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MARLENE OSCAR-BERMAN,2 HAROLD GOODGLASS, AND. DIANA GORENSTEIN CHERLOW. Aphasia Research Center, Boston Veterans Administration ...
Journal of Comparative and Physiological Pi 1973, Vol. 82, No. 2, 316-321

PERCEPTUAL LATERALITY AND ICONIC RECOGNITION OF VISUAL MATERIALS BY KORSAKOFF PATIENTS AND NORMAL ADULTS1 MARLENE OSCAR-BERMAN,2 HAROLD GOODGLASS, AND DIANA GORENSTEIN CHERLOW Aphasia Research Center, Boston Veterans Administration Hospital and Department o] Neurology, Boston University School oj Medicine Patients with Korsakofi's syndrome were compared to normal and alcoholic control subjects on their threshold for recognition of words or patterns presented monocularly to the lateral visual fields. The groups were then tested on backward visual masking of the same (target) stimuli to determine the ISI needed to escape the masking effect (critical ISI) in each lateral field. Threshold for recognition and critical ISI were elevated in Korsakoff patients. For all subjects, the right visual field was superior to the left for word recognition but not for pattern recognition. The critical ISIs were shorter in the right visual field for both types of material, suggesting that the dominant hemisphere is more efficient in the early (iconic) stages of information processing.

Current models of visual information processing and memory consolidation suggest that visual stimuli are mirrored in the nervous system for some milliseconds while the information is being categorized and converted into short-term memory (Atkinson & Shiffrin, 1968; Haber, 1970). The mirrored stimulus has been called an icon (Neisser, 1967); during "iconic memory" perception of the target stimulus outlasts its physical presentation. If a visual masking stimulus is presented in an appropriate spatial-temporal sequence following the appearance of the original target stimulus, perception of the target stimulus can be arrested. The ISI, or interval between target offset and mask onset, at which target recognition returns to premasking levels has been called the critical ISI by Kinsbourne and Warrington (1962); total processing time, however, includes the duration of the initial target presentation as well. It is assumed that the mask interferes with the 1 This study was supported in part by National Institutes of Health Grants NS-06209 to Boston University and NS-07615 to Clark University. We would like to thank Nelson Butters for his helpful comments, and MOB would like to express appreciation to T. S. Greatrex. 2 Requests for reprints should be sent to Marlene Oscar-Berman, Psychology Research, Boston Veterans Administration Hospital, 150 South Huntington Avenue, Boston, Massachusetts 02130.

processing of the icon either by fusing with it or by blocking it (Haber, 1970; Sperling, 1967; Turvey, 1970). In either case, the amount of time required for visual information processing can be manipulated and measured in the experimental paradigm of a visual backward masking situation. Since the encoding of material from iconic storage into short-term memory has a bearing on memory disorders, the masking situation was used for comparing the performance of patients with a neurologically based "memory disorder" (Korsakoff's syndrome; Talland, 1965) with that of neurologically intact subjects. Patients with Korsakoff's syndrome have been described as having an impairment of short-term memory (Brion, 1969; Talland, 1965). Such a description does not distinguish between the operations of recognizing or registering stimulus information and the operations of retrieving stimulus information from short-term storage. Since, theoretically, these operations can be impaired independently, we sought to assess the stimulus registration capacities of Korsakoff patients in the visual masking situation just described. Another purpose of the present experiment was to study the perceptual efficiency of the two cerebral hemispheres in dealing with verbal and nonverbal visual information. In man, the right visual field projects

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VISUAL PROCESSING IN KORSAKOFF PATIENTS to the left cerebral hemisphere and the left visual field projects to the right hemisphere. The traditional method of examining visual field differences has been to vary the amount of information in the target stimulus by varying its duration of presentation while allowing an indeterminate postexposure time for recognition to take place. It is assumed that information arriving in each visual cortex from the contralateral visual field is almost immediately shared, via the corpus callosum, with the visual association area of the other cerebral hemisphere (e.g., Gazzaniga, 1970; Mishkin, 1966; Sperry & Gazzaniga, 1967). However, interpretation of differences in recognition threshold between the lateral visual fields has involved the assumption that the information received directly from the contralateral field is more intact than that from the ipsilateral field, which is degraded by an extra step of transmission. In the present study we used that assumption, and we compared not merely the exposure threshold but also the critical ISI time required for information processing to take place in a backward masking situation (as described by Turvey, 1970, and Goodglass 1971). We also varied the type of visual material presented; a comparison was made of the processing time requirements for recognition of verbal and nonverbal materials presented independently in the right and left visual fields. With this method, then, we were able to compare the processing efficiency of the two visual fields for different types of materials, and we could assess the perceptual registration capabilities of patients with Korsakoff's syndrome. Whether or not processing times would distinguish Korsakoff's from control subjects, any perceptual laterality effects per se would be expected to be similar for all groups of subjects. METHOD Subjects There were three groups of right-handed subjects: a normal control group (NC), an alcoholic control group (AC), and a group of subjects with Korsakoff's syndrome (K). The NCs consisted of 19 Boston Veterans Administration Hospital staff members or neurologically intact hospital patients

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ranging in age from 19 to 50 yr. (X = 28 yr.). Eleven non-Korsakoff male alcoholic hospital patients, ages 36-50 yr. (X — 44 yr.), served as AC subjects; none had a clinically detectable memory deficit. The K group consisted of nine male patients, 42-66 yr. of age (X — 53 yr.), diagnosed by the neurology services of the Brockton and Boston Veterans Administration Hospitals as having Korsakoff's syndrome. The Wechsler Adult Intelligence Scale and three subtests of the Wechsler Memory Scale (orientation, digit span, and paired-associate learning) were given to the K patients to insure that their IQs and digit spans were within normal range. The etiology of the syndrome in eight of the nine Ks was malnutrition associated with chronic alcoholism; the ninth had suffered head trauma. Apparatus An Iconix three-channel monocular tachistoscope was used throughout the experiment. The distance from eye to stimulus was 42 in. The luminance of the target field was 7.5 mL. and that of the masking field, 11.3 mL., as measured with a McBeth illuminometer. Verbal stimuli consisted of 10 high-association three-letter words selected from the Thorndike-Lorge (1944) word book (frequency of occurrence at least 100 times per million in general reading material). The dimensions of each letter were 1A X '/4 in., and each word was arranged in a 1-in. vertical array. Nonverbal stimuli were 10 24-point computer-generated nonsense figures (Vanderplas & Garvin, 1959). The average dimensions of the figures were %e X 12/ie in- A choice card for identifying the figures by number was also constructed; the card contained all 10 figures, each having an identifying number. The masking stimulus for both the words and the forms was a 3/t X 1V4 in. checkerboard, with squares Ys X Vs in.; the mask appeared unilaterally, centered over the position of the preceding target. All stimuli were presented at 2.5° of visual angle to the left or to the right of the center of fixation. Procedure Threshold determination. Each subject was told to fixate with his left eye (as suggested by Overton & Weiner, 1966) on a dot in the center of the visual field and that 700 msec, later a word or a figure would appear to the right or the left of the fixation. The subject was told to report the word or identify the figure (by calling out its number) as soon as he could see it. A given stimulus was first presented at a subthreshold level; on succeeding trials the same stimulus was given with the presentation time increased by 1-msec. increments until the subject could identify the stimulus. Thresholds were determined for all the stimuli by this method of ascending limits. Order of stimulus presentation was randomized for field and type of material. Mean thresholds for words and for figures in both the right and left fields were computed. On five oc-

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casions the threshold for an item deviated appreciably from the mean (by a minimum of 90 msec.), and, therefore, it was not included in the data. Determination of critical ISI. In this phase of the experiment, each stimulus was presented for an interval of 10 msec, above the calculated mean .threshold for that type of material in the given hemifield. Presentation of the stimuli at a constant value above the threshold for each hemifield and type of material insured that differential field accuracy for masking would not reflect differential amounts of sensory input. The instructions were similar to those for threshold determination, except that the subject was told that the stimulus would be followed by a checkerboard pattern. The target stimulus was presented, and after a brief ISI the checkerboard mask came on for 50 msec, in the same visual field as the target. The method of ascending limits was again used; ISI time was increased by 5-msec. increments until the stimulus was identified (critical ISI). As with threshold determination, verbal and nonverbal materials and right and left field presentations were interspersed in a random sequence. Means in this phase of the study were determined for words and for figures, for each visual field. If the critical ISI for any item deviated from the mean for that material and field by 75 msec, or more, it was not included in the data. Processing times were computed by summing the mean threshold, the additional 10 msec., and the mean ISI times. Thus, processing times were computed for (a) words in the right field, (6) words in the left field, (c) figures in the right field, and (o!) figures in the left field.

RESULTS Since the mean ages differed among the three groups of subjects, we compared ranks of performance and age within groups on threshold and ISI measures, using the Spearman rank-order correlation test (Siegel, 1956). There were no significant correlations between age and time measures for TABLE 1 TOTAL PROCESSING TIMES (IN MSEC.) Words Group

Normal Alcoholic Korsakoff Overall

Patterns

Left field X

Right field

Left .field

Right field X

91.86 116.13 203.61** 137.20

80.54 96.43 166.70" 114.66

103.15 126.85 16S.73* 131.91

93.30 120.29 151.12* 121.57

Note. Significance levels indicate differences from control scores. * p< .05. ** p < .01.

any of the groups on either type of material with one exception: younger normal subjects had shorter ISIs for words than older normals (r = .58, p < .05). The NCs and ACs therefore were considered as adequate control subjects for comparison with K performance, and except where otherwise noted (and in the case of ISI-word measures) scores of the NC and AC groups together were compared to those of the K group using the Scheffe test (Edwards, 1960) following analyses of variance. Our results show increased processing time requirements by the amnesic patients (see Table 1). That is, patients with Korsakoff's syndrome required more time than control subjects to process visual information, both verbal (p < .01) and nonverbal (p < .05) and in either field of presentation (p < .05). In Figure 1 it can be seen that Korsakoff's recognition thresholds were higher than those of either of the other two groups (p < .05). Figure 1 also shows critical ISI requirements. The Ks required more time to escape the backward masking effect than did the NCs in every case except for form recognition in the left field (words left, p < .01; words right, p < .01; forms right, p < .06). ISI performance by the ACs fell between that of the other groups. Analyses of Group X Material interactions for threshold and ISI measures indicated that the Ks (relative to the controls) performed better with nonverbal than with verbal stimuli (p < .05). Our results also show expected laterality effects. In normal subjects, recognition thresholds were lower when words were presented to the right visual field than when presented to the left of fixation; the field differences were generally small but reliable (p < .05). This effect was present, although less consistently, in the alcoholic control group and in the Korsakoff patients (p < .10). With patterns as stimuli, recognition thresholds were not different for right and left visual fields. Perceptual laterality effects were not restricted to recognition thresholds; they were evident as well in the critical ISI requirements of the two fields. With words as stimuli, the ISI necessary for

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perception was shorter in the right field than in the left (NC: p < .05; AC: p < .05; K: p < .06). With patterns as stimuli, the ISI was shorter in the right field, but this effect reached statistical significance in normal subjects only (p < .05). Considering total processing time (mean threshold + 10 msec. + critical ISI), the right visual field evidenced superiority over the left regardless of the stimulus material employed. Mean processing times for the right field were 114.56msec. (words) and 121.57 msec, (patterns); for the left field, mean processing times were 137.20 msec, (words) and 131.91 msec, (patterns). In none of these measures was there any significant Group X Field interaction.

WORDS

PATTERNS

DISCUSSION There are two primary findings in the present study: (a) Amnesic (Korsakoff) patients have abnormally high visual-processing-time requirements, regardless of the field of stimulus presentation; and (b) for Right all subjects, the right visual field is superior Field Field to the left in processing visual information FIG. 1. Recognition thresholds (top) and critical (verbal or nonverbal) during the iconic interstimulus intervals (bottom) for materials prestage of information storage. to the left or right visual fields. (PerformSince Korsakoff patients have bilateral sented ance of Korsakoff [K] patients as compared to that cerebral damage (Barbizet, 1970; Brion, of alcoholic control [AC] and normal control [NC] 1969; Talland, 1965; Victor, Collins, & subjects.) Young, 1971), their perceptual laterality would be expected to be essentially un- visual information by Korsakoff patients, changed. Our results confirm that expecta- and the intermediate ISI performance by tion. We found, in addition, that Korsakoff alcoholic patients may be taken to indicate patients are slower than controls to process an incipient Korsakoff condition in these visual information; their recognition thresh- subjects not disclosed by standard clinical olds were higher than those of normals and evaluations. Furthermore, the finding that alcoholic controls, their ISI requirements Korsakoff patients performed better (relawere generally greater, and their total proc- tive to controls) with nonverbal than with essing times were abnormally high. Because verbal stimuli supports a recent finding by of the significant correlation between age- Butters, Lewis, Cermak, and Goodglass and word-ISI performance of normal sub- (1972)3 that Korsakoffs have a deficient jects, it might be argued that alcoholic sub- verbal encoding ability; improvement with jects constitute the only appropriate control nonverbal stimuli occurs because reliance group for this measure. However, that seems upon verbal encoding is minimzed. unlikely since performance of each of the Our results with Korsakoff patients do groups maintained the same relative posi- not support the previously untested astions on form-ISI measures (where there sumption that amnesic patients have "good were no significant age-performance corre*N. Butters, R. Lewis, L. Cermak, and H. Goodlations) . Rather, our data are interpreted as glass. Material-specific memory deficits in alcoholic indicating deficient iconic registration of Korsakoff patients. Unpublished manuscript, 1972.

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immediate registration of stimulus events" (e.g., see Ervin & Anders, 1970, p. 169). There is one experimental finding that an amnesic patient with hippocampal damage performed normally in a task of visual metacontrast (Milner, Corkin, & Teuber, 1968), but the discrepancy between our results and those of Milner et al. may be due to the procedural differences between masking and metacontrast tasks. In metacontrast, one target stimulus (usually a disc of light) is followed immediately by an annulus spatially surrounding the disc, and the subject must detect presence or absence of the target (typically by indicating its location in one of two positions near center field). In the backward masking task of the present study, subjects were required to identify each of a number of different target stimuli presented in either of the two lateral visual fields. Thus, our subjects were required to identify the target stimulus, not merely to report stimulus detection. As we have no data on a simple detection task, it is possible that our Korsakoff subjects, in a metacontrast situation, may have performed as well as Milner et al.'s subject. It is also possible that the discrepancy between our results and those of Milner et al. are attributable to differences in lesion location. The patient described by Milner et al. had hippocampal damage, whereas Korsakoff patients are thought to have diencephalic damage primarily (Barbizet, 1970; Brion, 1969; Talland, 1965; Victor et al., 1971). The extent to which the hippocampus is important for normal performance on our masking tasks would have to be tested empirically. In any case, our results show that Korsakoff patients require more than normal amounts of time for processing of visual information. These findings have important implications for studies where Korsakoff encoding or retrievel "deficits" may be confounded with inadequate stimulus input opportunity (especially where control and experimental subjects are given the same stimulus exposure times). Processing of visual information during the iconic stage of perception has been found here to be more efficient in the left

hemisphere regardless of verbal or nonverbal content. This phenomenon had not been observed previously with the conventional procedures of threshold determination. Dimond (1970) has reported in a reaction time experiment that the dominant hemisphere emerges superior to the contralateral one as signals are made more complex. In that experiment, when pairs of stimuli were directed to separate hemispheres (one signal to each of the heteronymous visual hemifields), reaction times were at their lowest values. Reaction times were greatest when both stimuli were presented to the same hemisphere (one signal to each of the homonymous hemifelds) and were even higher for the minor hemisphere than for the major one. Dimond suggests that the major hemisphere "as well as showing better response carries the principal burden of dealing with large quantities of fresh incoming information [1970, p. 617]." Likewise, in the present study, the dominant hemisphere emerges as superior when postthreshold information is read out from the stage of ionic storage for encoding in short-term memory, regardless of verbal or nonverbal stimulus content. REFERENCES ATKINSON, R. C., & SHIFFKIN, R. M. Human memory: A proposed system and its control processes. In W. Spence & J. T. Spence (Eds.), The psychology oj learning and motivation: Advances in research and theory. Vol. 2. New York: Academic Press, 1968. BARBIZET, J. Human memory and its pathology. San Francisco: W. H. Freeman, 1970. BEION, S. Korsakoff's syndrome: Clinico-anatomical and physiopathological considerations. In G. A. Talland & N. C. Waugh (Eds.), The pathology oj memory. New York: Academic Press, 1969. DIMOND, S. J. Hemispheric refractoriness and control of reaction time. Quarterly Journal of Experimental Psychology, 1970, 22, 610-617. EDWAEDS, A. L. Experimental design in psychological research. New York: Holt, Rinehart & Winston, 1960. ERVIN, F. R., & ANDEBS, T. R. Normal and pathological memory: Data and a conceptual scheme. In F. 0. Schmitt (Ed.), The neurosciences: Second study program. New York: Rockefeller University Press, 1970. GAZZANIQA, M. S. The bisected brain. New York: Appleton-Century-Crofts, 1970.

VISUAL PROCESSING IN KORSAKOFF PATIENTS GOODGLASS, H. Stimulus duration and visual processing time. Perceptual and Motor Skills, 1971, 33,179-182. HABEK, R. N. How we remember what we see. Scientific American, 1970, 222(5), 104-112. KINSBOURNE, M., & WARRINGTON, E. K. The effect of an aftercoming random pattern on the perception of brief visual stimuli. Quarterly Journal oj Experimental Psychology, 1962, 14, 223234. MILNEB, B., COBKIN, S., & TEHEES, H.-L. Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H. M. Neuropsychologia, 1968, 6, 215-234. MISHKIN, M. Visual mechanisms beyond the striate cortex. In R. Russell (Ed.), Frontiers of physiological psychology. New York: Academic Press, 1966. NBISSEB, U. Cognitive psychology. New York: Appleton-Century-Crofts, 1967. OVEBTON, W., & WEINEB, M. Visual field position and word-recognition threshold. Journal of Experimental Psychology, 1966, 71, 249-253. SIEQEL, S. Non-parametric statistics. New York: McGraw Hill, 1956.

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SPERLING, G. Successive approximations to a model for short-term memory. Ada Psychologica, 1967, 27, 285-292. SPEBBY, R. W., & GAZZANIQA, M. S. Language following surgical disconnection of the hemispheres. In F. L. Barley (Ed.), Brain mechanisms underlying speech and language. New York: Grune & Stratton, 1967. TALLAND, G. A. Deranged memory. New York: Academic Press, 1965. THOBNDIKE, E. L., & LOBGE, I. The teacher's word book oj 30,000 words. New York: New York Teacher's College, Columbia University, 1944. TUBVEY, M. Parameters of visual information processing prior to short-term memory. Paper presented at the meeting of the New England Psychological Association, Boston, November 1970. VANDEBPLAS, J. M., & GABVIN, E. A. The association value of random shapes. Journal oj Experimental Psychology, 1959, 57,147-159. VIOTOB, M., ADAMS, R, D., & COLLINS, G. H. The Wernicke-Korsakoff syndrome. Philadelphia: F.A.Davis, 1971. (Received February 10, 1972)