The role of binocular vision in prehension: a kinematic analysis

Vision Res. Vol. 32, No. 8, pp. 1513-1521, 1992 Printed in Great Britain. All rights reserved

Copyright

The Role of Binocular a Kinematic Analysis PHILIP

SERVOS,*

MELVYN

A. GOODALE,*?

0042-6989/92 $5.00 + 0.00 cI 1992 Pergamon Press Ltd

Vision in Prehension:

LORNA

S. JAKOBSON*

Received 8 November 1991

This study examined the contribution of binocular vision to the control of human prehension. Subjects reached out and grasped oblong blocks under conditions of either monocular or binocular vision. Kinematic analyses revealed that prehensile movements made under monocular viewing differed substantially from those performed under binocular conditions. In particular, grasping movements made under monocular viewing conditions showed longer movement times, lower peak velocities, proportionately longer deceleration phases, and smaller grip apertures than movements made under binocular viewing. In short, subjects appeared to be underestimating the distance of objects (and as a consequence, their size) under monocular viewing. It is argued that the differences in performance between the two viewing conditions were largely a reflection of differences in estimates of the target’s size and distance obtained prior to movement onset. This study provides the first clear kinematic evidence that binocular vision (stereopsis and possibly vergence) makes a significant contribution to the accurate programming of prehensile movements in humans. Humans Prehension Visuomotor behavior

Monocular

Binocular

Limb movements

INTRODUCTION The study of depth vision in humans has concentrated almost entirely on perceptual judgments about the visual world, and has largely ignored the role of depth cues in the programming and execution of skilled motor behavior. Moreover, most of these studies have focussed on estimates of the relative depth of objects as opposed to their actual distance from an observer. Yet many everyday actions, such as reaching out and picking up an object, require precisely the latter type of estimate. For example, perceiving that a coffee cup is closer to you than a box of cornflakes will be of limited use in planning the movements required to pick up that cup. What is needed here is an accurate estimate of the actual distance of the cup so that an efficient reaching movement can be executed without constant monitoring of the relative distances of the hand, cup and cereal box. What then are the visual cues that might form the basis of such estimates? In principle, a number of cues could be used, particularly with familiar objects. With respect to prehensile movements directed toward unfamiliar stationary targets, however, there are four strong candidates: (1) motion parallax, (2) accommodation, (3) vergence movements, and/or (4) stereopsis (in conjunction with binocular vertical disparities or perhaps vergence information). Although monocular cues such as

*Department

Ontario, tTo whom

of Psychology, University of Western Ontario, Canada N6A 5C2. all correspondence should be addressed.

London,

Distance estimation

Visual feedback

accommodation (Biersdorf, Ohwaki & Kozil, 1963; Fisher & Ciuffreda, 1988; but see Morrison & Whiteside. 1984) and motion parallax (Ferris, 1972; Gogel, 1982) could clearly provide some distance information, it is commonly believed that binocular cues are the most important source of absolute distance information (Bishop, 1989; Foley, 1980). But while several authors have suggested that such cues might play a critical role in the programming and execution of prehension in primates, including humans (Previc, 1990; Sheedy, Bailey, Buri & Bass, 1986), there have been almost no systematic investigations of the role of binocular vision in the control of this important skill. The purpose of the present study, then, was to examine the effect of removing this important source of distance information on the kinematics of normal reaching and grasping movements in humans. What evidence is there that binocular vision can provide estimates of distance that are accurate and reliable enough for the programming of prehensile movements? The perceptual literature would appear to suggest that convergence by itself is unable to provide the accurate distance estimates that are implicit in most acts of prehension. Thus, while observers are able to estimate the absolute distance of objects on the basis of convergence alone, their trial-to-trial performance is rather variable (Irving & Ludvigh, 1936; Heineman, Tulving & Nachmias, 1959; Gogel, 1961; Ogle, 1962; Foley & Held, 1972; Morrison & Whiteside, 1984). These studies are consistent with the finding that humans have great difficulty estimating the degree to which their eyes

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arc converged (Hill, 1972). At the level of perceptual report then. convergence appears to be a poor candidate for the generation of absolute distance estimates. It should be emphasized, however, that nearly all of these studies have relied on some sort of explicit report or cognitive judgment (i.e. they have depended on the subject’s conscious perception of distance). Subjects have not been asked to produce a motor output, such as a manual aiming movement, where the distance estimate is implicit in the act itself rather than explicitly required. It is entirely possible therefore that binocular cues such as convergence might provide accurate distance information for the control of motor output even though this information is not available for conscious perceptual report. Dissociations between perceptual report and visuomotor control have certainly been observed in a number of different paradigms where the location of a visual target has been manipulated (Bridgeman, Lewis. Heit & Nagle. 1979; Goodale. Pelisson & Prablanc. recent neuropsychological evidence 1986). Indeed, suggests that the neural substrates for perception and associated cognitive judgments may be quite independent of those underlying the visual control of skilled movements of the hand and limb (Goodale, Milner. Jakobson & Carey, 1991; Milner & Goodale. 1992). Paradoxically, absolute distance information must be implicitly available to permit the occurrence of certain perceptual phenomena such as stereoscopic depth constancy (Ono & Comerford, 1977). Vergencc is one of two sources of information that could provide the necessary absolute distance information for stereoscopic depth constancy (Foley. 1980); the other is vertical binocular disparities (Longuet-Higgins, 1982; Bishop, 1989; although see Cumming, Johnston & Parker, 1991). In contributing to the required computations, both of these mechanisms would appear to operate at a level that is most likely inaccessible to perceptual report. Moreover, both mechanisms function optimally at egocentric distances of up to approx. I m-viz. a region generally corresponding to prehension space. Thus, as was indicated earlier, either of these mechanisms, or both. could be used in the implicit computations of absolute distance required by the sensorimotor systems supporting prehension. Nevertheless, vergence and vertical disparities will generate absolute distance estimates only when the objects lie in the fixation plane. To compute the absolute distance of objects lying on either side of the horopter. horizontal disparities (stereopsis and even diplopic images) must also form part of the equation. In short, a constellation of binocular cues (e.g. vergence, vertical disparities, and stereopsis) could theoretically provide the information required for the programming of accurate prehensile movements of the hand and limb. There have been only a few attempts to investigate the role of such cues in the control of prehension. Moreover, such attempts have relied on rather indirect measures of performance, such as time to complete a task and accuracy, and have not looked at the kinematics of the actual movements produced under the different viewing

conditions. Moreover. the role of ;rhsolute dtstancc estimation in the performance of these [asks has been largely ignored. Sheedy et ul. (1986), for example, compared the performance of subjects on sel’eral manual tasks (e.g. threading beads onto a string) under monocular versus binocular viewing conditions. It was found. In general, that performance was best in the binocular condition. Tasks like threading beads, however, do not require the computation of absolute distance. While one task used by Sheedy et ~1. ( 1986). tossing bean bags at targets, presumably did involve some estimation of distance, only sketchy information about subjects’ performance was provided. Furthermore. the kinematics of the constituent movements were never examined in any of these tasks. The present study not only examined the kinematics of prehension under monocular vs binocular viewing conditions but also varied the size and distance of the objects that the subjects were required to pick up. Moreover, a viewing environment was selected which afforded a rich array of monocular and binocular depth and distance cues, an array similar to that available in everyday life. It was reasoned that if kinematic measures of movements made under binocular viewing differed significantly from those made under monocular viewing then this would provide strong support for the argument that binocular distance cues are critical to the guidance of manual prehension. What kinds of kinematic measures would be expected to change as a function of viewing condition’! Evidence from a number of anatomical, neurological, and developmental studies suggests that visually guided prehension consists of two relatively independent, but temporally-coupled, components (for review, see Jeannerod, 1988). One of these components is the reach itself in which the hand is transported to the location of the target object. The second component is the grasp, in which the posture of the hand and fingers is adjusted to reflect the size, shape and orientation of the object well before contact is made. A number of studies have shown that the peak velocity of the reach and several other transport kinematics vary as a function of object distance, whereas the grasp itself varies primarily as a function of the size of the target object (Jeannerod, 1988). The calibration of the grasp, of course, also depends on estimates of distance (Jakobson & Goodale, 1991), particularly with unfamiliar objects where object distance must be combined with the size of the subtended retinal image to compute object size. Thus. in the present experiment, where object size and distance were varied randomly from trial to trial, it was anticipated that the removal of binocular distance cues would interfere with the calibration of both the transport and the grasp components of manual prehension. METHOD

Subjects Nine undergraduates with normal or corrected-tonormal vision participated for pay (five males and four

BINOCULAR

VISION AND PREHENSION

females, mean age = 22.6 yr). All subjects were strong righthanders as determined by a modified version of the Edinburgh Handedness Inventory (Oldfield, 1971). Six subjects were right-eye dominant while the remaining three subjects were left-eye dominant. All subjects had stereoscopic vision in the normal range with assessed stereoacuities of 40” of arc or better as determined by the Randot Stereotest (Stereo Optical Co., Chicago, Ill.). Apparatus

Subjects sat at a table, 100 cm wide and 55 cm deep. The surface of the table was painted flat black. A circular 1 cm dia microswitch button located 15 cm from the subject functioned as the start position for each reaching movement. This button was located directly at the body midline. A circular fluorescent lamp was suspended approx. 80 cm above the table surface. This lamp, in which the condenser was pre-activated, could be illuminated by the experimenter from a remote switch which also triggered the start of data collection. Full illumination was achieved within 80 msec. Three red, oblong wooden blocks with the following top surface dimensions were used: 2 x 5, 3 x 7.5, 5 x 12.5 cm. All of the objects were 2cm high. The underside of each of the objects contained an embedded magnet, and could be positioned so as to make contact with one of three magnetic switches located under the table surface at distances of 20, 30 or 40 cm from the microswitch, along the midline. Upon picking up an object the contact between these two magnets was broken, signaling the end of collection for a given trial. Three 4 mm dia i.r. light-emitting diodes (IREDs) were attached with small pieces of cloth tape to the head of the radius at the wrist, the distal portion of the right border of the thumbnail, and the distal portion of the left border of the index fingernail. The tape permitted complete freedom of movement of the hand and fingers. The three IREDs were monitored by two high-resolution cameras positioned appox. 2 m from the subject. The instantaneous positions of the IREDs were digitized at a rate of 100 Hz into two-dimensional coordinates and then passed on to the data collection system of a WATSMART computer (Waterloo Spatial Motion Analysis and Recording Technique, manufactured by Northern Digital Inc., Waterloo, Ontario). Procedure

Subjects were instructed at the beginning of each session to make quick, accurate, and natural reaches with their right hand, picking up each object with their thumb and index finger along the long axis of the object, which was always perpendicular to the body midline. They were instructed to pick up the block as soon as the overhead light was illuminated and the block became visible. Subjects were told that prior to the start of a given trial they were to place the tips of the index finger and thumb of their right hand on the start button. For approximately a 5 set period before a given trial (i.e. as

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soon as the overhead fluorescent light was extinguished from a previous trial), subjects sat in the dark with their eyes closed. Once a block had been placed in a given position by the experimenter, subjects were given a ready signal which prompted them to open their eyes and to anticipate the illumination of the overhead light approx. l-2 set later. Two testing sessions were administered, each spaced at least 24 hr apart. The first session consisted of a handedness questionnaire, a test for eye dominance, a stereoacuity test, and a block of 72 experimental trials. five subjects were tested first under binocular viewing conditions while the remaining four subjects were first tested monocularly using their dominant eye (the nondominant eye was patched). The second session consisted of 72 trials either under monocular or binocular viewing conditions followed by 2 counterbalanced blocks (one monocular, the other binocular) of 27 trials of a simple reaction-time (RT) task. The experimental set-up for the RT task was identical to that used in the prehension conditions except that instead of picking up an object, subjects simply lifted their thumb and index finger off of the start key as quickly as possible when a block became visible. Subjects were explicitly instructed not to reach towards the blocks. RT was monitored by the release of the start key, On each test day, the 72 reaching trials consisted of 8 instances of each of the 9 possible distance x object size combinations. Trial presentations were random except for the stipulation that no more than 3 consecutive, identical trials were allowed. Also, in order to look at possible practice effects, each block of 72 trials consisted of two blocks of 36 trials (4 instances of each distance x object size combination). The simple RT task consisted of 3 instances of each of the 9 possible distance x object size combinations. All prehension conditions were preceded by a series of 5 practice trials while the simple RT conditions were preceded by a series of 3 such trials. Any trials in which the subject dropped an object were repeated at the end of a given block. Such occurrences were rare. Each testing session lasted approx. 90min. Accuracy of system

Calibration of the WATSMART system involved placing in the experimental workspace a rigid frame to which were attached 24 IREDs at known locations. The WATSMART calibration software calculated the threedimensional root-mean-square error of reconstruction for the locations of a minimum of 22 IREDs to be < 2 mm. A procedure similar in principle to that described by Haggard and Wing (1990) was used to provide an independent assessment of the system’s accuracy. Three IREDs were embedded in a rigid surface to form the vertices of a right-angled triangle measuring approx. 10 x 15 x 18 cm. The “triangle” was positioned adjacent to the start key of the experimental apparatus and in another trial it was placed along the midline, approx. 30 cm beyond this poistion in the x (forward-going) dimension. The three-dimensional coordinates of

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breaking the magnetic switch); (3) maximum grip aperture (the maximum vectored distance between the thumb and index finger IREDs); (4) peak resultant velocity and (5) the time at which it occurred following movement onset; (6) peak acceleration in the x (forward/backward) dimension and (7) the time at which it occurred following movement onset; (8) peak deceleration in the .V (forward/backward) dimension and (9) the time at which it occurred following movement onset. Measures (4) (9) were based upon data from the wrist IRED.

=3ocm

Object

;;

SERVOS

200

RESULTS 0

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500

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FIGURE subject-one

I

I 1000

1500

I 2000

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I. Velocity profiles for two reaches made reach was made under normal binocular other under monocular control.

by the same control, the

the static IREDs were sampled for 2 set in each location at a sampling frequency of 100 Hz. Comparisons of the average distance between any two given IREDs in both regions of the workspace were quite consistent, with differences ranging from 0.93 to 2.18 mm. The standard deviations of these measurements within each of the 2 set sampling periods varied from 0.29 to 1.10 mm. Data processing

The stored sets of two-dimensional coordinates were converted into three-dimensional coordinates off-line and filtered (a second-order Butterworth filter with a 7 Hz cut-off). The IREDS on the index finger and thumb provided information about the grip portion of the reach while all other kinematic variables were based on information from the wrist IRED. Dependent measures

Nine kinematic measures were computed from the three-dimensional coordinates corresponding to a given prehensile movement. These were: (1) time to movement onset (measured as the time for the thumb and index finger to release the mechanical start key); (2) movement duration (calculated by subtracting the movement onset time from the time at which an object was lifted, TABLE

I. Summary

For each of the nine subjects, mean values of each of the dependent variables were calculated across a minimum of 6 observations for each size x distance combination in each viewing condition. (Equipment failure resulted in some loss of data, but this constituted < 1% of the trials.) The mean values were entered into separate 2 x 3 x 3 x 2 (viewing condition x object size x object distance x practice) repeated measures analyses of variance. (The factor Practice, refers to a comparison between the first and last 36 trials of a given condition. There was no significant main effect of Practice for any kinematic variable. Nor were there any interpretable interactions with any other factor.) Degrees of freedom were corrected according to the Huynh-Feldt adjustment (Huynh & Feldt, 1976). All tests of significance were based upon an alpha level of 0.05. The effects qf aiewing condition on the transport component Summary of mainfindings. Figure 1 shows the velocity

profiles of two individual trials, one made under binocular viewing conditions, the other under monocular. Many of the differences in the transport component that became apparent under analysis of variance are illustrated in this figure. Under monocular vision, the latency to begin the movement and the movement duration were longer than under binocular vision. In addition, the peak velocity and acceleration of the reach under monocular vision were reduced relative to binocular vision. Finally, the time spent decelerating was longer under monocular viewing, particularly in the period of low velocity movement at the very end of the reach. (Means and tests of significance for each of these measures are summarized in Tables 1 and 2.)

table of effect of viewing condition on various values indicated in parentheses) Viewing

kinematic

variables

(SEM

condition

._ Kinematic

variable

Movement onset (simple) (msec) Movement onset (msec) Movement duration (msec) Peak velocity (mm/xc) Peak acceleration (dm/se?) Time to peak velocity (msec) Time to peak acceleration (msec) Maximum grip aperture (mm)

Monocular

Binocular

615 578 838 905 49 255 I16 84

500 (10.9) 496 (3.0) 611 (13.1) 1099 (23.7) 67 (I .7) 221 (3.7) 104 (3.4) 90(1.0)

(8.9) (3.4) (13.7) (15.6) (1.0) (3.0) (2.6) (1.1)

F statistic F,,,,, = 5.14. P < 0.05 F,,,,, = 87.25. P < 0.001 F,,,,,=21.40, P0.05 F,,,,,=5.11, P-CO.05

BINOCULAR TABLE

2. Summary

VISION

AND

table of kinematic markers related to the deceleration transport component of prehension Viewing

Kinematic

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PREHENSION

variable

Time spent decelerating (msec)* Normalized time spent decelerating (%)t Time spent in low velocity movement (msec)$ Normalized time spent in low velocity movement (%)$

Monocular 583 (12.7) 68.6 (0.5)

phase

of the

condition F statistic

Binocular 390 (10.3) 62.9 (0.5)

F,,,,, = 19.71, P <0.002 F<,,8)= 12.98, I’ < 0.007 = 60.26, P < 0.0001

441 (12.0)

247 (8.9)

&)

51.2 (0.7)

39.1 (0.8)

F,,,,,=54.70,

PiO.0001

*Calculated by subtracting the time to peak velocity from movement duration. tcalculated by subtracting the time to peak velocity from movement duration and dividing this difference by the movement duration (expressed as a percent). SCalculated by subtracting the time to peak deceleration from movement duration. §Calculated by subtracting the time to peak deceleration from movement duration and dividing this difference by the movement duration (expressed as a percent).

Diferences in deceleration phase. When reaching under monocular viewing conditions, subjects spent proportionately more time in the deceleration phase of the reach than under normal binocular viewing. In general, under monocular viewing conditions subjects spent 69% of their movement time decelerating compared to 63% under binocular viewing (see Fig. 1 and Table 2). In the final portion of the deceleration phase (defined as the part of the reach following the point of peak deceleration), a region characterized by low velocity movement, is compared between the monocular and binocular conditions, an even more dramatic difference becomes apparent. Under monocular viewing, subjects reached peak deceleration with more than 440 msec or 51% of the entire reach remaining. This contrasts sharply with their binocular performance, where they reached peak deceleration with less than 250 msec or 39% of the reach remaining (see Table 2). In other words, subjects in the monocular vision condition typically exhibited a relatively long tail of low velocity movement in the latter portion of the velocity profile. This elongated period of low velocity movements can also be seen in Fig. 1. The effects of object distance and size. Despite the clear differences in the kinematics of monocular and binocular reaches, most of these measures were correlated with distance under both conditions (see Fig. 2). In other words, removing binocular information did not abolish the usual relationship between distance and such measures as movement duration, peak velocity, and peak acceleration that others have reported (Jakobson & Goodale, 1991; Jeannerod, 1988); i.e. that reaches to distant objects take longer and reach higher peak accelerations and velocities than do reaches to closer objects. Nevertheless, the nature of the relationship between distance and some of these measures was not identical under the two viewing conditions. As can be seen in Fig. 2(B), for example, peak velocity showed a larger increase as a function of distance under binocular as compared to monocular viewing (viewing x distance interaction, F (,,,9,9.531 = 8.10, P < 0.02). At the same time, the increase

in movement duration that occurred with distance was larger under monocular than binocular viewing (viewing x distance mteraction, FC,,69,,3,53) = 8.94, P < 0.005). (A) 1250

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FIGURE 2. (A) Movement duration (msec) as a function of object distance and viewing condition. (B) Peak velocity (mmjsec) as a function of object distance and viewing condition. (C) Peak acceleration (cm/set) as a function of object distance and viewing condition.

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PHILIP SERVOS C/ al.

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50

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grip aperture(mm) as a function of object size and viewing condition.

The size of the object also appeared to affect several kinematic measures of the transport component of the reach. Reaches to larger objects took longer and reached higher peak velocities than reaches to smaller objects (respectively: F(,.&-1,.431= 23.97, P < 0.0001; F (2.0.16.0) = 6.74, P c 0.008). In addition, it took longer to achieve peak velocity with larger objects (~C2,0,,6.0, = 7.89, P < 0.004). There were no interactions with viewing condition. These effects of object size on the transport component of prehension are consistent with recent observations by Jakobson and Goodale (1991). The effects of viewing condition on the grasp component

The calibration of the grasp, as measured at maximum aperture, differed between viewing conditions. Although subjects in the monocular condition still scaled their grasp they did not open their hand as widely as they did under binocular viewing (see Table 1 for summary of means and tests of significance). There was also a significant interaction between viewing condition and object size such that this difference was most apparent for the two smallest objects but was diminished for the largest object. This could be due to ceiling effects in the size of the grasp that can be made when reaching towards larger objects (see Fig. 3). Simple reaction time

As Table 1 indicates, the pattern of RTs obtained under the simple RT conditions did not differ from those observed in the prehension experiment.

DISCUSSION Binocular vision and prehension -general

findings

Restricting vision to only one eye had dramatic effects on the normal pattern of reaching and grasping movements. Such reaches were slower to begin, achieved a lower peak velocity, and lasted longer than reaches made with binocular vision. In addition, under monocular viewing conditions, subjects spent proportionately more time decelerating and achieved smaher grip apertures than they did under binocular viewing. These differences in the kinematics were remarkably stable and did not change over a given testing session.

It is tempting to conclude that the more ctlicient performance of subjects under binocular viewing conditions was a direct consequence of the availability of binocular depth cues for the initial programming and on-line control of manual prehension. At least some of these differences, however. might simply have been due to binocular summation effects for object detection (see e.g. Haines, 1977; Ueno, 1977; Blake, Sloane & Fox. 1981; Jones & Lee, 1981). The simple RT task was used to test for this possibility. As Table 1 indicates, the binocular RT advantage was observed in both the simple RT task and in the prehension task, and was ofa similar magnitude. This suggests that binocular summation effects might account for the binocular RT advantage in the latency to initiate the movement; i.e. two eyes are more efficient at detecting the stimulus object than one. Other kinematic differences between the monocular and binocular conditions, however, are less easily explained by binocular summation arguments (see Tables 1 and 2). If computations of object distance and size were simply less reliable under monocular as opposed to binocular viewing conditions, then one might have expected to see increases in the variability of performance but no change in the mean values of kinematic variables such as peak velocity and acceleration. Quite the opposite pattern was observed, however. In other words. variability in performance did not change as a function of viewing conditions but the mean values of these kinematic measures did. Strategy eflects

The differences in the kinematics between the two viewing conditions serve to demonstrate that the removal of binocular information, even in a viewing environment that contains a rich array of monocular cues, can interfere with the performance of a skilled prehension movement. Thus, even though monocular cues such as motion parallax (head movements were not restricted), relative position, accommodation, and possibly familiar size (since the three objects were not perfectly proportional) were available, subjects’ performance was clearly disturbed by the removal of binocular information. Of course, one possible interpretation of many of the observed monocular-binocular differences is that the kinematic changes evident in the monocular condition were simply the consequence of a motor strategy the subjects used to cope with a predicted reduction in the opportunity to fine-tune the movement during its execution. In other words, it is possible that subjects were treating the monocular task as an essentially open-loop problem where visual information was degraded during movement execution. After all, the subjects were tested in blocks of monocular trials where such strategies could be evoked. Evidence from a recent study by Jakobson and Goodale (1991), however, makes this an unlikely possibility. Jakobson and Goodale tested 15 subjects under binocular vision in blocks of either visually closed or open loop using a set-up identical to

BINOCULAR

VISION

that used in the present study. Subjects were presented with a binocular view of the object, but when the movement was initiated vision of the hand and the target was removed. No differences were found between visually open- and closed-loop conditions with respect to the duration of reaching movement, length of the acceleration phase, and peak velocity [see Fig. 4(A-C)]. It appears then, from the work of Jakobson and Goodale (1991), that the initial binocular view of the object and the hand at the beginning of a reaching movement determines a good deal about its kinematics even if vision of the object and hand is denied during movement execution. It therefore seems unlikely that the slower movements produced under monocular viewing reflected a motor strategy designed to compensate for an anticipated degradation in visual control during the reach. Rather, these changes were more likely due to the characteristics of the monocular array itself, i.e. an array lacking only binocular cues. An underestimation of size and distance

In what way then, did the nature of the monocular array determine the observed differences in performance? Evidence from both the reach and grasp components of prehension is consistent with the notion that subjects in the monocular viewing condition were underestimating the distance of the target object and thus its size as well. First, the overall peak velocity of reaches was lower in the monocular viewing condition relative to the binocular condition even though subjects were still scaling for object distance. Notice in Fig. 2(B) that the

Duration

-

AND

slopes of the velocity-distance functions for the two conditions are quite similar. A similar interpretation can also be made with respect to peak positive acceleration. Indeed, the long period of deceleration discussed earlier could have reflected in part the need to adjust a trajectory that was programmed on the basis of an underestimate of object distance. Second, subjects in the monocular condition tended to generate smaller grip apertures although they still scaled their grips for object size. Such behavior is consistent with the idea that they were underestimating object distance, since the retinal image of the object combined with an underestimate of object distance would generate a corresponding underestimate of object size. It is again important to note that the smaller grip apertures observed in monocular testing cannot be explained by suggesting that subjects were employing a strategy designed to deal with open-loop conditions. Jakobson and Goodale (1991) observed that far from decreasing grip aperture, subjects reaching under openloop conditions achieved a maximum grip aperture that was larger than that observed under normal viewing conditions [see Fig. 4(D); see also Wing, Turton and Fraser, 19861. The present findings are generally at odds with studies which have investigated explicit perceptual estimates of distance under monocular and binocular viewing. For example, Crannell and Peters (1970) found that subjects generally underestimated the distance of a point source of light in both monocular and binocular viewing conditions. This study, however, did not employ

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FIGURE 4. Comparison of several kinematic variables under monocular and binocular viewing conditions (present study Exp. A above), and under visually “closed” and “open” loop testing conditions (from Jakobson & Goodale, 1991; Exp. B. above). (A) Movement duration (msec). (B) Peak velocity (mmjsec). (C) Duration of accleration phase (msec). (D) Maximum grip aperture (mm).

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PHILIP

SfiRVOS (‘I (I/.

three-dimensional objects nor did it present targets in grasping space; the closest target used was over 60cm away from the subjects. In fact, Foley (1977) found that subjects overestimated the distance of point light sources in both monocular and binocular viewing conditions when those light sources were presented in grasping space. Moreover, the overestimates made under monocular viewing were greater than those made under binocular vision. The same pattern of results was obtained when the subjects indicated the distance of the target by pointing under the table. Of particular relevance to the present findings is the fact that Foley’s (1977) subjects were more accurate under binocular viewing conditions when actual objects, rather than point sources of light, were used. Indeed, in this case, their verbal estimates slightly underestimated the distance of the objects although their manual estimates continued to overestimate the distance. Unfortunately, an analogous monocular testing condition with actual objects was not employed. The discrepancy between the present findings and those reported by Foley (1977) could be due to a number of things. First, the subjects in the Foley study were making explicit estimates of a target’s distance rather than simply reaching out and picking up an object. Even the manual pointing movements in the Foley study were an explicit attempt to replicate the distance of the target. Indeed, as mentioned in the Introduction. explicit judgments of this sort, even when made using a manual response, may well depend on visual processing that is quite separate from that controlling visually guided grasping (Goodale cr ul., 1991). Second, the pointing movements were made under visually open-loop conditions. Subjects in Foley’s study could not see their arm or hand under the table and as a consequence could not determine the accuracy of their end position with respect to the target. In the present study, of course, subjects had plenty of opportunity to correct their movements in flight, Finally, the pre-movement target viewing times in the two studies were probably different as well. In the present study, subjects on average viewed a given target (prior to movement onset) for only 500-600 msec whereas in the Foley study subjects presumably could take as long as they wished to indicate a given target’s distance. In future studies, we are planning to make direct comparisons between perceptual and “motor” estimates of distance under monocular and binocular viewing. At present, however, it remains unclear as to why subjects reaching towards objects under monocular viewing conditions appear to underestimate the distance of those objects. Pre-movement prehension

programming

and

on-line

control

of

Although the pattern of differences between monocular and binocular conditions suggests that binocular cues make an important contribution to the control of pre-

hension, the question remains as to where in the programming

and execution

of the constituent

movements

binocular information is used. Some clues are provided by the timing of the kinematic differences observed. The fact that peak acceleration and peak velocity are kinematic markers that occur quite early in the trajectory of a reach means that it is quite likely that monocular-binocular differences related to these variables were the consequence of differences in the initial programming rather than modifications that occurred during the execution of the movement. Peak acceleration, for example, was achieved in both viewing conditions at approx. 100 msec after movement onset a time window in which there would have been no opportunity for on-line modification of the reach trajectory. Moreover, recent unpublished work in our laboratory suggests that switching from a binocular to a monocular view immediately after subjects have initiated their reaches does not affect these early kinematic markers. Finally. evidence from the open-loop study (Jakobson & Goodale, 1991) discussed earlier provides additional support for the notion that the setting of many of the kinematic parameters takes place during the initial view of the object. Other changes that occurred in the monocular condition of the present experiment could have reflected the removal of a binocular contribution to on-line modification of the reach. Subjects. for example, spent a significantly longer period of time in the deceleration phase of the reach under monocular vision than they did when they could view the object with both eyes. In fact, whereas in the binocular condition subjects spent less than 40% of the reach in the low velocity deceleration phase, subjects under monocular vision spent over 51% of the reach in this phase. This suggests that subjects may have engaged in more on-line modification of their movement trajectories in the monocular condition relative to the binocular condition, since most adjustments to the reach occur in this low velocity portion of the movement (Soechting, 1984: Fisk & Goodale, 198X). This could mean, of course, that in the current study the longer deceleration phase under monocular viewing simply represented an attempt by the subjects to deal with an initial underestimate of target distance. Some recent work in our laboratory suggests. however, that the absence of binocular control during the actual reaching movement can result in a relatively longer lowvelocity phase at the end of the reach, even when the initial view of the object was binocular. Whatever the reason, it is clear that reaches made under monocular viewing are less efficient than those made under normal binocular viewing conditions. The contribution of individual binocular mechanisms to the initial programming and on-line control of prehension is at this point an open question. In the present experiment the entire movement, including its preparation, was performed under either monocular or fully binocular viewing conditions. Moreover. no attempt was made to isolate particular binocular cues. It is quite possible that rather different sources of binocular information are used in movement planning and execution. The initial programming of the movement, for example, could rely on a number of different binocular cues,

BINOCULAR

VISION

including stereopsis [and its allied absolute distance estimation mechanism(s)], convergence or a combination of these mechanisms. These cues could also play a role in on-line control. In addition, two other potential sources of information are available for on-line control. When the subject foveates a target, stereomotion from the moving hand (Regan, Erkelens & Collewijn, 1986) and (possibly) the extent of diplopia between the two eyes’ images of the moving hand (Hering, 1861; cited in Hochberg, 1971) could provide information about the hand’s trajectory. Although the contribution of all these mechanisms needs to be disentangled, the present study demonstrates that the removal of binocular vision in a situation which is otherwise rich in depth cues has a profound effect on the spatiotemporal organization of prehensile movements.

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Acknowledgements-This research was supported by Medical Research Council of Canada Grant No. MA-7269 to M. A. Goodale. L. Jakobson and P. Servos are recipients of Medical Research Council of Canada Studentships.