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

et al. (2012) Corticospinal Facilitation during Observation of Graspable Objects: A Transcranial Magnetic Stimulation Study. PLoS ONE 7(11): e49025. doi:10.1371/journal.pone.0049025 Corticospinal Facilitation during Observation of Graspable Objects: A Transcranial Magnetic Stimulation Study Michele Franca 0 Luca Turella 0 Rosario Canto 0 Nicola Brunelli 0 Luisa Allione 0 Nico 0 Golfre Andreasi 0 Marianna Desantis 0 Daniele Marzoli 0 Luciano Fadiga 0 Alessio Avenanti, University of Bologna, Italy 0 1 Department of Biomedical Sciences and Advanced Therapies, Section of Human Physiology, University of Ferrara , Ferrara , Italy , 2 Istituto Italiano di Tecnologia, Robotics, Brain and Cognitive Sciences Department , Genova , Italy 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. - . These authors contributed equally to this work. In his ecological approach to vision [1], Gibson argued that, when we look at objects, we directly perceive not only their physical properties, but also the constellation of potential actions we can perform on and with them. He called this set of potential actions affordances and stated that they are generated without the need or the intention to act on the observed object; at the same time, they are highly constrained by the observers motor repertoire. This theory suggests that a sensory-motor system, able to transform the physical properties of an object into motor commands at first sight and with minimum effort, is a pre-requisite for successfully interacting within a competitive environment. A very strong support to the affordance idea comes from neurophysiological studies in macaque monkeys, showing a corticocortical network devoted to transform object visual information into grasping actions which includes the anterior intraparietal region (AIP) and the ventral premotor cortex (in particular area F5). Premotor cortex, in turn, sends projections both to the primary motor cortex and to the cervical enlargement [26]. Rizzolatti and colleagues (1988), firstly reported a relevant population of neurons within premotor area F5, whose activity was strongly related to specific goal-directed actions such as grasping or manipulating specific objects [7]. The authors argued that motor neurons with different discharge properties code different goal-directed actions and all together they constitute a motor vocabulary always accessed by visual information. Among these motor neurons, about 20% showed object-related visual properties. More recently, area F5 visual properties were formally tested and it was described a set of bimodal visuomotor neurons with similar discharge pattern when a monkey grasps an object and when it simply watches a similar object without making any movement [8]. The visuomotor neurons belonging to this class have been successively named canonical neurons [9] to distinguish them from the other class of visuomotor neurons in area F5, the mirror neurons, responding instead to action observation [1011]. Further studies confirmed the existence of canonical neurons within both ventral and dorsal premotor cortex [1213], and within intraparietal region AIP and posterior parietal cortex [1415]. Consistent with monkey evidence, behavioral studies in humans have demonstrated that the mere observation of a graspable object potentiates the observers motor programs necessary to interact with it, even in absence of an explicit intention to act. This effect has been referred to as visuomotor priming or affordance effect [1617]. In a series of experiment it was demonstrated that, when subjects were viewing an object with a handle oriented to the left or to the right, they reacted faster when the response hand was congruent with a given handle orientation, even if it was irrelevant for executing the task. The same authors further showed that Reaction Times (RTs) to visually presented large or small objects were significantly affected by the type of response executed by the participants (precision vs whole hand prehension), being faster in presence of congruence between response type and object affordance [1820]. These results seem to confirm that, in the observer, the sight of the object recruits populations of neurons coding the motor program necessary to grasp it. The activity of such population may interact positively or negatively with the one coding the motor program of the selected hand response, both executed with the same muscular effectors. Similar results have been successively confirmed and extended in the framework of the more general premotor theory of attention [17,21]. Other authors described the time-course of the affordance effect adopting similar visual stimuli in the context of a Stimulus Onset Asynchrony (SOA) paradigm [22]. The reported effect was minimum for SOA = 0 and increased progressively with SOA, reaching its maximum for SOA = 800 and 1200. They thus concluded that the affordance effect develops gradually and persists for a relatively long period of time. These results were in agreement with a distributional analysis of reaction times performed in a prior study [19], allowing a further distinction from other Stimulus-Response Compatibility effects. Human neuroimaging studies have consistently shown that, during the mere observation of graspable objects, a parieto-frontal circuit involved in visually guided grasping becomes significantly active. A Positron Emission Tomoraphy (PET) experiment with right-handed subjects, reported bilateral activation of premotor cortex during the observation of familiar tools [23]. A functional Magnetic Resonance Imging (fMRI) stud (...truncated)