The role of stimulus discriminability and verbal codability in hemispheric specialization for visuospatial tasks

Neutopsychologia, Vol. 17, pp. 195 to 202, Pergamon Press Ltd. 1979. Printed in Great Britain.

THE ROLE OF S T I M U L U S D I S C R I M I N A B I L I T Y A N D V E R B A L C O D A B I L I T Y IN H E M I S P H E R I C SPECIALIZATION FOR V I S U O S P A T I A L TASKS* G. BERLUCCHI, D. BRIZZOLARA,'~ C. A. MARZI, G. RIZZOLATTI+ + and C. U M I L T , ~ t Institute of Physiology of the University of Pisa and Laboratory of Neurophysiology of the C.N.R., Pisa, Italy Abstract--Normal right-handed male subjects were required to read the time on a clockface tachistoscopically presented in the right and left visual fields. The response had to be made both accurately and quickly. The number of errors was the same for the two visual fields, but the speed of the vocal response was higher for the left field suggesting a right-hemisphere dominance for this task. It is argued from this result that the factor of verbal codability is not sufficient to induce a right-field/left-hemisphere superiority in the case of a difficult visuospatial discrimination. INTRODUCTION THE DEFINITIONOf the differential functions of the two hemispheres of the h u m a n brain, an issue whose importance has been stressed by HANS-LUKAS TEUBER with his usual clarity [I], can be attempted with a variety o f tests carried out on patients with unilateral brain damage or surgical or dysgenetic hemispheric disconnection, as well as on normal subjects with an intact nervous system [2, 3]. A c o m m o n difficulty with these approaches is the fact that the possibility of showing hemispheric specializations is contingent not only u p o n the nature of the test material and the conditions of testing, which can be fully determined by the examiner, but also u p o n the strategy adopted by the subject for performing the task, a factor which often the examiner can neither control nor exactly define. Thus, it has usually proven difficult to design tests for evidencing the superiority of the right hemisphere for several aspects of spatial vision, because this superiority can be masked by the utilization of mediating processes subserved by the left hemisphere, such as for example covert verbal encoding, in the performance o f ostensibly non-verbal visuospatial tasks. For example, the discrimination of line orientation, an ability which is severely affected by right-hemisphere lesions [4, 5], can similarly be shown to require a greater involvement of the right hemisphere in normals, but only when the discrimination is relatively difficult [6-9]. An opposite, left-hemisphere superiority has been observed for discriminations o f line orientations involving few stimuli that can be easily differentiated from each other [9, 10]. This finding has been tentatively accounted for by assuming that easily differentiable line orientations can be encoded verbally, thereby allowing the use of verbal mediation for performing the discrimination [8, 9]. However, according to this interpretation even *Work supported in part by a grant from the C.N.R. Hnstitute of Psychology of the University of Bologna. ~.Institute of Human Physiology of the University of Parma. 195

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G. BERLUCCHI, D. BRIZZOLARA, C. A. MARZI, G. RIZZOLATTI and C. UMILT~

difficult visuospatial tasks could be performed better by the left hemisphere, provided the subject could utilize a verbal code allowing the precise identification of the items in the array used for discrimination. Alternatively, it is possible that regardless of verbal mediation easy visuospatial tasks are carried out more efficiently by the superior analytical ability of the left hemispheres, whereas the right hemisphere becomes dominant when the difficulty of the task exceeds a critical level beyond which discrimination by analysis becomes uneconomical (see [11]). In an attempt to distinguish the relative importance of the two factors, discriminability and verbal codability, for hemispheric dominance in visuospatial tasks, we have tested the ability of normal subjects to read the time on a clockface tachistoscopically presented in the right and left visual fields. This task involves a visuospatial discrimination based on the judgement of the relative length and orientation of the two hands; on the other hand, each stimulus in the array can be precisely identified by a long established and highly practiced verbal response, thereby combining a relatively low discriminability, due to the fact that the orientation of each of the two hands can vary independently and ahnost continuously, with a perfect verbal codability. As in all visual tests of hemispheric specialization in normals, the basic assumption underlying the experinaent has been that superior performance of one visual field in terms of speed and/or accuracy of discrimination reflects the dominance of the contralateral hemisphere for the task under examination. METHOD Subjects Twenty-four right-handed male subjects ranging in age from 20 to 40 yr volunteered to take part in the experiment. They had normal vision and were naYve as to the purpose of the experiment.

Stimuli The stimuli were 80 aifferent slides tachistoscopically back-projected on a tangent screen made of g r o u n d glass which was positioned at 1 m from the subject's eyes. A Kodak Carousel projector equipped with an electronic shutter was used for the presentation of the stimuli. Each slide showed a circular clockface which was graduated into the usual twelve 5-min divisions but was not numbered. F r o m the observer's point of view the diameter of theclockface subtended 5 of visual angle, while the hour-hand and the minute-hand subtended respectively 1.5 and 2 . Each slide was projected to the right or the left of a fixation mark, the distance between this mark and the center of the dial being 7.5 ° of visual angle. The background luminance of the screen was about 3 cd/m2; the mean luminance of each stimulus was about 30 cd/m 2. The 80 different stimuli were selected and arranged into a fixed sequence according to the following criteria: (1) the minutehand always pointed to one of the 12 markers on the dial, while the hour-hand could take any position which, compatibly with the position of the other hand, would unequivocally indicate a given time: (2) the sequence was divided into two blocks of 40 stimuli in each of which either hand appeared the same n u m b e r of times in the right and left halves of the dial; (3) in each block of 40 stimuli either hand appeared the same n u m b e r of times in the upper and lower halves of the dial. (The subjects were informed before the experiments a b o u t the first restraint.) A typical stimulus is s h o w n in Fig. 1.

Procedure The subject sat on an easy chair provided with a head-rest. He was instructed to fixate binocularly on a black mark in the centcr of the tangent screen in response to an auditory warning signal. F r o m 2 to 3 sec following this signal a lateralized stimulus was projected for 100 msec. The task for the subject was to respond as fast and accurately as possible to each stimulus by reading aloud the time shown on the clockface. The signal from a nlicrophone attached to the head-rest and placed under the subject's chin was used to stop a millisecond counter which had been automatically started at the onset of the visual stimulus. An experimenter in a nearby r o o m recorded the reaction time and took note of whether the response was correct or not. Reaction times longer than 3 sec were not considered. In addition, reaction times from occasional trials on which the millisecond counter was stopped by irrelevant vocalizations preceding the actual response were also discounted. Each subject attended for one practice session and two test sessions which were run on ditferent days. In each test session the subject was tested on the fixed sequence of 80 stimuli, with a block of 40 stimuli being presented in one visual field and the other block in the opposite visual field. Each block of

197

HEMISPHERIC SPECIALIZATION FOR VISUOSPATIAL TASKS

FIG. 1. A typical stimulus. 40 trials was preceded by five practice trials using stimuli of the same nature b]at differing from those in the sequence. In the first session the right field was tested first in 12 subjects and the left field was tested first in the other 12 subjects. In the second session the reverse order was followed. No feedback was given as to accuracy and speed of each response in the two test sessions. RESULTS It was a p p a r e n t from the analysis of the protocols that in each subject the n u m b e r of correct reaction times available for analysis was considerably inferior to the n u m b e r of total trials, because of either incorrect responses, or delays longer t h a n 3 sec, or useless reaction times due to the stopping of the millisecond c o u n t e r by irrelevant vocalization. With the aim of o b t a i n i n g a more accurate assessment of individual reaction time, the data from those subjects who had provided less than 50~o usable reaction times, i.e. less t h a n 80 correct reaction times in a total of 160 trials, were dropped. Six subjects were thus discarded; since the field initially used for stimulus presentation was the right in 3 of these subjects a n d the left in the 3 others, the order of field a l t e r n a t i o n was exactly counterbalanced in the remaining 18 subjects. The mean data from this group of 18 subjects are shown in Table 1. The m e a n n u m b e r of correct reaction times available for analysis was Table 1 Mean reaction time (in brackets: standard deviation) Mean percentage of errors (in brackets: range)

RVF 1325.4 msec (299.7)

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105 with a m e a n of 52.1 reaction times for the right field a n d 52.9 reaction times for the left field. Thus, the n u m b e r of correct reaction times which were available for analysis was almost identical for the two visual fields. F o r each subject median reaction time was computed across sessions for each field. The mean across subjects of these medians was 1325.4 msec for the right field a n d 1273.1 msec for the left field. A t-test for matched scores indicated that this 52.3 msec difference in favor of the left field is statistically significant

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G. BERLUCCHI, D. BRIZZOLARA, C. A. MARZI, G. RIZZOLAT'TI a nd C. UMILTA

( P < 0.01). Thirteen subjects out o f 18 showed a faster reaction time for the left field. E r r o r s a n d d e l a y e d correct responses (longer than 3 sec) were equally distributed in the two fields. The conclusion from these findings is that the left field, a n d by implication the right hemisphere, p r e d o m i n a t e for the speed o f time reading, in spite o f the high verbal codability o f the stimuli a n d the use o f a verbal response. A n a d d i t i o n a l analysis was carried out to check for the existence o f correlations betxxeen reaction time a n d the position o f the clock hands. Since it was clear that reaction lime in relation to the position o f the h o u r - h a n d d e p e n d e d p r e d o m i n a n t l y on the acoustical properties o f the vocal response, this aspect of the analysis was not d e e m e d interesting. On the contrary, the acoustical properties o f the response did not influence the relation between reaction time a n d the position o f the minutehand. F o r e x a m p l e the r e a c t i o n times for three-five a n d three-fifteen could be c o m p a r e d d i s r e g a r d i n g the acoustical properties o f the response, the millisecond counter being stopped in either case by the w o r d three. The results o f the analysis o f the correlations between the p o s i t i o n o f the m i n u t e - h a n d a n d reaction time in the two fields are shown in Fig. 2. Since 0'

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FIG. 2 Relation between reaction time and the position of the minute-hand on the clockface. The mean reaction time to stimuli x~ith the minute-hand on the 0' position in the left field (shortest reaction time) was taken as 100°~; and the mean reaction times for stimuli ~ith the minute-hand oil the other positions in cilher field, or for stimuli in the minute-hand on the 0' position in the right field, are shown as per cent increases \~ith respect to the reference. the reaction times to stimuli with the m i n u t e - h a n d on the 0" position in the left field ~ e r e the shortest, the mean o f them was taken as a reference for the percentage increases of the m e a n reaction times to stimuli with the m i n u t e - h a n d in the other positions. The reaction times were generally shorter for the left field for all positions o f the minute-hand, but this left field superiority x~as less clear when the m i n u t e - h a n d was in the left half of the clockface. In a d d i t i o n , reaction times to stimuli with the m i n u t e - h a n d in the upper half o f the clockface ~ e r e c o n s i d e r a b l y s h o r t e r than reaction times to stimuli with the m i n u t e - h a n d in the lower h a l l both in the right a n d left visual field. A t-test for matched scores indicated a highly significant superiority' o f reaction time to stimuli with the minute h a n d in the upper half of the clockface ( P < 0.01 ). The ascending

HEMISPHERIC SPECIALIZATION FOR VISUOSPATIAL TASKS

199

order for the four blocks of reactions times corresponding to the combinations between the right and left visual fields (RF, LF) and the right and left halves of the clockface (rh, lh) was the following: LF, rh (fastest reaction time); LF, lh; RF, lh; RF, rh. DISCUSSION The findings agree with previous studies [9, 12-15] in indicating that the speed of the response is a rather sensitive measure for evidencing visual field asymmetries. According to the basic assumption of this experiment, the advantage of the left field for the speed of perceiving the position of the hands on a clockface reflects a superiority of the right hemisphere for this task. The possible importance of the language factor for the performance of this task can be discussed in relation to (a) the use of a vocal output, (b) the aspecific lateralization of attention to the left hemisphere presumably resulting from any kind of overt or covert verbal activities [16], and (c) the specific process of verbal encoding. KIMURA and DURNFORD [8] have suggested that a vocal reaction time is an inadequate measure for showing the superiority of the right hemisphere for a given task, since a vocal output would al~ays depend on left hemisphere mechanisms thereby introducing a bias in favor of this hemisphere. Yet a theoretical analysis of interhemispheric interactions shows that if the processing of a given sensory material is carried out by one particular hemisphere, then the discrimination of that material should be faster when the input is directed to the dominant hemisphere, regardless of xvhether the final response is produced by that or the opposite hemisphere. If only one hemisphere has access to the output while the other hemisphere is specialized at decoding the input, the channelling of the input into the hemisphere controlling the output should by no means increase the speed of the response, since informations would have to be relayed first to the other hemisphere for decoding [17]. The present experiment and at least three previous studies on hemispheric dominance for visuospatial abilities [14, 18, 19] have in fact demonstrated a superiority of the left visual field, and by implication of the right hemisphere, by means of a vocal reaction time measure. Particularly significant in this respect is the study by GROSS [14] showing the same advantage of the left field for the discrimination of cell matrices, independent of whether the response x~as vocal or manual. All these results of a left visual field superiority in tasks requiring a verbal response are also difficult to reconcile with the hypothesis of an unspecifi.c speechor language-related priming of the left hemisphere, resulting in an attentional bias in favor of the right visual field [16]. Granted that an overt response is compatible with a superiority of the right hemisphere, we now turn to the central point of this paper, i.e. the significance of verbal codability for hemispheric lateralization of visuospatial abilities. In accord with the idea that hemispheric asymmetry of functions is basically linked to the distinction between verbal and nonverbal activities, previous studies on normals [9, 20, 21] have suggested that the superiority' of the right hemisphere for visuospatial discriminations is contingent upon the difficulty to encode the stimuli in words. Hoxvever, stimuli which are difficult to encode verbally aie usually also difficult to differentiate, hence it is conceivable that a right hemisphere superiority for visuospatial discriminations may be associated with low discriminability, rather than (or in addition to) difficult codability. Our attempt to dissociate the two factors has indicated that highly verbalizable and familiar visuospatial stimuli can nevertheless be differentiated more efficiently, by the right hemisphere, presumably because of the complexity of the discrimination. Thus it can be suggested that for a complex visuospatial discrimination, such as the estimation of the position of the hands of a clock, verbal encoding

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G. BERLUCCHI, D. BRIZZOLARA,C. A. MARZI, G. RIZZOLATTIand C. UMILT.~

by the left hemisphere must be preceded by a processing o f the visual input in the right hemisphere. This suggestion is c o n s o n a n t with theories o f visuospatial gnosis derived from neurological data [22], a n d agrees well with Luria's finding that reading the time on a clockface is impaired, presumably at two different levels o f competence, by specific lesions o f either hemisphere [23]. In addition, it is in a c c o r d with data indicating that the two henrispheres differ in their ability to deal with visuospatial i n f o r m a t i o n already at an early stage o f processing [8, 24]. O f the additional effects observed in the present study, the large superiority for reaction time of the upper visual field over the lower is in line with similar reports of asymmetries o f visual perception a b o u t the horizontal meridian [25 27], an d can be related to theories o f a d a p t a t i o n o f the visual system to u p - d o w n asymmetries in a m b i e n t illumination (see e.g. [28]). The factor o f visual acuity is most likely responsible for the relations between right-left visual field asymmetries in reaction time and the position o f the nainute-hand in the right a n d left halves o f the clockface. The effect o f visual acuity should add to the left field effect for stimuli with the minute hand in the right half o f the dial, and detract from it for stimuli with the m i n u te - h a n d in the left half of the dial. This is exactly what was found. A final factor that should be taken into consideration is the relation between the speed o f a n a m i n g response a n d the average length o f the response in syllables a nd words [29]. This factor may at least in part a c co u n t for the fact that reaction time was considerably shorter for stimuli with the m i n u te - h an d on the 0' position (one word) than for all the other stimuli (two or more words). REFERENCES 1. TEUBER, H.-L. Why two brains? In The Neuroscienees': Third Study Program. F. O. SCHM1TTand F. G. WORDEN (Editors), pp. 71 74. MIT Press, Cambridge, Mass., 1974. 2. MILNER,B. lntcrhcmispheric differences in the localization of psychological processes in man. Brit. Med. Bull. 27, 272 277, 1971. 3. MmNER, B. Hemispheric specialization: scope and limits. In The Neuroscie#lces." T/tird Study Prograt#t, F. O. SC'H~,IITTand F. G. WORDE'q(Editors), pp. 75 89. MIT Press, Cambridg,~, Mass., 1974. 4. WARR1N(;-IOY,E. K. and RABIN. 1'. Perceptual matching in patients v,ith cerebral lesions. Nem'opsychologia 8, 475 487, 1970. 5. Bf.~IoN, A., HANrqAY, H. J. and VAR~EY, N. R. Visual perception of line direction in patients with unilateral brain disease. Neurology 2.5,907 910, 1975. 6. FONIENOT, D. J. and BENTOn, A. L. Perception of direction in the right and left visual ticlds. Neurop~Tcholo,~,ia 10, 447-452, 1972. 7. ATKINSON,J. and EC~Ellk H. Right hemisphere superiority in visual orientation matching. Canad. J. Psycho/. 27, 152 158, 1973. 8. KVqURA,D. and DUR'qFORD,M. Normal studies on the function of the right hemisphere in vision. In Hemisphere FU#lctio#l in the thtman Brahl, S. J. DV~IONDand J. G. BEAUrqONT(Editors), pp. 25 47. Elek Science, London, t974. 9. UMILT,~,C., RIZZOLATTI,O., MARZ1,C. A., ZAMBONI,G., ERANZINI,C., Q'AMARDA,R. and BERLU('CHI, G. Hemispheric differences in the discrimination of line orientation. Neltrop.Evchologia 12, 165 174, 1974. 10. Wtlll E, M. J. Visual hemifield differences in the perception of letter and contour orientation. Ca#tad. J. Psyehol. 25, 207 212, 1971. 11. BRADSHA\V,J. L., GALES, A. and ]:',~q{TERSON, K. Hemispheric differences in processing visual patterns. Quart. J. exp. P,vychol. 28, 667 681, 1976. 12. RIZZOLATTLG., Urq~Lr.k, C. and BIRLUC('t~I,G. Opposite superiorities of the right and left cerebral hemispheres in discriminative reaction time to physiognomical and alphabetical material. Brahl 94, 431-442, 1971. 13. GEFFEN,G., BRADStIA',V,J. L. and WALLACt:,G. hlterhemispheric eft'cots on reaction time to verbal and non-verbal visual stimuli. J. exp. Psychol. 87, 415 422, 1971. 14. GROSS,M. M. Hemispheric specialization for processing of visually presented verbal and spatial stimuli. Percept. Psychophys. 12, 357 363, 1972. 15. MOSCOVlTCH,M., SCULLION. D. and CHRISTIE,D. Early versus lute stages of processing and their relation to functional henaispheric asylnmetries in face recognition..l.e.vp. Ps),chol., Ht#mm Perception and Performance 2, 400 416, 1976.

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16. KINSBOURNE, M. The cerebral basis of lateral asymmetries in attention. A cta Psychol. 33, 193-201, 1970. 17. MARZI, C. A. and BERLUCCHI, G. Right visual field superiority for accuracy of recognition of famous faces in normals. Neuropsychologia 15, 751-756, 1977. 18. BEAUMONT,G. and DIMOND, S. Interhemispheric transfer of figural information in right- and non-right handed subjects. Acta Psychol. 19, 97-104, 1975. 19. LONGDEN, K., ELLIS, C. and IVERSEN, S. D. Hemispheric differences in the discrimination of curvature. Neuropsychologia 14, 195-202, 1976. 20. FONTENOT, D. J. Visual field differences in the recognition of verbal and non-verbal stimuli in man. J. comp. physiol. Psychol. 85, 564-569, 1973. 21. DEE, H. L. and FONTENOT, D. J. Cerebral dominance and lateral differences in perception and memory. Neuropsychologia 11, 167-173, 1973. 22. DE RENZI, E., Sco'rrl, B. and SPINNLER, H. Perceptual and associative disorders of visual recognition. Relationship to the side of the cerebral lesion. Neurology 19, 634-642, 1969. 23. LURIA, A. R. Higher Cortical Functions in Man. Tavistock, London, 1966. 24. BRYDEN, M. P. and ALLARD, F. Visual hemifield differences depend on typeface. Brain Lang. 3, '191-200, 1976. 25. JULESZ, B., BREITMEYER, B. and KROPFL, W. Binocular-disparity-dependent upper-lower hemifield anisotropy and left-right hemifield isotropy as revealed by dynamic random-dot stereograms. Perception 5, 129-141, 1976. 26. OLSON, D. R. and HILDYARD, A. On the mental representation of oblique orientation. Can. J. Psychol. 31, 3-13, 1977. 27. TARTAGLIONE,A., FAVALE, E. and BENTON, A. L. Researches on functional asymmetry and independence of lower versus upper visual field. In preparation. 28. GIBSON, J. J. The Perception of the Visual World. Houghton Mifflin, Boston, 1960. 29. BROWN, R. W. and LENNEBERG, E. H. A study in language and cognition. J. abnorm. Soc. Psychol. 42, 33-44, 1954. R~sum~

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