SHORT COMMUNICATION Influence of automatic

Received 31 July 1997, accepted 5 September 1997 rod on whose visible face the adjective either 'long' or 'short' was printed. We expected an effect of the ...
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© European Neuroscience Association

European Journal of Neuroscience, Vol. 10, pp. 752–756, 1998

SHORT COMMUNICATION Influence of automatic word reading on motor control Maurizio Gentilucci and Massimo Gangitano Institute of Human Physiology, University of Parma, via Gramsci 14, I-43100 Parma Italy Keywords: automatic word reading, humans, kinematics, object distance, object size, reaching-grasping

Abstract We investigated the possible influence of automatic word reading on processes of visuo-motor transformation. Six subjects were required to reach and grasp a rod on whose visible face the word ‘long’ or ‘short’ was printed. Word reading was not explicitly required. In order to induce subjects to visually analyse the object trial by trial, object position and size were randomly varied during the experimental session. The kinematics of the reaching component was affected by word presentation. Peak acceleration, peak velocity, and peak deceleration of arm were higher for the word ‘long’ with respect to the word ‘short’. That is, during the initial movement phase subjects automatically associated the meaning of the word with the distance to be covered and activated a motor program for a farther and/or nearer object position. During the final movement phase, subjects modified the braking forces (deceleration) in order to correct the initial error. No effect of the words on the grasp component was observed. These results suggest a possible influence of cognitive functions on motor control and seem to contrast with the notion that the analyses executed in the ventral and dorsal cortical visual streams are different and independent.

Introduction It is known that in the ventral and dorsal cortical visual streams objects are analysed in order to elaborate two different responses: a perceptual judgement in the ventral pathway and a motor response in the dorsal one (Milner & Goodale, 1995). Two different object analyses are performed in the two visual streams (Jeannerod et al., 1994; Milner & Goodale, 1995). In the ventral stream object is analysed in a holistic way, whereas in the dorsal one specific properties are extracted from the object for planning a movement. For example, intrinsic object properties (size, shape) are analysed to control grasping movements, whereas extrinsic object properties (distance) are analysed to control reaching movements (Jeannerod, 1984; Gentilucci et al., 1991). However, the influence of visual illusions (Gentilucci et al., 1996, 1997; Daprati & Gentilucci, in press) and of mental rotations (Gentilucci & Negrotti, 1996) on object visual analysis for motor output suggests an involvement of perceptual analysis in visuo-motor transformation, occurring within the dorsal pathway. This evidence seems in contrast with the notion that the analyses performed in the two visual pathways are different and independent. In the present experiment we hypothesized an involvement in motor control of a cognitive function strictly related to perceptual analysis, that is language. It is known that word presentation can automatically activate semantic and phonological representations even when viewers are not instructed to access to these processes explicitly (Posner et al., 1988; Posner & Petersen, 1990; MacLeod, 1991). We hypothesized that these implicit representations could influence object description used for arm movements. We required subjects to reach and grasp a

rod on whose visible face the adjective either ‘long’ or ‘short’ was printed. We expected an effect of the words on calculation of distance to be covered by the arm (reaching) and/or on calculation of size of the object to be grasped.

Methods Six right-handed subjects (five females and one male; age 20– 29 years) participated in the present study to which they gave informed consent. All of them were naive as to the purpose of the experiment. In a dark room the subjects sat in front of a table, with their right hand resting on its plane. At the beginning of each trial they placed their thumb and index finger, held in pinch position, on a microswitch (starting position) located along the subjects’ midline, 25 cm distant from their frontal plane. Stimuli were white wooden rods, that is parallelepipeds with square base (1.5 3 1.5 cm) either 5 cm (small object) or 6 cm (large object) high (Fig. 1). They were fixed by means of a magnet on an easel, placed on the plane of the table with an inclination by 45°. The principal axis of the objects was approximately parallel to the subjects’ sagittal plane. On the visible side of both the small and large objects either the Italian word LUNGO (long) or CORTO (short) was centrally printed in black (Fig. 1). The size of the two words (5 3 45 mm) was the same for both the objects. The stimuli could be presented either to the right or to the left with respect to the subjects’ midline, at two symmetrical locations, 34 cm distant from the starting position. The line joining the centre

Correspondence: M. Gentilucci, Istituto di Fisiologia Umana, via Gramsci 14, I-43100 Parma. E-mail: [email protected] Received 31 July 1997, accepted 5 September 1997

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FIG. 1. Photographic presentation of the objects to be reached and grasped. In upper row 5-cm rods (small objects) and in lower row 6-cm rods (large objects) are presented, respectively. The type of grip used to grasp the object is shown.

of the stimulus and the starting position was inclined by 25° with respect to the subjects’ sagittal plane. The beginning of each trial was given by a single tone (500 Hz, warning signal) generated by a PC. After a 1.5-s interval, the light of the room switched on (rising time of the lamp 15 ms). Threehundred milliseconds later a second tone (1000 Hz) was the starting signal for the movement. The interval between object presentation and starting signal was given in order to allow subjects to read the word on the object (Rayner, 1984). The subjects were required to reach the rod and grasp it at its extremities with their right thumb and index finger (Fig. 1). Removal of the rod from the easel was easy because of the weak strength of the magnet. The subjects were required to move with the maximal velocity compatible with the accuracy required by properly reaching and grasping the object. No instruction about the words printed on the objects was given to them. In the experimental session 56 trials were run. That is, seven trials for each stimulus size (small and large), position (right and left), and printed word (LUNGO and CORTO) were presented in pseudorandom order. Reaction time (RT), that is the interval between the starting signal and the release of the microswitch, was measured. RT served to verify that the subjects did not anticipate nor delay the response. The trials whose RTs were lower than 50 ms and higher than 800 ms were repeated at the end of the session.

The kinematics of the reaching-grasping movements was recorded using the ELITE system (B.T.S., Milan, Italy). Apparatus, movement reconstruction and data elaboration procedure are described elsewhere (Gentilucci et al., 1994). Spatial resolution of the ELITE system is 0.4 mm (Gentilucci et al., 1994). Four markers were used. The first marker was placed on the styloid process of the radius at the wrist. The second and third marker were positioned on the nails of the thumb and the index finger, respectively. The fourth marker, placed on the table along the subjects’ sagittal plane, 8 cm away from its edge, was used as a reference point. The marker placed on the wrist was used to study the reaching component. The following parameters were measured: peak acceleration, peak velocity, peak deceleration and reach time. These parameters were chosen in order to analyse the various movement phases of reaching. The time course of the distance between the two markers positioned on the thumb and the index finger was analysed in order to study the grasp component. Peak velocity of finger aperture and maximal finger aperture were the measured parameters. Reach and grasp were considered to start and stop in those samples in which displacement of the marker placed on the wrist and variation in distance between the markers placed on the thumb and the index finger became, respectively, greater and smaller than 0.4 mm (for a detailed description of the method to calculate beginning and end of reaching and grasping see Gentilucci et al., 1994).

© 1998 European Neuroscience Association, European Journal of Neuroscience, 10, 752–756

754 M. Gentilucci and M. Gangitano

FIG. 2. Representative examples of velocity profiles of the arm. Single movements are presented (subject B.B.). Filled circles and empty circles refer to movements directed to objects on whose visible face the words LUNGO (long) and CORTO (short) were printed, respectively. In the upper and lower row movements directed to the small and large objects are shown, respectively. In the right and left column movements directed to the left and right object are presented, respectively.

All parameters were submitted to separate ANOVAs whose withinsubjects factors were object size (small vs. large object), object position (right vs. left object), and word (LUNGO vs. CORTO). Newman–Keuls test was used as post hoc test. At the end of the experiment the subjects responded to a questionnaire in which they were asked whether they paid attention to the word printed on the object, and, in affirmative case, which object feature they associated the word with.

finger aperture, F1,5 5 64.9, P , 0.0005, 81.5 vs. 75.4 mm, Figs 3 and 4). On the questionnaire, half the subjects responded that they never paid attention to the word printed on the object. The remaining subjects responded that they associated the word with the size of the object: LUNGO with the large, and CORTO with the small object, respectively. No kinematic difference was found between the two groups.

Results

Discussion

Figure 2 presents examples of reaching velocity profiles in the various experimental conditions. Profiles are smooth in all conditions. They show greater velocities and, in most cases, shorter deceleration phases for presentation of the word LUNGO with respect to the word CORTO. The main kinematic parameters significantly increased for the word LUNGO in the comparison with the word CORTO (peak acceleration F1,5 5 10.6, P , 0.02, 8873.2 vs. 8680.5 mm/s2; peak velocity F1,5 5 23.0, P , 0.005, 1217.7 vs. 1199.5 mm/s; peak deceleration F1,5 5 11.0, P , 0.03, 7147.3 vs. 6866.6 mm/s2, see also Fig. 3). The interaction between object size and word was significant for peak velocity (F1,5 5 9.9, P , 0.03). The same interaction showed a trend to significance for peak deceleration (F1,5 5 5.7, P , 0.06). Post-hoc tests showed that the word effect was greater for the small than for the large object (Fig. 3). An increase in deceleration corresponded to an increase in acceleration. Consequently, reach time tended to remain constant (F1,5 5 5.0, P , 0.07). No effect of the words on the grasp component was observed (Fig. 4). Indeed, peak velocity of finger aperture (F1,5 5 0.6, P , 0.5, Fig. 3) and maximal finger aperture (F1,5 5 0.03, P , 0.9, Fig. 3) were not affected by the factor word. Both parameters were significantly higher for the large than for the small object (peak velocity of finger aperture, F1,5 5 8.8, P , 0.03, 528.1 vs. 490.3 mm/s; maximal

The reaching kinematics was affected by the words printed on the objects. The main kinematic landmarks, that is peak acceleration, peak velocity and peak deceleration, were higher for presentation of the word LUNGO (long) with respect to the word CORTO (short). It is well known (for a review on the argument see Jeannerod, 1988) that when the distance of arm path is made longer, acceleration and velocity of arm increase. It is logical to deduce that at the presentation of the word LUNGO, the subjects activated a motor program for a farther position of the target with respect to the presentation of the word CORTO. The variations in the parameters of the initial movement phase, that is peak acceleration and peak velocity, could cause misreaching of the object. This did not occur because the subjects compensated for miscalculation of initial acceleration forces by modifying the successive braking (deceleration) forces. This correction was gradual without any brisk variation in velocity profiles (see Fig. 2), as found in a previous experiment (Goodale et al., 1986). The word effect was more evident for the small than for the large object. Two not mutually exclusive explanations can be offered for this result. First, it is possible that accuracy required by the prehension of small objects (Gentilucci et al., 1991) induced subjects to a more accurate visual analysis of them. Consequently, the probability of automatic reading of the words increased. Second, it is possible that

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FIG. 3. Values averaged across the subjects of kinematic parameters of reaching (peak acceleration, peak velocity, and peak deceleration) and of grasping (peak velocity of finger aperture, and maximal finger aperture). Black bars and grey bars refer to movements directed to objects on whose visible face the words LUNGO (long) and CORTO (short) were printed, respectively. Significant differences between the two conditions of word presentation are shown by asterisks.

FIG. 4. Representative examples of time courses of the grasp. Single movements are presented (subject B.B.). Other conventions as in Figure 2.

the subjects analysed more attentively the extremities of the rods because they were the final points of finger trajectories. Because the words were centrally printed on the two objects and their sizes were equal (see Fig. 1), the words were nearer to the extremities of the small than of the large object. Consequently, they were more easily readable. No word effect on the grasp component was observed. This result is in contrast with the fact that the meaning of the two words could be associated with the length of the rods and, consequently, it could influence finger shaping during grasp. We can explain this result as follows. First, grasp planning requires a more complex visual analysis of the object with respect to reach planning (Daprati & Gentilucci, in press). Thus, the time of visual analysis could be insufficient for

an association of the meaning of the word with the object. Second, during the experimental session half the subjects were aware that the meaning of the word could be associated with object size. Consequently, they could try to avoid any possible word interference on size calculation. The word effect on reaching-grasping kinematics can be interpreted as a Stroop effect (for a exhaustive review see MacLeod, 1991), in that automatic reading of words influences responses on features of visual stimuli. However, there are some fundamental differences between the two effects. First, in the Stroop task the response requires a perceptual judgement. In contrast, in the present experiment it required an automatic visuo-motor transformation. Second, in the Stroop task a single stimulus feature such as colour or position (Shor,

© 1998 European Neuroscience Association, European Journal of Neuroscience, 10, 752–756

756 M. Gentilucci and M. Gangitano 1971; Seymour, 1974) is analysed, whereas in the present experiment the whole stimulus was analysed. Third, the Stroop effect can be explained as an imbalance between the fast process of automatic word reading and a more slow naming of ink colour, that is as an interference between two verbal responses. In the present experiment the interference exerted by automatic word reading occurred at level of visuo-motor integration, that is at level of computation of movement parameters (i.e. acceleration, velocity) according to object features. It is well known that in the ventral and dorsal cortical visual streams objects are differently analysed in order to emit, respectively, a perceptual judgement or a motor response. In the ventral stream objects are analysed in a holistic way, whereas in the dorsal stream specific properties are extracted from them in order to plan a movement (Jeannerod, 1994; Milner & Goodale, 1995). This theory has been extended by postulating an involvement of aspects of object perceptual analysis in visuo-motor integration (Gentilucci & Negrotti, 1996; Gentilucci et al., 1996, 1997; Daprati & Gentilucci, in press). The results of the present experiment add the notion that also cognitive functions related to perception, such as language, can be involved in visuo-motor transformation. Many functional imaging studies have investigated the brain areas associated with word processing (Petersen et al., 1988; for a review see Nobre & Plunkett, 1997). Only few ones (Petersen et al., 1990; Price et al., 1994, 1996), however, have addressed the problem of the localization of the areas involved in automatic processes of word recognition that, according to the results of the present experiment, can influence the activity of those involved in motor control. These studies (Petersen et al., 1990; Price et al., 1994, 1996) have showed that, when non-linguistic perceptual analysis was required in response to word presentation, the areas, known to be essential for word processing from both lesion studies (for a review see Mesulam, 1990) and PET studies (for a review see Nobre & Plunkett, 1997), became active. However, the problem whether the activity of these areas could influence non-perceptual processes, such as those of visuomotor transformation, was not addressed. It has been found that language areas involved in generation of words related to actions can overlap or can be adjacent to those involved in visuo-motor integration (Martin et al., 1995; for a review see Nobre & Plunkett, 1997). A similar anatomical organization may be postulated also for the two processes of retrieving the meaning of adjectives related to an object and planning an action directed towards it. That is, the areas of pragmatic object representation may be involved in both movement preparation and automatic word reading.

Acknowledgements We thank Dr E. Daprati and Dr V. Gallese for the comments on the manuscript. The work was supported by grants CNR (Centro Nazionale delle Ricerche) to the Institute of Human Physiology of Parma and MURST (Ministero dell’ Universita` e della Ricerca Scientifica e Tecnologica) to the Institute of Human Physiology of Parma and to M.G.

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