Impaired grating discrimination following right hemisphere damage

0X-3932189S3.00+0.00 :(" 1989PergamonPress plc

,Veuropsycholog!o. Vol. 27, No. 2. pp. 259-263. 1989

Prmtedm GreatBritain.

NOTE IMPAIRED

GRATING

DISCRIMINATION FOLLOWING DAMAGE

ANNA GRAB~WSKA,*$ CARLO SEmNzA,t$

RIGHT HEMISPHERE

GIANFRANC~ DENES: and STEFANOTESTAX

*Department of Neurophysiology, Nencki Institute of Experimental Biology, 3 Pasteur Street, 02-093 Warsaw, Poland; tDepartment of General Psychology, University of Padua, 3 Piazza Capltaniato, 35139 Padua, Italy; and SNeurological Clinic, University of Padua. 5 Via Giustiniani, 35128 Padua, Italy (Receiurd 17 March 1987; Accepted 20 April 1988) Abstract-We investigated the effect of unilateral brain lesions on visual discrimination of low-, middle- and high-frequency gratings. The performance of patients with right hemisphere lesions was significantly impaired compared with that of both controls and patients with left hemisphere lesions. This impairment was largely limited to patients with right posterior hemispheric lesions and was present with all spatial frequencies. These findings run counter to the hypothesis that high and low spatial frequencies are preferentially processed by different hemispheres.

INTRODUCTION IN THE last two decades

gratings have rated among the most frequently used stimuli in both neurophysiological and psychophysical research. This popularity is partially due to an interest in CAMPBELL and ROBSON'S hypothesis [S] that the nervous system analyses all visual patterns in terms of their spatial frequency Fourier components. Gratings, whose spatial frequency and contrast are easy to control. are therefore a convenient material in research on properties of cerebral processing. Campbell and Robson’s hypothesis [5] has also influenced views on brain lateralization in man. Attempts have been made at explaining hemispheric asymmetry in terms of effectiveness in analyzing high and low frequency information by the left and right hemispheres [20,21,22]. Sergent’s hypothesis suggests that the left hemisphere is specialized in processing information carried by high frequency, while the right hemisphere is biased towards efficient use of low frequency information. There are few reports in the literature on laterality effects in the perception of gratings. Most concern simple contrast sensitivity to gratings using detection as a critical performance. Some papers show a hemifield asymmetry [I, 153, others do not [Z, 3,9,18] and suggest that right left asymmetries can be attributed to retina1 nasal-temporal rather than hemispheric differences 19, 191. Some papers report differential effects of adaptation to gratings depending on the field of presentation of the test stimuli 17, 10, 241. Other authors present data which question this view 1191. This negative evidence, however, may not justify the conclusion that the two hemispheres are equipotential in dealing with different spatial frequencies. As many authors claim, hemispheric differences may emerge beyond the sensory level of processing where more complex cognitive operations are performed. In her spatial frequency model for hemispheric asymmetry, Sergent also assumed that the “output from the visual sensory areas is similar in both hemispheres” 1211. However, the hemispheres differ in basing on high or low spatial frequencies in their cognitive operations. According to this view, testing for hemispheric asymmetry would require the use of discrimination or recognition rather than detection tasks. Using more complex patterns might also be useful. Differences between the visual fields in various detection and discrimination tasks for simple and complex sinusoidal gratings were investigated by FIORENTINI and BERARDI 161. The results of their study indicated absence of lateralization effects for detection and discrimination of simple gratings. There was, however, an overall left field

SCorrespondence

to be addressed

to Dr Anna Grabowska 259

or Dr Carlo Semenza

260

NOTE

advantage in the spatial-phase discrimination of complex gratings and detection ofa higher frequency componcn! of the gratings. A similar result, i.e. a left visual field (LVF) advantage for discrimination of complex gratmga, was obtained by RENTSCHLER et al. 1171. This finding would sugget that the right hemisphere i$ more elrective in processing complex gratings containing various spatial frequencies, at least when a sufficiently complex task is performed. The recent study by SZEL.AG et al. [23] revealed no hemispheric asymmetry for reaction time (RT) in a simple grating discrimination, whereas a right hemisphere superiority was observed when the number of errors was considered. This laterality effect. however, was present only when the two gratings to be compared differed in their spatial frequency. We attempted to examine possible hemisphericasymmetries in grating perception by testing patients with left and right hemisphere lesions. We expected that if one hemisphere is characterized by a higher competence in grating processing, its lesion should cause a stronger impairment in such perception than would a lesion of the other hemisphere. If the hemispheres are equipotential in dealing with grating patterns, there should be no difference in performance between patients with left and those with right hemisphere lesions. If, however, one hemisphcrc specializes in analysing high frequencies and the other in low frequencies, there should occur an interaction between the frequency of gratings and the lesioned hemisphere. In our experiment, we used a method of grating discrimination. To make the task more “cognitive” the subjects were not only to decide if two gratings in a pair were the same or different, but also to assess whether !he spatial frequency of one stimulus was higher or lower than the spatial frequency of the other. Moreover, we made the interstimulus interval rather long (2 set) since, according to MOKOVITCH [I 31, hemispheric effects are more evident in tasks involving memory. The exposure time (300 msec) was short enough to render it impossible for the subjects to apply the strategy of counting the strips but long enough for brain damage patients to fulfill the task.

METHOD Twenty-eight neurological subjects (I 6 males) with no evidence of cerebral involvement acted as a control group in this study. The experimental group included 19 patients with a lesion to the right hemisphere (10 males) and 24 patients (14 males) with a lesion to the left hemisphere. Age and educational level were comparable in all groups: the mean age was 42.5 yr in the control group, 45.3 in the right hemisphere group and 49.6 in the left hemisphere group. All patients were right-handed. Care was taken to accept only patients who showed a visus of at least S/IO in both eyes, with or without lenses. Among patients with left hemisphere lesions, none showed language impairment that prevented a full understanding of the test. The etiology of the diseases for the right hemisphere group was as follows, neoplastic in 15 cases, vascular in two cases and cystic in the remaining two cases. In the left hemisphere group, 15 patients showed a neoplastic pathology, seven were vascular, and one was a traumatic case. Four patients in each group had a clinically detectable hemianopsia. All neoplastic patients were tested preopcrativcly. No clear subdivision could be made within each group of brain damaged patients along the anterior/posterior dimension, since lesions often extended to both anterior and posterior regions. However, since the investigation of the anterior,‘posterior dimension was felt to be of great interest, patieuts were subdivided according to the prevalence of anterior or posterior involvement, considering also clinical signs such as basic motor and sensory deficits. This rough division led to a classification of six right hemisphere patients as anterior and I3 as posterior. In the same manner, 13 left hemisphere patients were judged to be anterior and 1 I posterior. Stimulus

material

and procedure

The stimuli consisted of square wave horizontal gratings of high contrast, each alubtending a circular area with a diameter of I4 Gratings in a pair were presented one after the other, each for 300 msec at an interstimulus intervai of 2 sec. The spatial frequencies of the gratings in a pair were either the same or slightly different, but clearly discriminable [4, IS]. Low (0.7 c/deg and 1 c;deg). middle (2 c,‘deg and 2.X cideg) and high (6 c;deg and 10 c:deg) spatial frequencies were used. To ensure that the position ofbars did not provide a possible cue to discrimination, all gratings contained a full number ofcycles (e.g. whole bars were visible at edges ofthe gratings). After presentation -?f each pair the patients were asked to judge whether the spatial frequency of the second stimulus was the same as, or higher, or lower than the first one. Response was verbal or gestural. The experiment consisted of two identical blocks, each containing 30 comparisons in random order. Within the block, each of the three different pairs reappeared eight tirnes. On half ofthe trials, the frequency of the first stimulus in each pair was !ower and in the other half higher than the frequency of the second one. Each of the six pairs of “same” stimuli appeared once in each block. The gratings were presented centrally on a screen placed 1.7 m away from the subject’s eyes, by means of Kodak Carousel projector equipped with a timer controlling the duration of the stimuli and the interstimulus Interval. Practice sessions preceded the experiment to familiarize the subjects with the procedure and to assure that the instructions were understood.

NOTE

261

RESULTS For each subject, the number of correct responses was calculated. Data for “same” and “different” stimuli were treated separately. In both cases an ANOVA was performed according to a two-way mixed design in which three levels of the between-subjects variable (controls, right, and left damaged patients) and three levels of the withinsubjects variable (high, medium and low frequency) were considered. The ANOVA for different stimuli yielded significant main effects ofgroup (F=4.53; df 2, 68; Pt0.05) and type of frequency (F= 12.30; df 2, 136; P
Middle

Low

X ___~

LH damaged RH damaged Controls

12.33 (3.29) 10.74 (3.93) 13.50 (2.59)

11.71 (3.07) 11.32 (3.00) 12.50 (2.17)

13.66 (2.44) 12.26 (2.98) 14.46 (1.83)

12.57 (3.03) 1 I .44 (3.33) 13.49 (2.33)

A second ANOVA with the same design was performed after dividing the subjects into five groups according to an anterior/posterior subdivision. In the analysis of “different” stimuli, significant effects of group (F= 3.30; df4,66; PcO.05) and type of frequency (F= 10.65; df2, 132; P-cO.01) were found. The interaction was not significant (F=0.85; df 8, 132; n.s.). Post-hoc analysis via the Neuman-Keuls procedure revealed no reliable difference between controls and left posteriors. These two groups differed from all the remaining three groups (PcO.05) who did not differ reliably from each other. Again no significant effect was found for “same” stimuli. As far as erroneous estimations were concerned, “same” instead of “different” was by far the commonest answer (88.8,59.2, and 89.8% of errors in C. RH and LH groups respectively), while “lower” instead of “higher” responses (5.1,6.9 and 5.3% of errors) and “higher” instead of “lower” responses (6.1.3.9 and 4.9% of errors) occurred only occasionally. These data indicate that our groups of patients did not differ considerably in their response strategy. Table 2. Mean number of correct responses (out of 16 exposures) obtained and four right hemisphere damaged hemianopic patients in discrimination middle, and low spatial frequencies (“different” s:imuli).

LH damaged RH damaged

High

Middle

Low

14.5 9.5

11.5 10.5

14.25 11.5

by four left of high,

X 13.4 10.5

In addition to the general analysis, special attention was given to the results obtained by eight hemianopic patients (four m each group). Table 2 gives the number of correct responses for the left and right damaged hemianopic patien:s. It can be seen that for all spatial frequencies patients with right hemisphere lesions performed worse than patients with left lesions, the difference being even more drastic than when comparing the whole groups of patients.

DISCUSSION The results showed an asymmetrical ability of the two hemispheres to discriminate gratings. The right hemisphere appeared to be more efficient in discriminating gratings of all spatial frequencies. Since the present experiment used

262

NOTE

only gratings as stimuli. it is difficult to conclude whether the impairment shown by the patients with right hemisphere lesions was due to a loss of spatial frequency discrimination per se or due to a more general impairment in processing of non-verbal, visual-spatial stimuli. It seems, however, that our findings have some implications for Sergent’s spatial frequency model for hemispheric asymmetry. If the left hemisphere specializes in analysing high frequencies and the right specializes in analysing low frequencies, there should occur an interaction between the frequency of gratings and the side of the hemisphere damaged. No such interaction was found. Sergent has never tested her model using gratings as stimuli. She derived her hypothesis from observations that different forms of degradation of percepiual quality of s!imulus, such as increased retinal eccentricity. reduction m energy and duration of stimulus, or its blurring impair the performance more when the stimulus is presented to the right visual field (left hemisphere) than when it is presented to the left visual field (right hemisphere). see 18. 211 for a review. It is possible that such manipulations which lead to loss in high frequency information also produce some additional perceptual effects which may separately influence the pattern of hemispheric asymmetry. The studies which used gratings as stimuli showed either no laterality effects or an asymmetry similar to our finding, i.e. a right hemisphere superiority [b, 231. It seems that our posltlve finding was due to the use ofa test v,ith more cognitive demands than simple contrast sensitivity, and to the use of patients as subjects. It appears that the task was comparatively difficult (short time of exposure, 2 set interstimulub interval. randomized presentation of three different frequency ranges, three categories of answers) because even the controls made mistakes in comparing gratings which differed to a degree considerably higher than the discrimination threshold 14, 161. The statistics involving the anterior versus posterior localization ofthe damage revealed that the groups blth left and right hemisphere lesion differed reliably from one another only when the lesion was posterior. The left posterior group behaved like the controls, while the right posterior group scored significantly lower than the two former groups. It seems. therefore, that the observed hemispheric differences are mainly connected with the posterior regions of the brain. This interpretation is strongly supported by the results of hemianopic patients whose visual cortex was damaged. Left hemisphere damage did not affect their performance. while right hemisphere damage yielded a considerable impairment in grating discrimination. The two anterior groups performed less proficiently than both controls and left posteriors, while they did not diflcr from each other. This finding cannot be neglected even though the anterior ~posterior division was tcntatibe and the number of patients in the four subgroups differed considerably. It seems that this finding can be related hith some disorders following damage to the frontal cortex of the brain. PKISCO [ 141. reported in MILVJ.R [I 1. 121. In her study, patients were presented with two stimuli in succession and had tojudge whether the second stimulus was the bame or different from the first. Patients with frontal-lobe lesions were impaired in that task. Similar disorders in the perception of temporally ordered stimuli were observed in patient.\ with frontal lobe damage by other authors [l2, 151. It can be assumed. therefore, that our frontal lesion patients could be at a disadvantage in a task demanding a comparison of two consecutive stimuli, even though the effect was unrelated to the side of the lesion. nckno~l,/rdymlrnt--The contribution of A. Grabowska to this study was supported by a training fellowshlp from the European Science Foundation!Europcan Training Programme in Brain and Behavior Research. The atudy was aIs,, supported by grants ofCNR to Unitii 14. Scienze del Comportamenta, and of Ministcro della Publica Istruzionc to C. Semenra and G. Denes.

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