Neuropsychologia, Vol.

28, No. 10, pp. 1095 1116, 1990. Printed in Great Britain.

0028 3932 t;0 $3.00+//.00 t 1990 Pergamon Press pie

I N T E G R A T I O N O F VISUAL I N F O R M A T I O N A N D M O T O R O U T P U T IN R E A C H I N G A N D G R A S P I N G : THE C O N T R I B U T I O N S O F P E R I P H E R A L A N D C E N T R A L VISION BARBARA SIVAK a n d CHRISTINE L. MACKENZIE Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada (Received 21 August 1989: accepted 11 May 1990) Abstract--This study examined the contributions made by peripheral and central vision to reaching and grasping. A specially designed contact lens system was used to restrict information to the peripheral retina. Modified goggles were used to restrict information to the central retina. A WATSMART motion analysis system was used to record and reconstruct three dimensional kinematic data. Analyses included an examination of peak kinematic values as well as a qualitative description of the trajectory profiles as related to transport and grasp components. With only peripheral vision, information related to size and shape of an object was inadequate, thus affecting the organization of both the transport and grasp components. With only central vision, information related to the location of an object was inadequate, affecting the organization of the transport but not the grasp component. Implications are discussed relevant to the current models of visuomotor control of reaching and grasping.

INTRODUCTION VISION HAS an i m p o r t a n t role when reaching to g r a s p an object. Vision is i m p o r t a n t for processing i n f o r m a t i o n a b o u t the spatial l o c a t i o n of objects a n d object characteristics such as shape, size, weight a n d texture. JEANNEROD [9, 10] identified t r a n s p o r t a n d grasp c o m p o n e n t s ; the h a n d m u s t be t r a n s p o r t e d to the correct l o c a t i o n a n d d u r i n g this time, the fingers m u s t be p o s t u r e d to g r a s p the object. He suggested the existence of parallel, i n d e p e n d e n t v i s u o m o t o r channels w h e r e b y the t r a n s p o r t c o m p o n e n t is o r g a n i z e d from i n f o r m a t i o n arriving via the v i s u o m o t o r channel a b o u t extrinsic p r o p e r t i e s of an object (e.g. the location), a n d g r a s p c o m p o n e n t is o r g a n i z e d from i n f o r m a t i o n arriving from the v i s u o m o t o r channel a b o u t intrinsic p r o p e r t i e s of an object (e.g. size a n d shape). In a d d i t i o n , visual i n f o r m a t i o n has been s h o w n to i m p r o v e m o v e m e n t accuracy in both p o i n t i n g a n d g r a s p i n g tasks. Studies t h a t have m a n i p u l a t e d " w h a t " is seen d u r i n g the m o v e m e n t have s h o w n that vision of b o t h the h a n d a n d target resulted in the greatest accuracy in an a i m i n g task [4, 6, 11, 19] a n d in a grasping task [10], c o m p a r e d to vision of just the target or hand. In these cases, vision of b o t h the h a n d a n d target allowed for the best visual e r r o r i n f o r m a t i o n . JEANNEROD [10] s h o w e d that w i t h o u t vision of the h a n d d u r i n g the m o v e m e n t to the object or no vision of the h a n d or object after m o v e m e n t began, subjects u n d e r s h o t the target by a p p r o x 1-2 cm. PRABLANC et al. 1-19] have r e p o r t e d that vision of the h a n d in its starting p o s i t i o n before m o v e m e n t begins also m a k e s a big difference in m o v e m e n t accuracy. F u r t h e r m o r e , the i m p o r t a n c e of "when" visual i n f o r m a t i o n is available d u r i n g the 1095

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movement has been shown to be relevant in determining movement accuracy. PAILLARD [ 16] and BEAUBATONand HAY [3] showed that subjects benefited most from visual feedback information provided towards the final phase of the movement. However, visual feedback provided at the beginning of the movement also improved accuracy over conditions when no visual feedback information was provided during the movement. When reaching to grasp an object, visual information is normally provided by both central and peripheral vision. This needs to be experimentally addressed. Information from central and peripheral vision is used by the motor system to enable accurate movements. PAILLARD and BEAUBATON[18], PAILLARD f l 6-1 and PAILLARDand AMBLARD [17] acknowledged the important role of central and peripheral vision in the control of visually guided reaching to a target. They suggested that movement cues, mainly processed in the peripheral field, used to control the direction of the arm movement and central vision, sensitive to positional cues, are important in the late phase of the movement for accurate positioning of the hand on a target. Decomposition of the visual field into its central and peripheral components suggests the following possible contributions to grasping an object. Individuals usually fixate the eyes and turn the head toward an object to be grasped. Before the start of the grasping movement, both the hand and arm are in peripheral vision and the object is in central vision. During the grasping movement, the hand and arm remain in peripheral vision. At the end of the grasping movement, the hand comes into central vision, along with the object, while the arm remains in peripheral vision. Thus, peripheral and central vision must provide specific information to the organization and control of the grasping movement. The purpose of these experiments was to examine the specific contributions of peripheral and central vision to the organization and control of reaching and grasping. This was possible through a physical optical separation of peripheral and central visual fields. If central vision was eliminated how were the organization and control of reaching and grasping affected? Referred to as the condition with only peripheral vision, this was compared to a normal vision condition. Likewise, if peripheral vision was eliminated, how were the organization and control of reaching and grasping affected? Referred to as the condition with only central vision, this was compared to a normal vision condition. Two separate experiments were conducted, one to eliminate central vision, and one to eliminate peripheral vision. It was decided not to combine these visual manipulations in one experiment for several reasons. The difference in the method of isolating peripheral vision and central vision did not lend itself to counterbalancing, thus creating the possibility of carry-over effects. For example, consultation with clinicians at the School of Optometry, University of Waterloo, led to the recommendation that subjects should not put their own contact lenses in the eye for at least 5 h after using the specially designed contact lenses to isolate only peripheral vision. As contact lens wearers were used as subjects in the visual condition that isolated peripheral vision, this experimental condition could not be followed by testing under the only central vision condition. Furthermore, the testing session would have been too lengthy and impractical. In the following experiments, the WATSMART (Waterloo Spatial Motion Analysis and Recording Technique) three-dimensional analysis system was used. The study of trajectories of movement has been used by various researchers to make inferences about central nervous system operations [1,13, 21]. Systematic variance and invariances in these kinematic profiles over various experimental manipulations may be a reflection of neural mechanisms subserving motor planning and control processes.

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EXPERIMENT 1

Reachin,q and ,qraspinq with only peripheral vision The purpose of this experiment was to examine the contributions made by peripheral vision to reaching to grasp an object. We hypothesized that with only peripheral vision the grasp component and not the transport component would be affected compared to normal vision. JEANNEROD [-9] suggested that the grasp component is organized from visual information about the intrinsic properties (e.g. size) of an object. Since peripheral vision is lacking in high resolution vision, it is logical to predict that the grasp component would be affected compared to normal vision. In contrast, JEANNEROD[9] suggested that the transport component is organized from visual information about the extrinsic properties (e.g. location ) of an object. Since peripheral vision has a large field of view and thus is capable of providing location information and information from the moving limb, we predicted that the transport component would not be affected compared to normal vision. The task required subjects to reach and grasp a wooden dowel placed in front of them with only a peripheral vision or full normal vision. Method Subjects. Six, right-handed university students were tested; all were experienced contact lens wearers. Subjects were instructed to wear their own corrective glasses over the experimental lenses if near vision needed correction. Method ~['isolatinq peripheral vision. A special contact lens system was developed using a piggyback contact lens design in which a partially painted hard lens was positioned on top of a special soft lens carrier (Fig. 1; for details see [20]). The hard lenses were painted black in the center so that when lenses were inserted in both eyes, no visual information was available through the center 10 of the visual field. Field size reduction was measured using a standard clinical tangent screen and procedure for individuals with central field impairment. Approximately l 0 of the central field remained as a scotoma and therefore could not be used to provide visual information even when the eyes or head moved. Apparatus and experimental set-up. The apparatus consisted of a wooden dowel 2.5 cm in diameter and I 1.5 cm in length. The starting position for the hand was on a table in front of the body midline of the seated subject. The distance between the start position and the dowel was 30 cm. Movements were in a forward direction in a sagital plane corresponding to the body midline. Procedure and experimental desi.qn. The subject's head was supported in a chin rest to stabilize the head in a straight ahead position. All visual conditions were conducted using binocular vision. However, in the only peripheral vision condition, if subjects looked straight ahead they could not see the dowel. Turning their eyes enabled subjects to see the dowel situated in front of them. Subjects turned the eyes approx 25 30' to position the dowel within the peripheral visual field of both eyes. Visual fixation of the dowel was controlled by the subject. Whether subjects looked to the left or to the right was counterbalanced among subjects by instructions from the experimenter. Pilot testing had revealed that whether both the head and eyes were turned to the left or right or whether the head remained in a straight ahead position and the eyes turned did not affect the transport or grasp components, for the midline reaches used in this experiment. Subjects were shown the apparatus before testing began. Subjects started each trial with the forearm and medial surface of the hand resting on the table. The tips of the index finger and thumb, touching in a relaxed manner, were positioned 2 cm above the starting position. Due to the resting posture and the location and shape of the object to be grasped, it was assumed that very little motion about the wrist occurred during the movement. Subjects were instructed to grasp the dowel near the top using the pads of index finger and thumb and lift it offthe table. Subjects were instructed to proceed at their own pace on hearing the word "go". Only the preferred right hand was tested. The left hand rested in the lap. The visual conditions included only peripheral vision (no central 10' of visual field, as restricted by the lenses) and normal vision (including both central and peripheral vision). Subjects participated in both conditions. The order of the visual conditions was counterbalanced. For each vision condition there were 16 trials, the first 4 of which were practice trials and not recorded. Of the remaining 12 trials, the last 8 trials free of problems were used in analyses of the data. Re:ordinq system. A three camera WATSMART system was used for recording and analysis of the data. 1REDs (infra-red emitting diodes) served as markers and were positioned on the proximal lateral corner of the index linger nail. proximal medial corner of the thumb nail and wrist (on the skin above the distal end of the radius) of each subject, as well as on the top center of the dowel. The wrist | R E D was used to indicate the transport component. The

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Fig. 1. E x p e r i m e n t 1. (a) C o n t a c t lens system used to restrict vision to peripheral retina. These lenses were inserted in both eyes. (b) Typical visual field m a p p e d for one subject when lenses were positioned in both eyes. N o t e that hatched area indicates that a p p r o x 1 0 of central vision remained as a scotoma.

subject, as well as on the top center of the dowel. The wrist IR E D was used to indicate the t r a n s p o r t c o m p o n e n t . The index finger and t h u m b I R E D s gave a measure of the aperture between the index finger and t h u m b to indicate the g r a s p c o m p o n e n t . The t w o - d i m e n s i o n a l position of the I R E D s over time was sampled at a frequency of 200 Hz by each of three cameras. The a n g u l a r placement of c a m e r a 1 a n d 2 was 4 4 , c a m e r a s 2 and 3 was 60 ~and c a m e r a s 3 and I was 104" to each other. The distances from the center of the calibration cube to c a m e r a s 1, 2 and 3 were 177 cm, 172 cm and 179 cm respectively. S t r o b i n g of the I R E D s a n d s a m p l i n g rate were controlled by the I B M - P C and W A T S M A R T unit. E r r o r of the W A T S M A R T d a t a as m e a s u r e d with the c a l i b r a t i o n cube was s h o w n to be less than 1 mm. In a d d i t i o n , static calculation of k n o w n distances between two I R E D s was accurate to within 1 mm. For each s a m p l i n g point the best two sets of two d i m e n s i o n a l co-ordinates were reconstructed after d a t a collection to provide three d i m e n s i o n a l c o - o r d i n a t e s of the position of the I R E D s . The d a t a were rotated to define X, Y and Z axes as follows: X axis as m o v e m e n t in the forward direction; Y axis as o r t h o g o n a l d e v i a t i o n from the forward direction (positive Y to the left); a n d Z axis as the m o v e m e n t vertically (positive Z is up). To s m o o t h and minimize d i s t o r t i o n of the reconstructed 3-D position data, a second o r d e r B u t t e r w o r t h filter p r o g r a m with a dual pass was used. This e l i m i n a t e d phase lag. A residual analysis of signal to noise ratio indicated 4 Hz as the o p t i m a l frequency to filter the data. Thus, the d a t a were filtered at a frequency of 4 Hz. The start and end of the m o v e m e n t were o p e r a t i o n a l l y defined by the use of a contact b r e a k i n g system. This

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consisted of a metal disk (2 cm dia., glued to the medial surface of the subject's hand) that made contact with a rectangular metal plate (3 cm x 2.5 cm) placed by the starting position. Lifting the hand broke contact and defined the start of the movement. A similar metal disk placed on the bottom of the dowel made contact with a similar rectangular metal plate. The end of the movement was defined when the contact was broken at the dowel lift. Contact breaking signals were recorded on a WATSCOPE channel concurrent with the recording on the WATSMART system. Movement time, defined as the time between breaking the start and end contacts, was used as one dependent measure. As well, trajectories were windowed and normalized in time, based on the start and end defined by the contact breaking system. Data analyses. After data were filtered, differentiated and windowed, analyses involved examination of peak kinematic values for both the transport and grasp components as well as a qualitative, descriptive analysis of the trajectory profiles. For the transport component (wrist IRED), velocity was derived from the filtered displacement data from each of the X, Y and Z axes using the central finite difference method. Each of these X, Y and Z velocities was then squared and the square root of their sum provided a measure of the resultant velocity (or speed along the path of the trajectory) for any given point in time. The resultant velocity data were differentiated to obtain the rate of change of speed along the path of the movement; for simplicity, these will be referred to as "acceleration data". For the grasp component, the distance between the thumb and index finger IREDs was calculated from the filtered displacement data over the time course of each trial. The process of normalizing profiles (velocity, acceleration and aperture) was obtained by scaling each trial in the temporal domain to 100 points after velocity and accelaration were derived. This procedure permitted comparisons to be made between curves across experimental conditions. That is, systematic patterns in the time normalized profiles can be used to infer underlying organization and control processes. If across experimental conditions, temporal scaling of curves related to the transport and grasp components does not result in curves of the same shape, this may be interpreted as evidence for different organization and control processes [14]. Transport component. Dependent measures were derived from kinematic peaks for the wrist IRED. We report the times (msec) to the kinematic peaks and normalized time (per cent MT) after the kinematic peaks. The dependent measures included: peak speed along the path of the movement (highest point on the resultant velocity curve), time spent to reach peak speed (msec), per cent of movement time spent in deceleration {from peak speed to the end of the movement, from time normalized profiles), peak acceleration along the path of the trajectory (highesl point on the differentiated resultant velocity profile), time spent to peak acceleration (msec), per cent of movemenl time spent after peak acceleration to the end of the movement, peak deceleration along the path of the movement (lowest point on the differentiated resultant velocity profile), time spent to peak deceleration (msec), and per cent of movement time spent after peak deceleration to the end of the movement. These measures were computed for each trial. Means and SDs were computed over 8 trials in each experimental condition and for every subject. Grasp component. For grip aperture (distance between the thumb and index finger IREDs), the following dependent measures were derived: maximum aperture (largest distance between thumb and index finger IREDs), time to reach maximum aperture (msec), per cent of movement time spent after maximum aperture (from time normalized profiles). Mean and SD values were computed over 8 trials for each dependent measure in each experimental condition and for every subject.

Results T a b l e s 1 a n d 2 c o n t a i n a s u m m a r y o f all d e p e n d e n t m e a s u r e s for t h e t r a n s p o r t a n d g r a s p c o m p o n e n t s for t h e t w o v i s u a l c o n d i t i o n s r e s p e c t i v e l y . M o v e m e n t time. A r e p e a t e d m e a s u r e s a n a l y s i s o f v a r i a n c e o f m o v e m e n t t i m e r e v e a l e d t h a t subjects moved slower when they had peripheral vision than with normal vision, F ( 1, 5) = 13.1, P < 0.01. M o v e m e n t t i m e v a l u e s r a n g e d f r o m 1502 m s e c t o 1797 m s e c for o n l y p e r i p h e r a l v i s i o n a n d f r o m 1018 m s e c t o 1205 for n o r m a l v i s i o n . It is s u g g e s t e d t h a t s u b j e c t s m o v e d s l o w e r b e c a u s e t h e y w e r e c a u t i o u s as a r e s u l t of t h e u n n a t u r a l v i s u a l s i t u a t i o n c r e a t e d with peripheral vision. Transport component. A n a l y s e s o f v a r i a n c e o f p e a k v e l o c i t y v a l u e s r e v e a l e d t h a t s u b j e c t s r e a c h e d a l o w e r p e a k s p e e d w i t h o n l y p e r i p h e r a l v i s i o n (424 m m / s e c ) t h a n w i t h n o r m a l v i s i o n (533 m m / s e c ) , F (1, 5 ) = 8 . 1 3 , P < 0 . 0 5 (Fig. 2(a)). A l s o , s u b j e c t s s h o w e d a t e n d e n c y to r e a c h p e a k s p e e d l a t e r w i t h o n l y p e r i p h e r a l v i s i o n (574 m s e c ) t h a n n o r m a l v i s i o n (440 m s e c ) , F(1, 5)=4.23, P

Integration of visual information and motor output in reaching and grasping: the contributions of peripheral and central vision.

This study examined the contributions made by peripheral and central vision to reaching and grasping. A specially designed contact lens system was use...
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