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Hemispheric differences in the discrimination of line orientation
Neuropayehologia, 1974, Vol. 12, pp. 165 to 174. Pergamon Press. Printed in England.
H E M I S P H E R I C D I F F E R E N C E S IN T H E D I S C R I M I N A T I O N OF L I N E O R I E N T A T I O N * C. UMILT.~, G. RIZZOLATTI, C. A. MAR.ZI, G. ZAMBONI, C. FRANZINI, R. CAMARDA a n d G. BERLUCCHI Istituto di Psicologia dell'Universit/i di Bologna; Istituto di Fisiologia Umana dell'Universit~t di Parma; Istituto di Fisiologia e Laboratorio di Neurofisiologia del CNR, Pisa, Italy
(Received 21 September 1973) Abstract--Normal, right-handed subjects trained to discriminate between rectangles oriented with their major axis along the vertical, the horizontal and the two intermediate directions, and presented to the right or left side of a fixation point, exhibited faster discriminative reactions (pressing of a key) to stimuli appearing in the right visual field. By contrast, two other groups of normal, right-handed subjects performing a similar reaction-time task with stimuli oriented along other directions (respectively, 30° and 45 ° from the vertical to the right and the left; 15°, 30°, 45° and 60° from the vertical) were faster in discriminating stimuli presented in the left visual field. These differences in performance for the two halves of the visual field are attributed to hemispheric differences in the discrimination of line orientation. The opposite hemispheric superiorities found with the different discriminations are in turn attributed to the use of verbal mediators in the discrimination preferred by the left hemisphere, and by the use of a non-verbal strategy in the discriminations preferred by the right hemisphere.
1. INTRODUCTION PERCEPTUAL asymmetries between the right a n d left ears, or the right a n d left visual fields o f n o r m a l h u m a n s can, in m o s t cases, be r e a s o n a b l y a t t r i b u t e d to functional differences between the cerebral hemispheres (see review in [1]). A c c o r d i n g to a b r o a d l y accepted, t h o u g h oversimplified, i n t e r p r e t a t i o n o f the differential roles o f the cerebral hemispheres in perception, sensory material t h a t can be easily e n c o d e d in words is analyzed p r i m a r i l y by the left hemisphere, while " n o n - v e r b a l " signals with complex a n d ill-defined t e m p o r a l o r spatial organizations are analyzed p r i m a r i l y by the right hemisphere. Recently, m o r e analytical questions have been raised a b o u t these perceptual differences between the hemispheres. A r e they due to the fact t h a t the two hemispheres are e n d o w e d with different capacities for extracting specific cues f r o m sensory signals, or to a m o r e f u n d a m e n t a l distinction between the hemispheres in terms o f mechanisms for discrimination, perception, m e m o r y a n d t h o u g h t ? W h a t are the relations between various unspecific aspects o f p e r c e p t u a l a n d discriminative tasks, such as item difficulty, familiarity, confusability a n d the like, a n d the factor o f cerebral d o m i n a n c e ? These are h a r d questions, a n d one can scarcely h o p e to provide definite answers to them, n o w o r in the near future. However, some meaningful i n f o r m a t i o n has a l r e a d y been p r o v i d e d b y experiments on n o r m a l man. Thus, for example, STUDDERT-KENNEDY a n d SHANKWEILER [2] a n d DARWIN [3] have shown t h a t the left hemisphere is superior to the right in extracting linguistic * The results reported here have been preliminarily communicated at the Third Intensive Study Program of the Neuroscience Research Program, Boulder, Colorado (see 29) and at the 1972 Annual Meeting of the European Brain and Behaviour Society (see 30). 165
166 C. UMILT.~,G. RIZZOLATTI,C. A. MARZI,G. ZAMBONI,C. FRANZINI,R. CAMARDAand G. BERLUCCHI f e a t u r e s f r o m a c o u s t i c signals; similarly, UM1LTA et al. [4] h a v e c o n c l u d e d t h a t the s u p e r i o r i t y o f t h e left h e m i s p h e r e in the d i s c r i m i n a t i o n o f visually p r e s e n t e d letter displays can be a s c r i b e d to the f a c t t h a t t h e d i s c r i m i n a t i o n is e v e n t u a l l y p e r f o r m e d o n the a c o u s t i c t r a n f o r m s o f the visual stimuli. S i m i l a r analyses are still l a c k i n g for stimuli " p r e f e r r e d " by the r i g h t h e m i s p h e r e , p r o b a b l y b e c a u s e s u c h stimuli are u s u a l l y h i g h l y c o m p l e x . It w o u l d be h a r d , f o r e x a m p l e , to find o u t t h e specific f e a t u r e s by v i r t u e o f w h i c h p h o t o g r a p h s o f h u m a n faces are b e t t e r d i s c r i m i n a t e d by the r i g h t h e m i s p h e r e t h a n by t h e left [see 5, 6]. A s to the i n f l u e n c e o f s t i m u l u s f a m i l i a r i t y a n d difficulty, KIMURA [7] a n d STUDDERT-KENNEDY a n d SHANKWEILER [2] h a v e s h o w n t h a t these f a c t o r s are n o t crucial in d e t e r m i n i n g a s y m m e t r i e s b e t w e e n t h e ears in d i c h o t i c tests, b u t n o i n f o r m a t i o n o f this k i n d is a v a i l a b l e f o r visual tasks. F i n a l l y , a specific m o d e o f p e r c e p t i o n - - c a t e g o r i c a l vs c o n t i n u o u s - - h a s b e e n sugg e s t e d to be t y p i c a l o f the speech m e c h a n i s m s in the left h e m i s p h e r e [see 2, 8, 9]. I n t h e p r e s e n t e x p e r i m e n t , we h a v e c o n c e r n e d o u r s e l v e s w i t h s o m e o f these q u e s t i o n s . C l i n i c a l d a t a [see 10, 11] h a v e i n d i c a t e d t h a t p e r f o r m a n c e o n a t a s k i n v o l v i n g t h e disc r i m i n a t i o n o r t h e j u d g m e n t o f line o r i e n t a t i o n is i m p a i r e d after r i g h t h e m i s p h e r e lesions b u t n o t a f t e r left. I n a t t e m p t i n g to e x t e n d these findings to n o r m a l m a n b y u t i l i z i n g a r e a c t i o n t i m e ( R T ) p a r a d i g m [see 5], we h a v e f o u n d t h a t h e m i s p h e r i c d o m i n a n c e c a n v a r y a n d i n d e e d reverse itself, w i t h i n the s a m e task, d e p e n d i n g o n d i s c r i m i n a t i o n p r o c e s s e s w h i c h we will try to specify in t h e D i s c u s s i o n . 2. M E T H O D The experimental design and procedure were similar to those of a previous study on hemispheric differences in RT [see 5]. In brief, the general plan of the experiment was as follows. Monocularly-occluded subjects were seated inside a sound-proof room and positioned in a head and chin rest so as to face a translucent hemispheric screen 1 meter in diameter, located at a distance of 50 cm from them. An acoustic signal prompted the subjects to fixate on a clearly marked central point of the screen. Two to 3 sec following the warning signal, a 5.5 x 1 cm luminous rectangle oriented in one of four possible directions was backprojected for 100 msec on to the screen, either to the right or to the left of the fixation point, and on a level with it. The distance between this point and the nearest point of the rectangle was approximately 5 degrees of visual angle. The subject was asked to discriminate between the different orientations of the rectangle by pressing a key as fast as possible following the appearance of the rectangle in two previously specified orientations, and by refraining from pressing the key following the appearance of the rectangle in the other two orientations. Pressing of the key stopped an electronic millisecond counter that was started at the beginning of the 100 msec exposure period, thus providing a RT measure to the nearest millisecond. Forty-two right-handed male students of the University of Bologna took part in the experiment. They were divided into three groups (12, 18 and 12 subjects) to which different ranges of stimulus orientations were presented. For the subjects in Experiment 1 the four possible orientations were vertical (V), horizontal (H), right oblique (RO) and left oblique (LO), the latter two orientations resulting from a 45 ° clockwise and counter-clockwise rotation of the rectangle in the upright position. The positive stimuli were RO and H for 6 subjects, and LO and V for the other 6 subjects. For the subjects in Experiment 2, the four possible orientations were 30 ° and 45 ° from the vertical to the right (30°R and 45°R) and 30 ° and 45 ° from the vertical to the left (30°L and 45°L), the positive stimuli being 30 ° R and 45°L for 9 subjects, and 30°L and 45°R for the other 9 subjects. For the subjects in Experiment 3, the four possiblc orientations were 15 °, 30 °, 45 ° and 60 ° from the vertical position; for symmetry, the rotations were clockwise for stimuli presented to the left of the fixation point, and counterclockwise for stimuli presented to the right of the fixation point. The positive stimuli were 15° and 45 ° for 6 subjects, and 30 ° and 60 ° for the other 6 subjects. An illustration of the three stimulus conditions is given in Fig. 1. Within any one group, half of the subjects were tested using the right eye and half using the left eye, and in each group the eye assignment was counterbalanced against the assignment to one of the two selected arrangements of positive and negative stimuli. Formal tests began after an informal practice session during which the subjects were acquainted with the experimental situation and learned to fixate the central point of the screen and to press the key in response to the positive stimuli. Each subject was tested during four sessions which were run on separate days. Each session consisted of 20 practice trials and 120 regular trials, divided into 4 blocks of 5 initial practice trials and 30 regular trials. Within each session, the stimulus appeared to the right of the fixation point on half of the trials and to the left on the other half; likewise the right hand was used for responding on half of the
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
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trials, and the left hand was used on the other half. The four intrasession blocks corresponded to the four possible combinations between side of stimulus and responding hand; their sequence was balanced over sessions within any one group according to a Latin square design. The alternation between the stimuli within each block was subject to the constraints that the same stimulus was never shown more than twice in a row and that a succession of more than 3 positive or 3 negative stimuli could not occur. Otherwise the sequence of stimulus presentations was random. For the analysis of the data, the median of the RTs to each one of the two positive stimuli was computed within each block of trials. The means of the medians thus obtained were then averaged across sessions, so that eventually each subject contributed four scores, corresponding to the hand-field combinations. Further, the separate averaging of the two intrablock medians across blocks within each session, and the separate averaging across sessions of the two means thus obtained led to an overall measure of RT to each positive stimulus for each subject. Within any one group, the analysis of errors was limited to their distribution in relation to the field of stimulation, without distinguishing between errors of omission and commission. RESULTS T a b l e 1 s h o w s t h a t b o t h s p e e d a n d a c c u r a c y o f the r e s p o n s e s d e c r e a s e d c o n s i d e r a b l y f r o m E x p e r i m e n t 1 t o E x p e r i m e n t 2 a n d f r o m E x p e r i m e n t 2 t o E x p e r i m e n t 3. T h e differe n c e s w e r e h i g h l y significant, as i n d i c a t e d b y t w o tailed t-tests f o r u n c o r r e l a t e d s c o r e s carried o u t o n i n d i v i d u a l m e a n R T s ( E x p . 1 vs E x p . 2: t = 3'842, df = 28, F < 0"001; E x p . 2 vs E x p . 3: t = 5"563, d f = 28, P < 0"001) a n d o n i n d i v i d u a l s c o r e s ( E x p . 1 vs E x p . 2: t = 5 ' 3 4 5 ; d f = 28, P < 0'001 ; E x p . 2 vs E x p . 3: t ---- 2"428, d r = 28, P < 0"02). Table 1. Mean reaction times (msec) and mean number of errors for the three experimental conditions Number of subjects
Reaction time (msec) Mean SD 427.2 30.3
Experiment 1
12
Experiment 2
18
598.8
125.5
Experiment 3
12
774.1
120.3
T h e results o f e a c h e x p e r i m e n t will n o w b e d e s c r i b e d s e p a r a t e l y .
Errors Mean SD 8.8 4.0 (1.6 %) 19.4 14"8 (3"5 %) 60.8 27.5 (10.9 70)
168 C. UMILTA,G. RIZZOLATTi,C. A. MARZI, G. ZAMBONI,C. FRANZINI, R. CAMARDAand G. BERLUCCHI
Experiment 1 Table 2 gives overall mean RTs in relation to side of stimulation, responding hand and the interaction between these two factors. Overall mean R T was 421 msec for stimuli presented in the right visual field and 433 msec for stimuli presented in the left field. Eleven subjects out of 12 showed a superiority of the right visual field over the left for RT. Overall mean R T was slightly shorter for the left hand than for the right. The right hand was on the average faster in 6 subjects, while the left hand prevailed in the other 6 subjects. There was no apparent relation either between prevailing hand and eye used during testing or between prevailing hand and arrangement o f positive and negative stimuli. Within each visual field, overall mean R T was slightly faster with the ipsilateral hand than with the contralateral hand. Table 2. Experiment 1--Overall mean reaction times (msec)
Left hand Right hand Mean
Side of stimulus Left Right 428 423 438 419 433 421
Mean 425.5 428.5
A n analysis o f variance for a two-factor repeated measurements design, field x h a n d x subjects, with subjects assumed as having r a n d o m effects (see 12, p. 170), was carried out on individual mean RTs. According to this analysis, field was a highly reliable source of R T variance ( F z 9"13; d J ' ~ 1, 11; P < 0 0 2 5 ) ; neither hand nor the field by h a n d interaction yielded significant F values. There were very few errors of omission or commission (see Table 1) and a two-tailed t-test for correlated scores indicated that there was no significant difference in number of errors between left and right visual fields (P > 0"2). Within each one o f the two subgroups responding to different pairs of positive stimuli ( R O and H ; L O and V), no clear relations between R T and type of stimulus were apparent. Overall mean RTs are given in Table 3. In both subgroups there was no significant difference between RTs to the two positive stimuli (P > 0'2 by a two-tailed t-test for correlated scores). Table 3. Experiment 1--Overall mean reaction times (msec) in the two subgroups responding to different pairs of positive stimuli Stimulus RO H L O V
Mean RT 417 423 438 429
Conclusion. The only reliable effect was that of visual field on speed of response, the right visual field stimulation yielding faster responses than the left. Experiment 2 Table 4 gives overall mean RTs in relation to side of stimulation, responding hand and the interaction between these two factors. A n analysis of variance similar to that performed on the results of Experiment 1 showed that neither field, nor hand, nor the interaction between field and hand had any significant effect on RT. Similarly, errors were uniformly distributed in relation to right and left fields (P > 0"2 by a two-tailed t-test for correlated scores).
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
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Table 4. Experiment 2--Overall mean reaction times (msec)
Left hand Right hand Mean
Side of stimulus Left Right 592 605 596 601 594 603
Mean 598'5 598.5
Table 5 shows overall m e a n R T s for the two subgroups r e s p o n d i n g to different pairs of positive stimuli, in relation to the two stimuli. Six o f the 9 subjects r e s p o n d i n g to 30 ° L a n d 45 ° R h a d faster R T scores for the first stimulus t h a n for the second, with an overall significant difference between R T s to the two stimuli (t - - 2"613; d f = 35; P < 0"02). Similarly, 7 o f the 9 subjects r e s p o n d i n g to 30 ° R a n d 45 ° L h a d faster R T scores for the first stimulus t h a n for the second, the overall difference between the RTs to the two stimuli falling just short o f significance (t = 1"889; dr= 35; P < 0'1). Table 5. Experiment 2--Overall mean reaction times (msec) in the two subgroups responding to different pairs of positive stimuli Stimulus 30° L 45 ° R 30°R 45 ° L
Mean RT 599 646 559 590
Conclusion. W i t h a t a s k m o r e d e m a n d i n g t h a n in E x p e r i m e n t 1, the superiority o f the right visual field for R T was no longer apparent. On the contrary, there was a tendency t o w a r d a left field advantage, a l t h o u g h the interfield difference was n o t significant. RTs to the two orientations less inclined f r o m the vertical were clearly faster t h a n RTs to the other two orientations. Experiment 3 T a b l e 6 gives overall m e a n RTs in relation to side o f stimulation, r e s p o n d i n g h a n d and the interaction between these two factors. Ten subjects o u t o f 12 h a d faster R T scores for the left visual field; 8 subjects were faster with the right hand, 4 with the left hand. A n analysis o f variance similar to t h a t used in Experiments 1 a n d 2 indicated t h a t only field h a d a significant effect on R T ( F = 1l'47; df = 1, 11; P < 0"01). N o significant relation was f o u n d between n u m b e r o f errors and field o f stimulation (P > 0'2). Table 6. Experiment 3--Overall mean reaction times (msec)
Le~ hand Right hand Mean
Side of stimulus Le~ Right 750 800 740 805 745 802-5
Mean 775 772"5
T a b l e 7 gives overall m e a n R T s for the two s u b g r o u p s r e s p o n d i n g to different pairs o f positive stimuli, in relation to the two stimuli. Five o f the 6 subjects r e s p o n d i n g to 15° a n d 45 ° showed faster scores for the first stimulus than for the second; the overall difference between the RTs to the two stimuli was highly significant (t = 3"864; dr= 23; P < 001). Five o f the 6 subjects r e s p o n d i n g to 30 ° and 60 ° showed faster scores for the second stimulus
170 C. UMILT)~,G. RIZZOLATTI, C. A. MARZI, G. ZAMBON[,C. FRANZINI, R. CAMARDAand G. BERLUCCHI
than for the first; also in this case, the overall difference between the RTs to the two stimuli was significant (t = 3"665; df= 23; P < 0'01). Table 7. Experiment 3--Overall mean reaction times (msec) in the two subgroups responding to different pairs of positive stimuli Stimulus 15° 45° 30° 60°
Mean RT 676 811 855 754
Conclusion. There was a significant interfield difference, the dominant field being opposite to that favored in Experiment 1. Faster RTs were obtained from the left visual field than from the right. The two extreme orientations within the range of four presented yielded significantly faster RTs. 4. D I S C U S S I O N Theoretically, the speed of discriminative responses may vary as a function of (a) the amount of information conveyed by the signals, and (b) the "difficulty" of the discrimination. In our three experiments, the number of stimuli was constant, and the probability of occurrence of each particular stimulus was the same. Thus the information content of the signals did not vary over the three tasks. The differences in RT found between tasks must therefore have resulted from differences in discrimination difficulty. The difficulty of a discrimination is a poorly defined entity, which may be considered to be inversely related to two separate factors: stimulus discriminability and stimulus codability. Stimulus discriminability is usually expressed as a function of the number of features on the basis of which the stimuli can be differentiated from one another, and of the degree to which the stimuli differ from one another with respect to each of the distinguishing features. Mathematical formulae for the measurement of discriminability as a determinant of speed of decisions have been proposed [see e.g. 13, 14] but their general applicability is still debated [see 15]. In the present context, stimulus codability may be loosely defined as the ease and economy with which stimuli can be described by words [see e.g. 16]. The stimuli used in our three experiments could be distinguished from one another on the basis of one and the same feature: their orientation. It was the degree to which the stimuli differed from one another with respect to this feature that was different in the three experiments. The angles formed by each of the positive stimuli with the two negative stimuli were 45 ° and 90 ° in Experiment 1, 15° and 60 ° in Experiment 2, 15° and 45 ° in Experiment 3. As for stimulus codability, a word suffices to identify each of the stimuli in Experiment 1: horizontal and vertical for H and O; right for RO, left for LO. It is interesting that these highly codable orientations usually serve as standards of comparison for the judgment of line orientation, the vertical and horizontal providing the primary anchors, and the two intermediate orientations providing the secondary anchors within the orientation continuum [see 17]. Further, it is known from several psychophysical studies that the human visual system is better tuned for the vertical and horizontal orientations than for the oblique orientations [see review in 18]. Unlike the stimuli of Experiment 1, the description of the stimuli in Experiments 2 and 3 (as opposed to their pictorial representation) is neither easy nor economical. The suggestion can perhaps be made that the distinction ~-~_tween right and
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
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left might be used to split up the task in Experiment 2 into two separate discriminations. With all these considerations in mind, we expected absolute RT to be shortest in Experiment l, intermediate in Experiment 2 and longest in Experiment 3. This expectation is clearly supported by the findings. In addition, the findings show a right-field superiority for RT in the "easy" task, an opposite left-field superiority for RT in the "difficult" task, and no clear-cut interfield differences in the task of intermediate difficulty. The most parsimonious interpretation of asymmetries in discriminative RT between left and right visual fields, such as those observed in the present study, assumes that they are due to (1) a qualitative differentiation between perceptual mechanisms in the two hemispheres, and (2) a more direct, and perhaps more efficient communication between each visual field and the contralateral cerebral hemisphere [see e.g. 5]. Accordingly, it is assumed that the left hemisphere prevailed in the performance of the task of Experiment 1 while the right hemisphere prevailed in the performance of the task of Experiment 3; only a tendency toward a right-hemisphere predominance was apparent for the task of Experiment 2. This would imply that discrimination of line orientation is performed by the left hemisphere when the task is an "easy" one, and by the right hemisphere when the task is a "difficult" one. How is this to be reconciled with current views about the hemispheric lateralization of verbal abilities to the left side, and of perception of spatial relations and nonverbal visual patterns to the right side? The discrimination of line orientation typically qualifies as a spatial task; hence one would expect it to belong fully to the domain of specializations of the right hemisphere, regardless of whether the discrimination is easy or difficult. The consideration of some findings related to ours may help the discussion of this issue. WHITE [19] has tested the ability of normal subjects to report the orientation of a thin line flashed for 20-25 msec at 3 degrees to the right or to the left of the fixation point. Four orientations were used, corresponding exactly to the ones employed in our Experiment 1. A response code allocated a different number to each particular orientation, and subjects responded by calling out the number corresponding to the perceived orientation. Accuracy of recognition was significantly better in the right field than in the left, and this right field superiority correlated positively with the superiority of the same field shown by the same subjects on a similar task involving the verbal identification of single letters. From this finding WHITE [19] has inferred that the right field superiority for the recognition of line orientations depends on the existence of a selective contour-tuning apparatus in the left hemisphere, and that this same apparatus, rather than the left-hemisphere speech mechanisms, may be responsible for the right-field superiority in the perception of single letters. This interpretation has been questioned by GEFFNERet al. [20], who suggest that the use of a vocal response in White's experiment on discrimination of line orientation may have introduced a bias in favor of the left hemisphere, thereby masking a possible right hemisphere superiority for this spatial task. Yet, their account of White's results is made unlikely by the similarity between his results and those of our Experiment 1, in which we used a motor rather than vocal response. On the other hand, White's explanation of his own findings is made unlikely by the results of our Experiments 2 and 3, since his postulated contour-tuning apparatus should have caused a superiority of the right visual field in these experimental conditions as well. The superiority of the right visual field, and presumably of the left hemisphere, seen in our Experiment 1 as well as in the comparable experiment by WHITE [19], can be due to the high discriminability of the stimuli, or to their codability, or to both. Although we have no evidence to reject completely the discriminability factor, the present state of knowledge
172 C. UMILT,~,G. RIZZOLATTI,C. A. MARZ1,G. ZAMBONI,R. FRANZINI,R. CAMARDAand G. BERLUCCHI about functional asymmetries between the hemispheres suggests that it was codability which was instrumental in favoring the left hemisphere under these experimental conditions. Discriminative responses to these highly codable orientations were most probably facilitated by a verbal mediator: hence the superiority of the left hemisphere. On the other hand, it is clear that a verbal mediation does not offer itself as the best strategy for performing the discrimination tasks of Experiments 2 and 3. Here, identification of the stimuli by a purely "visual" process of matching would appear much more economical than their recognition through the matching of each visually presented item with its verbal (acoustic) label. We suggest that it was the adoption of a visual matching strategy that shifted the hemispheric dominance toward the right side in Experiments 2 and 3. Recent studies in normal man have documented the superior ability of the right hemisphere in perceiving spatial relations in the visual modality. The results of Experiments 2 and 3 and their present interpretation are in accord with these studies [21, 22, 23]. If our explanation of the results is correct, then it follows that discrimination of line orientation in man is a much more complex affair than is assumed by current neurophysiological theories based on the neuronal line detectors discovered by HUBEL and WIESEL [24, 25, 26] in the visual cortex of cats and monkeys. While it seems most reasonable that these detectors must constitute a preliminary stage in the discrimination process, the foregoing discussion suggests that the discriminative decision ultimately depends on higher order processes lateralized to one hemisphere. Whether it is the left hemisphere or the right that directs the response appears to be determined by the role played by verbal mediation. The suggestion that discrimination of line orientation may involve a verbal process is implicit in the theory proposed by ATTNEAVEand REID [27], who argue that perceived orientation depends upon its naming or description within a labile subjective frame of reference whose main axes normally coincide with the physical horizontal and vertical co-ordinates, but which can revolve about this position by spontaneous decision or instruction. However, a pictorial representation of stimulus orientations within the selected frame of reference would seem more appropriate for efficient discriminative responses when verbal categorization of the stimuli with respect to the main axes is equivocal or uneconomical. Such is certainly the case for the stimuli used in Experiment 2 and especially those in Experiment 3. The preference for the stimuli which were closest to the vertical in Experiment 2, and for the stimuli which were closest to the vertical and the horizontal in Experiment 3 would suggest that they were used as "derived" anchors [see 17] within the normal frame of reference. No clear preference for a particular stimulus was found in Experiment 1, although faster responses were expected for the vertical and horizontal orientations, in view of both the psychophysical findings quoted on page 170 and the above mentioned study of ATTNEAVE and REID [27]. These authors found that the perceived vertical and horizontal orientations evoked faster responses than the other two orientations. On the other hand WHITE [19] has reported that accuracy of responses to the same four orientations did not vary significantly as a function of the stimulus while DICK and DICK [28] found a superiority of the two diagonals over the vertical and horizontal orientations for accuracy of response. It must be pointed out that the experiments by DIcK and DICK [28] and WHITE [19] and our own Experiment 1 differed from the experiment by ATTNEAVE and REID [27] in that presentation of the stimuli was in the center of the visual field in the latter experiment, and lateralized to the left or right visual fields in the former three experiments. Whether the discrepancy in the results is due to this or to other procedural differences must be settled by future experiments.
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
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REFERENCES 1. MILNER, B. Interhemispheric differences in the localization of psychological processes in man. BE. meal. Bull. 27, 272-277, 1971. 2. STUODERT-KENNEDY,M. and SHANKWEmER,D. Hemispheric specialization for speech perception. J. acoust. Soc. Am. 48, 579-594, 1970. 3. DARWIN, C. J. Ear differences in the recall of fricatives and vowels. Q. J. exp. Psychol. 23, 46-62, 1971 4. UMILT~, C., FROST, N. and HYMAN,R. Interhemispheric effects on choice reaction times to one-two-, and three-letter displays. J. exp. Psychol. 93, 198-204, 1972. 5. RIZZOLATTL G., Ur~rT~k, C. and BERLUCCHI,G. Opposite superiorities of the right and left cerebral hemispheres in discriminative reaction time to physiognomical and alphabetical material. Brain 94, 431-442, 1971. 6. GEFFEN, G., B~a~sHAw, J. L. and WALLACE,G. Interhemispheric effects on reaction time to verbal and nonverbal visual stimuli. J. exp. Psychol. 87, 415-422, 1971. 7. K a y , D. Functional asymmetry of the brain in dichotic listening. Cortex. 3, 163-178, 1967. 8. LIBERMAN,A. M. Some characteristics of perception in the speech mode. Res. Publ. Ass. Herr. ment. Dis. 48, 238-254, 1970. 9. SrUDDERT-KENNrDY,M., LIBERMAN,A. M., HARRIS, K. S. and COOPER, F. S. Motor theory of speech perception: a reply to Lane's critical review. Psychol. Rev. 77, 234-269, 1970. 10. W ~ a ~ O r O N , E. K. and RABn~, P. Perceptual matching in patients with cerebral lesions. Neuropsychologic 8, 475-487, 1970. 11. DE RENZI, E., FAGLIONI, P. and ScoTrI, G. Judgements of spatial orientation in patients with focal brain damage. J. Neurol. Neurosurg. Psychiat. 34, 489-495, 1971. 12. MYERS, J. L. Fundamentals of Experimental Design. Allyn & Bacon, Boston, 1966. 13. CROSSraAN, E. R. F. W. The measurement of discriminability. Q. J. exp. Psychol. 7, 176-195, 1955. 14. LAMINC, D. R. J. Information Theory of Choice-Reaction Times. Academic Press, New York, 1968. 15. BROADBENT,D. E. Decision and Stress. Academic Press, New York, 1971. 16. COHEN, G. The effect of codability of the stimulus on recognition reaction time. BE. J. Psychol. 60, 25-29, 1969. 17. KEENE, G. C. The effect of response codes on the accuracy of making absolute judgments of lineal inclinations. J. gen. Psychol. 69, 37-50, 1963. 18. APPELLE, S. Perception and discrimination as a function of stimulus orientation: "The oblique effect" in man and animals. Psychol. Bull. 78, 266-278, 1972. 19. W.rrE, M. J. Visual hemifield differences in the perception of letter and contour orientation. Can. J. Psychol. 25, 207-212, 1971. 20. GEFFEN, G., B~DSnAW, J. L. and NETTLETON, N. C. Hemispheric asymmetry: verbal and spatial encoding of visual stimuli. J. exp. Psychol. 95, 25-31, 1972. 21. K~MX~A, D. Dual functional asymmetry of the brain in visual perception. Neuropsychologia 4, 275-285, 1966. 22. K a M ~ , D. Spatial localization in left and right visual field. Can. J. Psychol. 23, 455-458, 1969. 23. DtrRNFORD, M. and KI~URA, D. Right hemisphere specialization for depth perception reflected in visual field differences. Nature, Lond. 231, 394-395, 1971. 24. HtraEL, D. H. and WrESEL,T. N. Receptive fields of single neurones in the cat's striate cortex. J. Physiol., Lond. 148, 574-591, 1959. 25. Ht~EL, D. H. and WIESEL, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229-289, 1965. 26. HUBEL,D. H. and WrESEL, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol., Lond. 195, 215-243, 1968. 27. ArTNEAW, F. and REID, K. W. Voluntary control of frame of reference and slope equivalence under head rotation. J. exp. Psychol. 78, 153-159, 1968. 28. DICK, A. O. and DICK, S. O. An analysis of hierarchical processing in visual perception. Can. J. Psychol. 23, 203-211, 1969. 29. BERLUCCnX, G. Cerebral dominance and interhemispheric communication in normal man. In The Neurosciences: A Third Study Program. The M.I.T. Press, Cambridge, Mass., 1973 (in press). 30. Ur~LT~,, C., l~zzoLAr'n, G., MARZI, C. A., ZAMBO~, G., FRANZlNI,C., CAMARDA,R. and BERLUCCHI,G. Hemispheric differences in normal human subjects: further evidence from study of reaction time to lateralized visual stimuli. Brain Res. 49, 499-500, 1973.
R~um~----Des sujets normaux droitiers 6taient entralnrs ~, discriminer entre des rectangles orientrs avec leur axe majeur vertical, horizontal et selon les deux directions intermrdiaires. Ces stimulus ont 6t6 prrsentrs ~ droite et h gauche du point de fixation. Les sujets ont montr6
174 C. UMILT/~, G. R1ZZOLATTI, C. A. MARZI, G. ZAMBONI,C. FRANZINI, R. CAMARDAand G. BERLUCCHI des r6actions discriminatives (soit la d6pression d'un levier) plus rapides aux stimulus apparaissant dans le champ visuel droit. D'autre part, deux autres groupes de sujets normaux droitiers ex6cutant une t~,che de temps de r6action semblable 5, la premi6re mais avec des stimulus orient6s dans d'autres directions (respectivement 30 ° et 45 ° h droite et ~t gauche de l'axe vertical; 15 °, 30 °, 45 ° et 60 ° du plan vertical), ont montr6 des reactions discriminatives plus rapides aux stimulus pr6sent6s dans le champ visuel gauche. Les diff~,rences de performance entre les deux moiti6s du champ visuel sont attribu6es ~t des diff6rences h6misph6riques dans la discrimination de l'orientation des lignes. Le fait que les h6misph6res soient superieurs r u n par rapport ~, rautre selon le type de la discrimination est, b, son tour, attribu6 ~, l'utilisation des m6diateurs verbaux dans le cas des discriminations pr6fer6es par l'h6misph6re gauche, et ~t l'usage d'une strat6gie non verbale dans le cas des discriminations pr6f6r6es par l'h6misph6re droit. Zusammenfassung--Normale, rechtshfindige Versuchspersonen, welche gelernt hatten, Rechtecke zu unterscheiden, welche mit ihrer langen Seite vertikal, horizontal oder in den beiden Zwischenrichtungen orientiert waren und welche entweder rechts oder links yore Fixationspunkt dargeboten wurden, konnten diese Aufgabe schneller 18sen (das heisst einen Knopf dr/icken), wenn die Testreize in der rechten H~ilfte des Gesichtsfeldes dargeboten wurden. Zwei andere Gruppen von normalen und rechtsh~indigen Versuchspersonen hatten eine/ihnliche Aufgabe mit Messung der Reaktionszeit bei Testzeichen zu 18sen, die in andere Richtungen orientiert waren (je nachdem 30 ° und 45 ° yon der vertikalen nach links und rechts abweichend; oder 15 °, 30 °, 45 ° und 60 ° yon der vertikalen abweichend), l m Gegensatz zu der ersten Gruppe waren jene nun schneiler wenn die Reize in der linken H/ilfte des Gesichtsfeldes dargeboten wurden. Diese Unterschiede in der Leistungsfahigkeit zwischen den beiden Gesichtsfeldh/ilften werden mit hemispharischen Verschiedenheiten in der Unterschiedsempfindlichkeit for Linienorientierungen in Verbindung gebracht. Die unterschiedlichen hemisph~rischen Leistungsf/ihigkeiten, die bei den verschiedenen Aufgaben ermittelt wurden, werden der Bevorzugung einer verbalen Strategie durch die linke Hemisph~ire zugeschrieben, w~ihrend angenommen wird, dass in der rechten Hemisphare zur Unterscheidung eine nicht verbale Strategie zur Anwendung kommt.
H E M I S P H E R I C D I F F E R E N C E S IN T H E D I S C R I M I N A T I O N OF L I N E O R I E N T A T I O N * C. UMILT.~, G. RIZZOLATTI, C. A. MAR.ZI, G. ZAMBONI, C. FRANZINI, R. CAMARDA a n d G. BERLUCCHI Istituto di Psicologia dell'Universit/i di Bologna; Istituto di Fisiologia Umana dell'Universit~t di Parma; Istituto di Fisiologia e Laboratorio di Neurofisiologia del CNR, Pisa, Italy
(Received 21 September 1973) Abstract--Normal, right-handed subjects trained to discriminate between rectangles oriented with their major axis along the vertical, the horizontal and the two intermediate directions, and presented to the right or left side of a fixation point, exhibited faster discriminative reactions (pressing of a key) to stimuli appearing in the right visual field. By contrast, two other groups of normal, right-handed subjects performing a similar reaction-time task with stimuli oriented along other directions (respectively, 30° and 45 ° from the vertical to the right and the left; 15°, 30°, 45° and 60° from the vertical) were faster in discriminating stimuli presented in the left visual field. These differences in performance for the two halves of the visual field are attributed to hemispheric differences in the discrimination of line orientation. The opposite hemispheric superiorities found with the different discriminations are in turn attributed to the use of verbal mediators in the discrimination preferred by the left hemisphere, and by the use of a non-verbal strategy in the discriminations preferred by the right hemisphere.
1. INTRODUCTION PERCEPTUAL asymmetries between the right a n d left ears, or the right a n d left visual fields o f n o r m a l h u m a n s can, in m o s t cases, be r e a s o n a b l y a t t r i b u t e d to functional differences between the cerebral hemispheres (see review in [1]). A c c o r d i n g to a b r o a d l y accepted, t h o u g h oversimplified, i n t e r p r e t a t i o n o f the differential roles o f the cerebral hemispheres in perception, sensory material t h a t can be easily e n c o d e d in words is analyzed p r i m a r i l y by the left hemisphere, while " n o n - v e r b a l " signals with complex a n d ill-defined t e m p o r a l o r spatial organizations are analyzed p r i m a r i l y by the right hemisphere. Recently, m o r e analytical questions have been raised a b o u t these perceptual differences between the hemispheres. A r e they due to the fact t h a t the two hemispheres are e n d o w e d with different capacities for extracting specific cues f r o m sensory signals, or to a m o r e f u n d a m e n t a l distinction between the hemispheres in terms o f mechanisms for discrimination, perception, m e m o r y a n d t h o u g h t ? W h a t are the relations between various unspecific aspects o f p e r c e p t u a l a n d discriminative tasks, such as item difficulty, familiarity, confusability a n d the like, a n d the factor o f cerebral d o m i n a n c e ? These are h a r d questions, a n d one can scarcely h o p e to provide definite answers to them, n o w o r in the near future. However, some meaningful i n f o r m a t i o n has a l r e a d y been p r o v i d e d b y experiments on n o r m a l man. Thus, for example, STUDDERT-KENNEDY a n d SHANKWEILER [2] a n d DARWIN [3] have shown t h a t the left hemisphere is superior to the right in extracting linguistic * The results reported here have been preliminarily communicated at the Third Intensive Study Program of the Neuroscience Research Program, Boulder, Colorado (see 29) and at the 1972 Annual Meeting of the European Brain and Behaviour Society (see 30). 165
166 C. UMILT.~,G. RIZZOLATTI,C. A. MARZI,G. ZAMBONI,C. FRANZINI,R. CAMARDAand G. BERLUCCHI f e a t u r e s f r o m a c o u s t i c signals; similarly, UM1LTA et al. [4] h a v e c o n c l u d e d t h a t the s u p e r i o r i t y o f t h e left h e m i s p h e r e in the d i s c r i m i n a t i o n o f visually p r e s e n t e d letter displays can be a s c r i b e d to the f a c t t h a t t h e d i s c r i m i n a t i o n is e v e n t u a l l y p e r f o r m e d o n the a c o u s t i c t r a n f o r m s o f the visual stimuli. S i m i l a r analyses are still l a c k i n g for stimuli " p r e f e r r e d " by the r i g h t h e m i s p h e r e , p r o b a b l y b e c a u s e s u c h stimuli are u s u a l l y h i g h l y c o m p l e x . It w o u l d be h a r d , f o r e x a m p l e , to find o u t t h e specific f e a t u r e s by v i r t u e o f w h i c h p h o t o g r a p h s o f h u m a n faces are b e t t e r d i s c r i m i n a t e d by the r i g h t h e m i s p h e r e t h a n by t h e left [see 5, 6]. A s to the i n f l u e n c e o f s t i m u l u s f a m i l i a r i t y a n d difficulty, KIMURA [7] a n d STUDDERT-KENNEDY a n d SHANKWEILER [2] h a v e s h o w n t h a t these f a c t o r s are n o t crucial in d e t e r m i n i n g a s y m m e t r i e s b e t w e e n t h e ears in d i c h o t i c tests, b u t n o i n f o r m a t i o n o f this k i n d is a v a i l a b l e f o r visual tasks. F i n a l l y , a specific m o d e o f p e r c e p t i o n - - c a t e g o r i c a l vs c o n t i n u o u s - - h a s b e e n sugg e s t e d to be t y p i c a l o f the speech m e c h a n i s m s in the left h e m i s p h e r e [see 2, 8, 9]. I n t h e p r e s e n t e x p e r i m e n t , we h a v e c o n c e r n e d o u r s e l v e s w i t h s o m e o f these q u e s t i o n s . C l i n i c a l d a t a [see 10, 11] h a v e i n d i c a t e d t h a t p e r f o r m a n c e o n a t a s k i n v o l v i n g t h e disc r i m i n a t i o n o r t h e j u d g m e n t o f line o r i e n t a t i o n is i m p a i r e d after r i g h t h e m i s p h e r e lesions b u t n o t a f t e r left. I n a t t e m p t i n g to e x t e n d these findings to n o r m a l m a n b y u t i l i z i n g a r e a c t i o n t i m e ( R T ) p a r a d i g m [see 5], we h a v e f o u n d t h a t h e m i s p h e r i c d o m i n a n c e c a n v a r y a n d i n d e e d reverse itself, w i t h i n the s a m e task, d e p e n d i n g o n d i s c r i m i n a t i o n p r o c e s s e s w h i c h we will try to specify in t h e D i s c u s s i o n . 2. M E T H O D The experimental design and procedure were similar to those of a previous study on hemispheric differences in RT [see 5]. In brief, the general plan of the experiment was as follows. Monocularly-occluded subjects were seated inside a sound-proof room and positioned in a head and chin rest so as to face a translucent hemispheric screen 1 meter in diameter, located at a distance of 50 cm from them. An acoustic signal prompted the subjects to fixate on a clearly marked central point of the screen. Two to 3 sec following the warning signal, a 5.5 x 1 cm luminous rectangle oriented in one of four possible directions was backprojected for 100 msec on to the screen, either to the right or to the left of the fixation point, and on a level with it. The distance between this point and the nearest point of the rectangle was approximately 5 degrees of visual angle. The subject was asked to discriminate between the different orientations of the rectangle by pressing a key as fast as possible following the appearance of the rectangle in two previously specified orientations, and by refraining from pressing the key following the appearance of the rectangle in the other two orientations. Pressing of the key stopped an electronic millisecond counter that was started at the beginning of the 100 msec exposure period, thus providing a RT measure to the nearest millisecond. Forty-two right-handed male students of the University of Bologna took part in the experiment. They were divided into three groups (12, 18 and 12 subjects) to which different ranges of stimulus orientations were presented. For the subjects in Experiment 1 the four possible orientations were vertical (V), horizontal (H), right oblique (RO) and left oblique (LO), the latter two orientations resulting from a 45 ° clockwise and counter-clockwise rotation of the rectangle in the upright position. The positive stimuli were RO and H for 6 subjects, and LO and V for the other 6 subjects. For the subjects in Experiment 2, the four possible orientations were 30 ° and 45 ° from the vertical to the right (30°R and 45°R) and 30 ° and 45 ° from the vertical to the left (30°L and 45°L), the positive stimuli being 30 ° R and 45°L for 9 subjects, and 30°L and 45°R for the other 9 subjects. For the subjects in Experiment 3, the four possiblc orientations were 15 °, 30 °, 45 ° and 60 ° from the vertical position; for symmetry, the rotations were clockwise for stimuli presented to the left of the fixation point, and counterclockwise for stimuli presented to the right of the fixation point. The positive stimuli were 15° and 45 ° for 6 subjects, and 30 ° and 60 ° for the other 6 subjects. An illustration of the three stimulus conditions is given in Fig. 1. Within any one group, half of the subjects were tested using the right eye and half using the left eye, and in each group the eye assignment was counterbalanced against the assignment to one of the two selected arrangements of positive and negative stimuli. Formal tests began after an informal practice session during which the subjects were acquainted with the experimental situation and learned to fixate the central point of the screen and to press the key in response to the positive stimuli. Each subject was tested during four sessions which were run on separate days. Each session consisted of 20 practice trials and 120 regular trials, divided into 4 blocks of 5 initial practice trials and 30 regular trials. Within each session, the stimulus appeared to the right of the fixation point on half of the trials and to the left on the other half; likewise the right hand was used for responding on half of the
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
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trials, and the left hand was used on the other half. The four intrasession blocks corresponded to the four possible combinations between side of stimulus and responding hand; their sequence was balanced over sessions within any one group according to a Latin square design. The alternation between the stimuli within each block was subject to the constraints that the same stimulus was never shown more than twice in a row and that a succession of more than 3 positive or 3 negative stimuli could not occur. Otherwise the sequence of stimulus presentations was random. For the analysis of the data, the median of the RTs to each one of the two positive stimuli was computed within each block of trials. The means of the medians thus obtained were then averaged across sessions, so that eventually each subject contributed four scores, corresponding to the hand-field combinations. Further, the separate averaging of the two intrablock medians across blocks within each session, and the separate averaging across sessions of the two means thus obtained led to an overall measure of RT to each positive stimulus for each subject. Within any one group, the analysis of errors was limited to their distribution in relation to the field of stimulation, without distinguishing between errors of omission and commission. RESULTS T a b l e 1 s h o w s t h a t b o t h s p e e d a n d a c c u r a c y o f the r e s p o n s e s d e c r e a s e d c o n s i d e r a b l y f r o m E x p e r i m e n t 1 t o E x p e r i m e n t 2 a n d f r o m E x p e r i m e n t 2 t o E x p e r i m e n t 3. T h e differe n c e s w e r e h i g h l y significant, as i n d i c a t e d b y t w o tailed t-tests f o r u n c o r r e l a t e d s c o r e s carried o u t o n i n d i v i d u a l m e a n R T s ( E x p . 1 vs E x p . 2: t = 3'842, df = 28, F < 0"001; E x p . 2 vs E x p . 3: t = 5"563, d f = 28, P < 0"001) a n d o n i n d i v i d u a l s c o r e s ( E x p . 1 vs E x p . 2: t = 5 ' 3 4 5 ; d f = 28, P < 0'001 ; E x p . 2 vs E x p . 3: t ---- 2"428, d r = 28, P < 0"02). Table 1. Mean reaction times (msec) and mean number of errors for the three experimental conditions Number of subjects
Reaction time (msec) Mean SD 427.2 30.3
Experiment 1
12
Experiment 2
18
598.8
125.5
Experiment 3
12
774.1
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Errors Mean SD 8.8 4.0 (1.6 %) 19.4 14"8 (3"5 %) 60.8 27.5 (10.9 70)
168 C. UMILTA,G. RIZZOLATTi,C. A. MARZI, G. ZAMBONI,C. FRANZINI, R. CAMARDAand G. BERLUCCHI
Experiment 1 Table 2 gives overall mean RTs in relation to side of stimulation, responding hand and the interaction between these two factors. Overall mean R T was 421 msec for stimuli presented in the right visual field and 433 msec for stimuli presented in the left field. Eleven subjects out of 12 showed a superiority of the right visual field over the left for RT. Overall mean R T was slightly shorter for the left hand than for the right. The right hand was on the average faster in 6 subjects, while the left hand prevailed in the other 6 subjects. There was no apparent relation either between prevailing hand and eye used during testing or between prevailing hand and arrangement o f positive and negative stimuli. Within each visual field, overall mean R T was slightly faster with the ipsilateral hand than with the contralateral hand. Table 2. Experiment 1--Overall mean reaction times (msec)
Left hand Right hand Mean
Side of stimulus Left Right 428 423 438 419 433 421
Mean 425.5 428.5
A n analysis o f variance for a two-factor repeated measurements design, field x h a n d x subjects, with subjects assumed as having r a n d o m effects (see 12, p. 170), was carried out on individual mean RTs. According to this analysis, field was a highly reliable source of R T variance ( F z 9"13; d J ' ~ 1, 11; P < 0 0 2 5 ) ; neither hand nor the field by h a n d interaction yielded significant F values. There were very few errors of omission or commission (see Table 1) and a two-tailed t-test for correlated scores indicated that there was no significant difference in number of errors between left and right visual fields (P > 0"2). Within each one o f the two subgroups responding to different pairs of positive stimuli ( R O and H ; L O and V), no clear relations between R T and type of stimulus were apparent. Overall mean RTs are given in Table 3. In both subgroups there was no significant difference between RTs to the two positive stimuli (P > 0'2 by a two-tailed t-test for correlated scores). Table 3. Experiment 1--Overall mean reaction times (msec) in the two subgroups responding to different pairs of positive stimuli Stimulus RO H L O V
Mean RT 417 423 438 429
Conclusion. The only reliable effect was that of visual field on speed of response, the right visual field stimulation yielding faster responses than the left. Experiment 2 Table 4 gives overall mean RTs in relation to side of stimulation, responding hand and the interaction between these two factors. A n analysis of variance similar to that performed on the results of Experiment 1 showed that neither field, nor hand, nor the interaction between field and hand had any significant effect on RT. Similarly, errors were uniformly distributed in relation to right and left fields (P > 0"2 by a two-tailed t-test for correlated scores).
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
169
Table 4. Experiment 2--Overall mean reaction times (msec)
Left hand Right hand Mean
Side of stimulus Left Right 592 605 596 601 594 603
Mean 598'5 598.5
Table 5 shows overall m e a n R T s for the two subgroups r e s p o n d i n g to different pairs of positive stimuli, in relation to the two stimuli. Six o f the 9 subjects r e s p o n d i n g to 30 ° L a n d 45 ° R h a d faster R T scores for the first stimulus t h a n for the second, with an overall significant difference between R T s to the two stimuli (t - - 2"613; d f = 35; P < 0"02). Similarly, 7 o f the 9 subjects r e s p o n d i n g to 30 ° R a n d 45 ° L h a d faster R T scores for the first stimulus t h a n for the second, the overall difference between the RTs to the two stimuli falling just short o f significance (t = 1"889; dr= 35; P < 0'1). Table 5. Experiment 2--Overall mean reaction times (msec) in the two subgroups responding to different pairs of positive stimuli Stimulus 30° L 45 ° R 30°R 45 ° L
Mean RT 599 646 559 590
Conclusion. W i t h a t a s k m o r e d e m a n d i n g t h a n in E x p e r i m e n t 1, the superiority o f the right visual field for R T was no longer apparent. On the contrary, there was a tendency t o w a r d a left field advantage, a l t h o u g h the interfield difference was n o t significant. RTs to the two orientations less inclined f r o m the vertical were clearly faster t h a n RTs to the other two orientations. Experiment 3 T a b l e 6 gives overall m e a n RTs in relation to side o f stimulation, r e s p o n d i n g h a n d and the interaction between these two factors. Ten subjects o u t o f 12 h a d faster R T scores for the left visual field; 8 subjects were faster with the right hand, 4 with the left hand. A n analysis o f variance similar to t h a t used in Experiments 1 a n d 2 indicated t h a t only field h a d a significant effect on R T ( F = 1l'47; df = 1, 11; P < 0"01). N o significant relation was f o u n d between n u m b e r o f errors and field o f stimulation (P > 0'2). Table 6. Experiment 3--Overall mean reaction times (msec)
Le~ hand Right hand Mean
Side of stimulus Le~ Right 750 800 740 805 745 802-5
Mean 775 772"5
T a b l e 7 gives overall m e a n R T s for the two s u b g r o u p s r e s p o n d i n g to different pairs o f positive stimuli, in relation to the two stimuli. Five o f the 6 subjects r e s p o n d i n g to 15° a n d 45 ° showed faster scores for the first stimulus than for the second; the overall difference between the RTs to the two stimuli was highly significant (t = 3"864; dr= 23; P < 001). Five o f the 6 subjects r e s p o n d i n g to 30 ° and 60 ° showed faster scores for the second stimulus
170 C. UMILT)~,G. RIZZOLATTI, C. A. MARZI, G. ZAMBON[,C. FRANZINI, R. CAMARDAand G. BERLUCCHI
than for the first; also in this case, the overall difference between the RTs to the two stimuli was significant (t = 3"665; df= 23; P < 0'01). Table 7. Experiment 3--Overall mean reaction times (msec) in the two subgroups responding to different pairs of positive stimuli Stimulus 15° 45° 30° 60°
Mean RT 676 811 855 754
Conclusion. There was a significant interfield difference, the dominant field being opposite to that favored in Experiment 1. Faster RTs were obtained from the left visual field than from the right. The two extreme orientations within the range of four presented yielded significantly faster RTs. 4. D I S C U S S I O N Theoretically, the speed of discriminative responses may vary as a function of (a) the amount of information conveyed by the signals, and (b) the "difficulty" of the discrimination. In our three experiments, the number of stimuli was constant, and the probability of occurrence of each particular stimulus was the same. Thus the information content of the signals did not vary over the three tasks. The differences in RT found between tasks must therefore have resulted from differences in discrimination difficulty. The difficulty of a discrimination is a poorly defined entity, which may be considered to be inversely related to two separate factors: stimulus discriminability and stimulus codability. Stimulus discriminability is usually expressed as a function of the number of features on the basis of which the stimuli can be differentiated from one another, and of the degree to which the stimuli differ from one another with respect to each of the distinguishing features. Mathematical formulae for the measurement of discriminability as a determinant of speed of decisions have been proposed [see e.g. 13, 14] but their general applicability is still debated [see 15]. In the present context, stimulus codability may be loosely defined as the ease and economy with which stimuli can be described by words [see e.g. 16]. The stimuli used in our three experiments could be distinguished from one another on the basis of one and the same feature: their orientation. It was the degree to which the stimuli differed from one another with respect to this feature that was different in the three experiments. The angles formed by each of the positive stimuli with the two negative stimuli were 45 ° and 90 ° in Experiment 1, 15° and 60 ° in Experiment 2, 15° and 45 ° in Experiment 3. As for stimulus codability, a word suffices to identify each of the stimuli in Experiment 1: horizontal and vertical for H and O; right for RO, left for LO. It is interesting that these highly codable orientations usually serve as standards of comparison for the judgment of line orientation, the vertical and horizontal providing the primary anchors, and the two intermediate orientations providing the secondary anchors within the orientation continuum [see 17]. Further, it is known from several psychophysical studies that the human visual system is better tuned for the vertical and horizontal orientations than for the oblique orientations [see review in 18]. Unlike the stimuli of Experiment 1, the description of the stimuli in Experiments 2 and 3 (as opposed to their pictorial representation) is neither easy nor economical. The suggestion can perhaps be made that the distinction ~-~_tween right and
HEMISPHERIC DIFFERENCES IN THE DISCRIMINATION OF LINE ORIENTATION
171
left might be used to split up the task in Experiment 2 into two separate discriminations. With all these considerations in mind, we expected absolute RT to be shortest in Experiment l, intermediate in Experiment 2 and longest in Experiment 3. This expectation is clearly supported by the findings. In addition, the findings show a right-field superiority for RT in the "easy" task, an opposite left-field superiority for RT in the "difficult" task, and no clear-cut interfield differences in the task of intermediate difficulty. The most parsimonious interpretation of asymmetries in discriminative RT between left and right visual fields, such as those observed in the present study, assumes that they are due to (1) a qualitative differentiation between perceptual mechanisms in the two hemispheres, and (2) a more direct, and perhaps more efficient communication between each visual field and the contralateral cerebral hemisphere [see e.g. 5]. Accordingly, it is assumed that the left hemisphere prevailed in the performance of the task of Experiment 1 while the right hemisphere prevailed in the performance of the task of Experiment 3; only a tendency toward a right-hemisphere predominance was apparent for the task of Experiment 2. This would imply that discrimination of line orientation is performed by the left hemisphere when the task is an "easy" one, and by the right hemisphere when the task is a "difficult" one. How is this to be reconciled with current views about the hemispheric lateralization of verbal abilities to the left side, and of perception of spatial relations and nonverbal visual patterns to the right side? The discrimination of line orientation typically qualifies as a spatial task; hence one would expect it to belong fully to the domain of specializations of the right hemisphere, regardless of whether the discrimination is easy or difficult. The consideration of some findings related to ours may help the discussion of this issue. WHITE [19] has tested the ability of normal subjects to report the orientation of a thin line flashed for 20-25 msec at 3 degrees to the right or to the left of the fixation point. Four orientations were used, corresponding exactly to the ones employed in our Experiment 1. A response code allocated a different number to each particular orientation, and subjects responded by calling out the number corresponding to the perceived orientation. Accuracy of recognition was significantly better in the right field than in the left, and this right field superiority correlated positively with the superiority of the same field shown by the same subjects on a similar task involving the verbal identification of single letters. From this finding WHITE [19] has inferred that the right field superiority for the recognition of line orientations depends on the existence of a selective contour-tuning apparatus in the left hemisphere, and that this same apparatus, rather than the left-hemisphere speech mechanisms, may be responsible for the right-field superiority in the perception of single letters. This interpretation has been questioned by GEFFNERet al. [20], who suggest that the use of a vocal response in White's experiment on discrimination of line orientation may have introduced a bias in favor of the left hemisphere, thereby masking a possible right hemisphere superiority for this spatial task. Yet, their account of White's results is made unlikely by the similarity between his results and those of our Experiment 1, in which we used a motor rather than vocal response. On the other hand, White's explanation of his own findings is made unlikely by the results of our Experiments 2 and 3, since his postulated contour-tuning apparatus should have caused a superiority of the right visual field in these experimental conditions as well. The superiority of the right visual field, and presumably of the left hemisphere, seen in our Experiment 1 as well as in the comparable experiment by WHITE [19], can be due to the high discriminability of the stimuli, or to their codability, or to both. Although we have no evidence to reject completely the discriminability factor, the present state of knowledge
172 C. UMILT,~,G. RIZZOLATTI,C. A. MARZ1,G. ZAMBONI,R. FRANZINI,R. CAMARDAand G. BERLUCCHI about functional asymmetries between the hemispheres suggests that it was codability which was instrumental in favoring the left hemisphere under these experimental conditions. Discriminative responses to these highly codable orientations were most probably facilitated by a verbal mediator: hence the superiority of the left hemisphere. On the other hand, it is clear that a verbal mediation does not offer itself as the best strategy for performing the discrimination tasks of Experiments 2 and 3. Here, identification of the stimuli by a purely "visual" process of matching would appear much more economical than their recognition through the matching of each visually presented item with its verbal (acoustic) label. We suggest that it was the adoption of a visual matching strategy that shifted the hemispheric dominance toward the right side in Experiments 2 and 3. Recent studies in normal man have documented the superior ability of the right hemisphere in perceiving spatial relations in the visual modality. The results of Experiments 2 and 3 and their present interpretation are in accord with these studies [21, 22, 23]. If our explanation of the results is correct, then it follows that discrimination of line orientation in man is a much more complex affair than is assumed by current neurophysiological theories based on the neuronal line detectors discovered by HUBEL and WIESEL [24, 25, 26] in the visual cortex of cats and monkeys. While it seems most reasonable that these detectors must constitute a preliminary stage in the discrimination process, the foregoing discussion suggests that the discriminative decision ultimately depends on higher order processes lateralized to one hemisphere. Whether it is the left hemisphere or the right that directs the response appears to be determined by the role played by verbal mediation. The suggestion that discrimination of line orientation may involve a verbal process is implicit in the theory proposed by ATTNEAVEand REID [27], who argue that perceived orientation depends upon its naming or description within a labile subjective frame of reference whose main axes normally coincide with the physical horizontal and vertical co-ordinates, but which can revolve about this position by spontaneous decision or instruction. However, a pictorial representation of stimulus orientations within the selected frame of reference would seem more appropriate for efficient discriminative responses when verbal categorization of the stimuli with respect to the main axes is equivocal or uneconomical. Such is certainly the case for the stimuli used in Experiment 2 and especially those in Experiment 3. The preference for the stimuli which were closest to the vertical in Experiment 2, and for the stimuli which were closest to the vertical and the horizontal in Experiment 3 would suggest that they were used as "derived" anchors [see 17] within the normal frame of reference. No clear preference for a particular stimulus was found in Experiment 1, although faster responses were expected for the vertical and horizontal orientations, in view of both the psychophysical findings quoted on page 170 and the above mentioned study of ATTNEAVE and REID [27]. These authors found that the perceived vertical and horizontal orientations evoked faster responses than the other two orientations. On the other hand WHITE [19] has reported that accuracy of responses to the same four orientations did not vary significantly as a function of the stimulus while DICK and DICK [28] found a superiority of the two diagonals over the vertical and horizontal orientations for accuracy of response. It must be pointed out that the experiments by DIcK and DICK [28] and WHITE [19] and our own Experiment 1 differed from the experiment by ATTNEAVE and REID [27] in that presentation of the stimuli was in the center of the visual field in the latter experiment, and lateralized to the left or right visual fields in the former three experiments. Whether the discrepancy in the results is due to this or to other procedural differences must be settled by future experiments.
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REFERENCES 1. MILNER, B. Interhemispheric differences in the localization of psychological processes in man. BE. meal. Bull. 27, 272-277, 1971. 2. STUODERT-KENNEDY,M. and SHANKWEmER,D. Hemispheric specialization for speech perception. J. acoust. Soc. Am. 48, 579-594, 1970. 3. DARWIN, C. J. Ear differences in the recall of fricatives and vowels. Q. J. exp. Psychol. 23, 46-62, 1971 4. UMILT~, C., FROST, N. and HYMAN,R. Interhemispheric effects on choice reaction times to one-two-, and three-letter displays. J. exp. Psychol. 93, 198-204, 1972. 5. RIZZOLATTL G., Ur~rT~k, C. and BERLUCCHI,G. Opposite superiorities of the right and left cerebral hemispheres in discriminative reaction time to physiognomical and alphabetical material. Brain 94, 431-442, 1971. 6. GEFFEN, G., B~a~sHAw, J. L. and WALLACE,G. Interhemispheric effects on reaction time to verbal and nonverbal visual stimuli. J. exp. Psychol. 87, 415-422, 1971. 7. K a y , D. Functional asymmetry of the brain in dichotic listening. Cortex. 3, 163-178, 1967. 8. LIBERMAN,A. M. Some characteristics of perception in the speech mode. Res. Publ. Ass. Herr. ment. Dis. 48, 238-254, 1970. 9. SrUDDERT-KENNrDY,M., LIBERMAN,A. M., HARRIS, K. S. and COOPER, F. S. Motor theory of speech perception: a reply to Lane's critical review. Psychol. Rev. 77, 234-269, 1970. 10. W ~ a ~ O r O N , E. K. and RABn~, P. Perceptual matching in patients with cerebral lesions. Neuropsychologic 8, 475-487, 1970. 11. DE RENZI, E., FAGLIONI, P. and ScoTrI, G. Judgements of spatial orientation in patients with focal brain damage. J. Neurol. Neurosurg. Psychiat. 34, 489-495, 1971. 12. MYERS, J. L. Fundamentals of Experimental Design. Allyn & Bacon, Boston, 1966. 13. CROSSraAN, E. R. F. W. The measurement of discriminability. Q. J. exp. Psychol. 7, 176-195, 1955. 14. LAMINC, D. R. J. Information Theory of Choice-Reaction Times. Academic Press, New York, 1968. 15. BROADBENT,D. E. Decision and Stress. Academic Press, New York, 1971. 16. COHEN, G. The effect of codability of the stimulus on recognition reaction time. BE. J. Psychol. 60, 25-29, 1969. 17. KEENE, G. C. The effect of response codes on the accuracy of making absolute judgments of lineal inclinations. J. gen. Psychol. 69, 37-50, 1963. 18. APPELLE, S. Perception and discrimination as a function of stimulus orientation: "The oblique effect" in man and animals. Psychol. Bull. 78, 266-278, 1972. 19. W.rrE, M. J. Visual hemifield differences in the perception of letter and contour orientation. Can. J. Psychol. 25, 207-212, 1971. 20. GEFFEN, G., B~DSnAW, J. L. and NETTLETON, N. C. Hemispheric asymmetry: verbal and spatial encoding of visual stimuli. J. exp. Psychol. 95, 25-31, 1972. 21. K~MX~A, D. Dual functional asymmetry of the brain in visual perception. Neuropsychologia 4, 275-285, 1966. 22. K a M ~ , D. Spatial localization in left and right visual field. Can. J. Psychol. 23, 455-458, 1969. 23. DtrRNFORD, M. and KI~URA, D. Right hemisphere specialization for depth perception reflected in visual field differences. Nature, Lond. 231, 394-395, 1971. 24. HtraEL, D. H. and WrESEL,T. N. Receptive fields of single neurones in the cat's striate cortex. J. Physiol., Lond. 148, 574-591, 1959. 25. Ht~EL, D. H. and WIESEL, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229-289, 1965. 26. HUBEL,D. H. and WrESEL, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol., Lond. 195, 215-243, 1968. 27. ArTNEAW, F. and REID, K. W. Voluntary control of frame of reference and slope equivalence under head rotation. J. exp. Psychol. 78, 153-159, 1968. 28. DICK, A. O. and DICK, S. O. An analysis of hierarchical processing in visual perception. Can. J. Psychol. 23, 203-211, 1969. 29. BERLUCCnX, G. Cerebral dominance and interhemispheric communication in normal man. In The Neurosciences: A Third Study Program. The M.I.T. Press, Cambridge, Mass., 1973 (in press). 30. Ur~LT~,, C., l~zzoLAr'n, G., MARZI, C. A., ZAMBO~, G., FRANZlNI,C., CAMARDA,R. and BERLUCCHI,G. Hemispheric differences in normal human subjects: further evidence from study of reaction time to lateralized visual stimuli. Brain Res. 49, 499-500, 1973.
R~um~----Des sujets normaux droitiers 6taient entralnrs ~, discriminer entre des rectangles orientrs avec leur axe majeur vertical, horizontal et selon les deux directions intermrdiaires. Ces stimulus ont 6t6 prrsentrs ~ droite et h gauche du point de fixation. Les sujets ont montr6
174 C. UMILT/~, G. R1ZZOLATTI, C. A. MARZI, G. ZAMBONI,C. FRANZINI, R. CAMARDAand G. BERLUCCHI des r6actions discriminatives (soit la d6pression d'un levier) plus rapides aux stimulus apparaissant dans le champ visuel droit. D'autre part, deux autres groupes de sujets normaux droitiers ex6cutant une t~,che de temps de r6action semblable 5, la premi6re mais avec des stimulus orient6s dans d'autres directions (respectivement 30 ° et 45 ° h droite et ~t gauche de l'axe vertical; 15 °, 30 °, 45 ° et 60 ° du plan vertical), ont montr6 des reactions discriminatives plus rapides aux stimulus pr6sent6s dans le champ visuel gauche. Les diff~,rences de performance entre les deux moiti6s du champ visuel sont attribu6es ~t des diff6rences h6misph6riques dans la discrimination de l'orientation des lignes. Le fait que les h6misph6res soient superieurs r u n par rapport ~, rautre selon le type de la discrimination est, b, son tour, attribu6 ~, l'utilisation des m6diateurs verbaux dans le cas des discriminations pr6fer6es par l'h6misph6re gauche, et ~t l'usage d'une strat6gie non verbale dans le cas des discriminations pr6f6r6es par l'h6misph6re droit. Zusammenfassung--Normale, rechtshfindige Versuchspersonen, welche gelernt hatten, Rechtecke zu unterscheiden, welche mit ihrer langen Seite vertikal, horizontal oder in den beiden Zwischenrichtungen orientiert waren und welche entweder rechts oder links yore Fixationspunkt dargeboten wurden, konnten diese Aufgabe schneller 18sen (das heisst einen Knopf dr/icken), wenn die Testreize in der rechten H~ilfte des Gesichtsfeldes dargeboten wurden. Zwei andere Gruppen von normalen und rechtsh~indigen Versuchspersonen hatten eine/ihnliche Aufgabe mit Messung der Reaktionszeit bei Testzeichen zu 18sen, die in andere Richtungen orientiert waren (je nachdem 30 ° und 45 ° yon der vertikalen nach links und rechts abweichend; oder 15 °, 30 °, 45 ° und 60 ° yon der vertikalen abweichend), l m Gegensatz zu der ersten Gruppe waren jene nun schneiler wenn die Reize in der linken H/ilfte des Gesichtsfeldes dargeboten wurden. Diese Unterschiede in der Leistungsfahigkeit zwischen den beiden Gesichtsfeldh/ilften werden mit hemispharischen Verschiedenheiten in der Unterschiedsempfindlichkeit for Linienorientierungen in Verbindung gebracht. Die unterschiedlichen hemisph~rischen Leistungsf/ihigkeiten, die bei den verschiedenen Aufgaben ermittelt wurden, werden der Bevorzugung einer verbalen Strategie durch die linke Hemisph~ire zugeschrieben, w~ihrend angenommen wird, dass in der rechten Hemisphare zur Unterscheidung eine nicht verbale Strategie zur Anwendung kommt.