Learning Is Better with the Hands Free: The Role of Posture in the Memory of Manipulable Objects

RESEARCH ARTICLE Learning Is Better with the Hands Free: The Role of Posture in the Memory of Manipulable Objects Léo Dutriaux1,2,3*, Valérie Gyselinck1,2,3,4 1 Laboratoire Mémoire et Cognition, Université Paris Descartes, Sorbonne Paris Cité, Paris, France, 2 Institut de Psychologie, Centre Henri Piéron, Boulogne Billancourt, France, 3 Centre de Psychiatrie et Neurosciences, INSERM U894, Paris, France, 4 IFSTTAR—LPC, Versailles, France * a11111 OPEN ACCESS Citation: Dutriaux L, Gyselinck V (2016) Learning Is Better with the Hands Free: The Role of Posture in the Memory of Manipulable Objects. PLoS ONE 11 (7): e0159108. doi:10.1371/journal.pone.0159108 Editor: Marco Iacoboni, UCLA, UNITED STATES Received: April 12, 2016 Accepted: June 27, 2016 Abstract Grounded cognition proposes that memory shares processing resources with sensorimotor systems. The aim of the present study was to show that motor simulation participates in the conceptual representation of manipulable objects in long-term memory. In two experiments, lists of manipulable and nonmanipulable objects were presented. Participants were instructed to memorize the items while adopting different postures. In the control condition, they had to keep their hands at rest in front of them. In the interference condition, participants had to keep their hands crossed behind their back to make their hands less free for action. After each list, participants had to perform first a distractive task, and then an oral free recall. The results showed that the interfering posture produced a specific decrease in the recall of manipulable objects, but not of nonmanipulable ones. This decrease was similar when the items were presented as pictures (Experiment 1) or as words (Experiment 2), thus excluding a purely visual effect. These results provide strong evidence that the motor simulation plays a role in the memory trace of the object. Published: July 14, 2016 Copyright: © 2016 Dutriaux, Gyselinck. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data of both experiments are available from the Open Science Framework database (URL: osf.io/5qbpd). Funding: The work was supported by Grant ANR13-APPR-0009 from the French National Research Agency (ANR). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Introduction According to grounded-cognition theories, semantic memory shares processing resources with perception, emotion and action [1–3]. Glenberg [4] underlined the importance of the motor system, claiming that the main function of conceptual knowledge is to support action. He proposed that memory encodes the environment in terms of affordances. The affordance of an object is defined here as the potential actions that an organism can perform on it, given the actual state of the object, the prior history of the organism’s interactions with this object, and the organism’s ability to act. Consistently, numerous studies have shown that action-related concepts involve an automatic activation of the motor cortex, analogous to when the action is actually performed (for a review, see [5]). This phenomenon, often referred to as motor simulation, has been reported during the observation of actions (e.g., [6,7]), or while processing action sentences (e.g., [8– 11]), but also while processing manipulable objects. Evidence for motor simulation of PLOS ONE | DOI:10.1371/journal.pone.0159108 July 14, 2016 1 / 11 Memory, Manipulable Objects and Posture affordance comes from neurophysiological studies on monkeys. The so-called “canonical” neurons, found in the F5 area of the macaque premotor cortex, fire both when the monkey simply views an object, and when the monkey actually grasps that object [12]. It has also been consistently shown in humans that both viewing manipulable objects (e.g., [13–16]) and reading the names of manipulable objects (e.g., [17–19]) activate motor regions more than nonmanipulable objects or animals. In the same vein, using Transcranial Magnetic Stimulation (TMS), several studies have shown that Motor Evoked Potentials are modulated by pictures of manipulable objects [20–22]. On the behavioral side, it has been demonstrated via the stimulus-response compatibility paradigm that the viewing of a manipulable object potentiates motor actions associated with the use of that object (e.g., [18,23–28]). Tucker and Ellis [27] asked their participants to indicate whether an object was a man-made or a natural object. The response could be either a power or a precision grip, and was performed while simultaneously viewing a real object which would normally be grasped using either a power or precision grip. Faster reaction times were found when the response and the object grip were congruent (i.e., faster for power response/ power grip and precision/precision trials than power/precision and precision/power trials). In the same vein, viewing tools facilitates the gesture compatible with their grasping or their use [23]. Importantly, both studies found the same kind of results with words denoting the same manipulable objects. This suggests that this effect of object affordance results, at least in part, from semantic information in memory, rather than only from perceptual information elicited by pictures. However, while the above-mentioned studies suggest that the processing of action-related concepts involves a motor activation, such activations may be incidental to the activation of their representations from long-term memory, rather than part of it. Therefore, these results are not only consistent with the view that conceptual and motor systems share processing resources, but also with a modular view of these two systems, as has been largely discussed by Mahon and Caramazza [29]. Consistent with the former view, there is some evidence suggesting that manipulability is a semantic dimension [30], and that conceptualization relies on action relevant properties [31,32]. As suggested by Mahon and Caramazza [29], another convincing way to show that memory and action share processing resources would be to see whether the suppression or the impairment of the motor system involves a deficit in memory. Several studies have addressed the effect of motor interference on the processing of manipulable objects. First, it seems that using TMS on the right inferior parietal lobule, which is known for its role in praxis, slows down the naming of manipulable objects, but not the naming of nonmanipulable objects [33]. Importantly, a few neuropsychological studies confirm these results, demonstrating that brain injured patients suffering from apraxia show a decrease in manipula (...truncated)