Exp Brain Res (2003) 153:260–265 DOI 10.1007/s00221-003-1600-8

RESEARCH ARTICLE

Maurizio Gentilucci

Object motor representation and language

Published online: 20 August 2003
Springer-Verlag 2003

Abstract Results of kinematic studies on the control of the reaching–grasping motor act (Gentilucci 2003, Exp Brain Res 149:395–400) suggest that grasp is guided by a single motor representation, which codes all the possible types of interactions with the objects. Neuroimaging studies in humans (Chao and Martin 2000, Neuroimage 12:478–484; Grabowski et al. 1998, Neuroimage 7:232– 243; Grafton et al. 1997, Neuroimage 6:231–236; Martin et al. 1995, Science 270:102–105) suggest that these representations are coded in the premotor cortex and are automatically activated when naming the object or viewing it without the execution of an overt action. If an object motor representation is accessed by language, naming of object properties related to sensory-motor transformation can automatically influence the object motor representation. This hypothesis was verified by behavioural experiments (Gentilucci and Gangitano 1998, Eur J Neurosci 10:752–756; Gentilucci et al. 2000, Exp Brain Res 133:468–490; Glover and Dixon 2002, Exp Brain Res 146:383–387), which showed that automatic reading (and probably silent naming; MacLeod 1991, Psychol Bull 109:163–203) of adjectives related to object properties analysed for planning the reaching–grasping motor act influenced the control of the arm movement. In a new study it was determined whether the class of a word can be a factor selectively influencing motor control. Participants were required to reach for and grasp an object located either on the right or on the left, and to place it on the opposite side. Either a verb (“place” SPOSTA versus “lift” ALZA) or an adjective (“lateral” LATERALE versus “high” ALTO) was printed on the target. A greater influence of the verbs than of the adjectives was observed on the kinematics of the action. In particular, when the verb ALZA was printed on the object, hand-path height M. Gentilucci ()) Dipartimento di Neuroscienze, Sezione di Fisiologia Umana, Via Volturno 39, 43100 Parma, Italy e-mail: [email protected] Tel.: +39-0521-903899 Fax: +39-0521-903900

and vertical component of arm velocity were higher than when the adjective ALTO was presented on the object. The data support the hypothesis that the object motor representation is mainly coded in terms of possible interactions with the object. Keywords Language · Reaching–grasping kinematics · Placing kinematics · Humans · Automatic word reading

Introduction In order to grasp an object, a particular type of grip has to be selected. Moreover, when reaching to grasp the target, the fingers are first shaped (grip-aperture phase) and then closed on the object (grip-closure phase). Kinematics studies (Gentilucci et al. 1991; Goodale et al. 1994; Jakobson and Goodale 1991; Jeannerod 1988) found that intrinsic object properties (i.e. size and shape) influence both the selection of the type of grip and the grasp kinematic implementation. These properties are referred to as object affordances, i.e. object features eliciting particular types of interaction with the object (motor representations). Object features can be related to a single object affordance, and, consequently, to a specific type of grip and grasp motor pattern (i.e. a specific motor representation). Conversely, object features can be associated with different affordances, and hence to different types of grip and grasp motor patterns. For example, the shape and size of a fruit are usually related to the affordances that elicit grasping its body or its stalk. Thus, it is possible that grasp is guided by multiple and independent representations of the target object, each of which codes a different grasp motor act according to the physical properties of that item. Conversely, it could be the case that grasp is guided by a single motor representation that codes all the possible affordances enabled by the target-object. If the hypothesis of multiple object motor representations is correct, grasping a fruit stalk should be affected only by the affordances related to the fingers’ opposition space (Arbib 1990). In contrast, if the

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hypothesis of a single motor representation is correct, grasping a fruit stalk should be affected also by the affordances related to the other fruit parts, and, in particular, by those commonly used to grasp it. The results of a previous study (Gentilucci 2002) supported the second hypothesis. In this study, grasping stalks of equal size and shape on each of two fruits (an apple and a strawberry) was influenced by the fruit body. Data showed that size, shape and familiarity of the object influenced the grasp kinematics and that the closeness of the fruit body to the stalk (Gangitano et al. 1998) was not responsible for the interference effect (Gentilucci 2003). Overall, current experimental data support the hypothesis that a single object motor representation, which codes all the object affordances, is involved in the kinematic implementation of reaching–grasping acts. Naming of tools (Grabowski et al. 1998; Grafton et al. 1997; Martin et al. 1995) as well as viewing pictures of tools (Chao and Martin 2000) has been shown to activate the human premotor cortex. These findings suggest that the motor representations of an object (i.e. the actions associated to the object) are coded in premotor areas and can be automatically activated by simply naming or viewing the object, without executing an object-related action. Naming of object properties related to sensorymotor transformation can activate automatically the object motor representation, and modify the control of the action directed to that object. Indeed, the results of previous kinematic studies (Gentilucci et al. 2000; Gentilucci and Gangitano 1998; Glover and Dixon 2002) showed that automatic reading of adjectives related to object properties computed for movement planning influenced the control of movement execution. In particular, the words “large” (GRANDE) and “small” (PICCOLO) printed on the object target of a reaching– grasping movement influenced the initial grasp kinematics congruently with the word meaning. Conversely, the words “far” (LONTANO) and “near” (VICINO) influenced the initial reach kinematics. The previous studies (Gentilucci et al. 2000; Glover and Dixon 2002), however, left unsolved the following problem. The presented words could be either congruent or incongruent with the object property. For example, the words GRANDE and PICCOLO were presented on both a small and a large object. Can an adjective unrelated to the object properties computed for the actual action also influence the control of a movement? This problem was addressed in the present study by presenting the word “high” (ALTO) on a target object located at the same height of the hand starting position. Neuroimaging studies showed stronger activation of the human premotor cortex when silently naming a tool’s use than when naming the same tool (for example, “to shave” versus “razor”; Grafton et al. 1997). This result is in agreement with the hypothesis that motor representations are coded especially in terms of interactions with the object. The second aim of the present study was to test this hypothesis behaviourally. To do this, the effect of automatic reading of verbs on the control of an action was

compared with that of reading of adjectives. In particular, the influence on movement control of a verb (“lift”, ALZA) and an adjective (“high”, ALTO), words both unrelated to the actual action, were compared with one another.

Methods Sixteen right-handed (according to Edinburgh Inventory; Oldfield 1971) subjects (12 females, 4 males, age 21–25 years.) participated in the present study to which they gave informed consent. All were nave as to the purpose of the experiment. Participants sat in front of a black table in a dark and soundproof room. They placed their right thumb and index finger, held in the pinch position, on a flat disk located on the table plane (starting position, SP; Fig. 1), 20 cm distant from their chest. SP was aligned with the participants’ sagittal axis. The target object was a white parallelepiped with square base (dimensions 55 cm, height 1 cm) on the visible face of which either a word or a nonword was printed in black. The target object was placed either to the right or to the left with respect to the participant’s sagittal axis (Fig. 1). The target object was 20 cm distant from and 30 inclined with respect to SP. A white paper square (dimensions 55 cm) was placed at a symmetrical location (20 cm distant from the targetobject) on the opposite side with respect to the participant’s sagittal axis (placing location). Participants were required to reach out and grasp the target object with their thumb and index finger, and to place it on the placing location (Fig. 1). The object was grasped by the sides parallel to the participants’ frontal plane. Participants were required to execute the entire action (reaching–grasping and placing) with the maximal velocity compatible with the precision required by the acts of grasping the target and placing it on the placing location. They were provided with no instruction about the words printed on the visible face of the target. In the following two experiments they were required to execute the action of reaching–grasping and placing: Experiment 1. Presentation of verbs and non-word: on the visible face of the target object the verbs SPOSTA (“place”) or ALZA (“lift”) or the non-legal non-word XTRSK were printed. The verbs were presented in imperative form. Experiment 2. Presentation of adjectives and non-word: on the visible face of the target object the adjectives LATERALE (“lateral”) or ALTO (“high”) or the non-legal non-word XTRSK were printed.

Fig. 1 Schematic representation of the experimental apparatus. SP starting position

262 In summary, in both experiments a word congruent with and a word unrelated to the action (or the object property) were presented to the participant. Each letter was 5.0 mm wide and 6.0 mm high. Different samples of eight subjects participated in each experiment. Each of the two words and the non-word were randomly presented 12 times, 6 times on the left and 6 times on the right, for a total of 36 trials. Left and right locations were randomized across the experimental session. Movements of the participant’s hand were recorded using the 3D-optoelectronic ELITE system (B.T.S., Milan, Italy). It consists of two cameras detecting infrared reflecting markers at a sampling rate of 50 Hz. Movement reconstruction in 3-D coordinates and computation of the kinematic parameters are described in a previous work (Gentilucci et al. 1992). In the present study three markers were placed on the hand. The first marker was placed on the styloid process of the wrist radium; the second and the third markers were placed on the base of the nail of the thumb and the index finger, respectively. A fourth marker was placed on the plane of the table along the participant’s sagittal axis, 15 cm from the chest, in order to provide a reference point. The marker placed on the participant’s wrist was used to analyse the reach and the placing components. The following kinematic parameters were analysed: peak of the module of the tangential velocity (peak velocity), peak of the component of velocity along the vertical axis (vertical peak velocity), and maximal height of the wrist path (maximal height). The grasp component was studied by analysing the time-course of the distance between the thumb and the index finger. The measured grasp kinematic parameters were peak velocity of finger aperture, and maximal finger aperture. Selection of the parameters was consequent upon the fact that if an influence of the word SPOSTA or LATERALE on arm movement could be observed, according to previous results showing a word effect on reaching–grasping kinematics (Gentilucci et al. 2000), peak velocity could increase, whereas an influence of the word ALZA or ALTO on arm movement could be observed by an increase in vertical peak velocity and/or maximal height. In addition, the words congruent with the action (SPOSTA) or with the target location (LATERALE) could influence also the grasp kinematics inducing an increase in finger aperture velocity and maximal finger aperture. The procedure used to calculate beginning and end of reaching–grasping is described in a previous work (Gentilucci et al. 1994). The experimental design included the following two withinsubjects factors: string-of-letters SPOSTA (experiment 1) or

Fig. 2 Effects of verbs (SPOSTA “place”, ALZA “lift”) and non-word (XTRSK) on kinematics parameters of the action formed by reaching– grasping and placing. Each symbol represents the value averaged across the participants in experiment 1, with bars indicating SEs. * Significant in the statistical analysis (P