eye movement in the hand muscles at rest. Indeed, simply observing an object increased corticospinal excitability in the hand muscles at rest (Franca, et al, 2012). In this study, automatic facilitation of the MEP in the opponens pollicis and the FDI muscles was observed within a small time interval after visual presentation of graspable objects.…”

“…Not only motor commands to the eye muscles but also visual feedback occurs during eye movements. It has been reported that visual processing modulates corticospinal excitability; e.g., observing an object increased corticospinal excitability in the FDI and opponent pollicis muscles at rest (Franca, Turella, Canto, Brunelli, Allione, Andreasi, et al, 2012). Thus, the decrease in corticospinal excitability across the hand muscles during smooth pursuit eye movement observed in the previous study by Maioli, et al may be related to visual feedback rather than motor commands to the eye muscles.…”

Priming of grasping muscles when viewing a safety handle is diminished with age

“…Simply observing graspable objects within reaching distance can activate motor cortical networks suitable for grasping these objects, suggesting that we put our world into motor terms automatically [1][2][3][4][5][6]. This effect is evident as faster reaction times when hand responses are subliminally primed [7], but also using measures such as functional Magnetic Resonance Imaging [1] and Transcranial Magnetic Stimulation [6] to detect underlying changes in brain activity when viewing graspable objects. A direct link between visual perception and action offers a way to overcome transmission delays within a distributed nervous system.…”

“…To address our specific aim, factors established in previous motor affordance research were used to inform a focused design. For example, past studies have shown that objects affording a particular type of grasp produce rapid excitability changes in muscles involved in grasping these viewed objects when they are within graspable range of the individual [2][3][4][5][6] but, this effect was absent when objects were out of reach, and for non-graspable 'control' objects [3]. Based upon this foundation we streamlined our approach to measure CSE in hand muscles during two distinct visual conditions: (i) viewing a wall-mounted safety handle or (ii) viewing no handle (i.e.…”