~rlcn,p,lrhok,y,o. Vol. 27. No Printed m Great Bnt.un
3, pp. 303-313. 1989
EVENT-RELATED
c
0028 393249 $3.00+0 CO 1989 Pergamon Press plc
POTENTIALS IN CHILDREN WITH SPECIFIC VISUAL COGNITIVE DISABILITY K. T. CIESIELSKI
Department
of Applied
Sciences in Medicine and Department of Pediatrics, University of Alberta. Edmonton T6G 2G3, Canada (Receired
Faculty
of Medicine,
15 July 1987: accepted 25 April 1988)
Abstract-Event-related potentials (ERPs) elicited by novel and well memorized non-verbal visual patterns were recorded over the right and left hemispheres from ten children with Specific Visual Cognitive Disability (SVCD) and ten matched Control subjects (C). ERPs of SVCD children were generally longer in latency (particularly N2) and decreased in amplitude (particularly P3) relative to the ERPs of Cs. No hemisphere differences were observed in the SVCD group, while the latency of N2 in the C group tended to be slightly shorter and the amplitude of P3 was significantly larger over the right than over the left hemisphere. The results are discussed in terms of deficits in visual learning and visual pattern analysis. The different hemispheric pattern in SVCD children as compared to Cs is suggested to be a symptom secondary to basic visual cognitive deficits.
INTRODUCTION
with specific visual cognitive disabilities (SVCD) constitute one of the subgroups of dyslexia “. . a disorder manifested by difficulty in learning to read despite conventional instruction, adequate intelligence and socio-cultural opportunity” [ 131. The heterogeneity of this disorder has frequently been blamed for the variation among experimental results [for review see 15, 521. Some classification systems for different subtypes of dyslexia have been proposed recently [2, 46, 551. The present experimental design addresses perception and perceptual memory abilities in children with difficulties in recognizing and reproducing complex or similar-to-each-other visual patterns, and who present a selective impairment of visual identification of words as gestalt patterns, reminiscent of dyseidetic dyslexia in Boder’s classification [3,4]. The visual perceptual and visual memory deficits in dyslexia have not received much research attention, despite the fact that dyslexia was initially described as a specific visual disability and labelled as “cognitive word blindness” [32]. The key question is whether children with specific visual disabilities (SVCD) have difficulties in discriminating visual patterns per se, or do they have difficulties in establishing a visual memory template, and hence, in the recognition of memorized forms? Will SVCD children reveal a pattern of brain functional specialization to visual processing different from that of Controls? To address these questions, visual event-related potentials (ERPs) were recorded over the parietal cortex from a group of children with specific visual disabilities and from a group of matched controls during perception of non-familiar and familiar complex patterns. The particular value of non-verbal visual-~spatial patterns is that they are specific to the visual cognitive disability and that they help to avoid the negative emotional,
CHILDREN
303
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K. T. CIESIELSKI
motivational and attentional attitudes which dyslexics often demonstrate to written verbal tasks. ERPs provide insight into cerebral processes involving attention, perception and memory, and offer an excellent opportunity to investigate human information processing at levels where the anomalies ofcognitive disorders originate [60]. No visual ERP research in the subpopulation of children with specific visual disabilities and reading disorders could be found in the literature; that was surprising considering that late, cognitive brain potentials (N2 peaking at approx. 20&300 msec and P3, peaking approximately between 300-400 msec) have been described to reflect human brain activity when subjects attend to visual stimulation [28, 291. The latency and, in some circumstances, the amplitude of parietooccipital negativities within the N2-latency range varies with spatial frequency, orientation of the visual pattern [29], physical discriminability between stimuli [24, 611, perceptual complexity of the stimulus [Sl] and hemisphere specialization [7, 10, 301. Distinct components have been differentiated within the N2 latency range [42, 471. The most elaborated distinction is between the N2 mismatch negativity and the processing negativity [for review see 381. N2 mismatch was isolated by NAATANEN et al. [38,40] from the N2 or N2-P3a complex [59] and described as elicited by a physically deviant event in a homogeneous repetitive stimulus sequence. It appears to be independent of attention and stimulus content and reflects a genuine, automatic comparison process [41]. The second negative, modality unspecific component, N2b, is superimposed on the N2 mismatch. The N2b occurs when the stimulus input is attended to. It forms a wave complex with the positive component P3a. Another component described as reflecting the integrative processes occurring between the sensory input and the content of the working memory is the sensoryspecific processing negativity emerging in selective attention tasks [38]. It has been suggested that this processing reflects attentional selection of stimuli for further processing, a selection based on certain pre-set physical stimulus criteria, that are stored and maintained in the working memory. Such storage NGTLNEN termed the “attentional trace” [39]. The processing negativity is, according to him, an on-line reflection of a comparison process between the sensory input and the attentional trace, relatable conceptually to the stimulus-set mode ofattention described by BROADBENT[S]. In such context the processing negativity is of particular relevance to the present study. The classical P3 has been described to be dependent strongly on psychological stimulus content [.59] and is associated with stimuluscategorization [ 12, 191, template matching [31] and memory updating processes [19]. Considering the above, N2 and P3 were selected as the components of interest for this study, to be measured over the parietal scalp. ERPs from sites over the parietal cortex have been reported to be involved in visual-spatial pattern discrimination [45,58,62] and abnormalities in these ERPs have been consistently found in children with reading difficulties [21]. Numerous studies on undifferentiated dyslexics report abnormality of ERPs over the left cerebral hemisphere [9, 25, 493. Most of these studies used stimuli that were verbally mediated, and therefore presumably were specific to the left posterior brain. It is important to determine whether the left lateralization of abnormal responses reflects the abnormal processing of language mediated stimuli only, or if it points to an abnormal mechanism of information processing in general. If there is a general abnormality in visual information processing, the abnormality should occur with non-verbal as well as verbal material. Nonverbal amoeboid patterns, derived from the material developed by NEVSKAYA [43] at the Pavlov Institute were chosen for the present study. An initial study using these patterns with normal adults [7] showed right parietal lateralization of the late N2 component only when
ERPs IN CHILDKEPU‘
WITH
305
SVCD
the reaction to non-verbal stimuli was overlearned but not when the task was one of simple perception [S]. It has earlier been shown in normal adults that with practice the major interference in stimulus processing can be greatly reduced and the time leading to recognition shortened [22,48, 561. Reduced response time can result in decreased ERP latencies, since there is a positive correlation between Rt and N2 latency [SO]. Whether the SVCD children would show the pattern of ERP for unfamiliar and for memorized patterns as is expected in normal subjects, is an empirical question. Special care was taken to minimize behavioral factors which could confound the ERP data and contribute to the group differences, notably by choosing a simple visual perception task and by using pre-experimental training until both groups (SVCD and C) were equivalent in the speed and accuracy of performance. There are, therefore, two major empirical questions in this study: (i) does the neural mechanism of visual discrimination for novel and well memorized non-verbal patterns, as measured by ERP recordings, differ between SVCD children and control subjects and (ii) is there evidence in SVCD children of incomplete functional specialization of the brain for nonverbal patterns. METHOD Subjects
Ten children with specific visual cognitive disabilities (SVCD) between the ages of 8 and 15 (mean of 12) were selected from the outpatient population of the Manchester Clinics in England using standard psychometric techniques [WISC, 63; Neale Analysis of Reading Ability, 44; Harris Test of Lateral Dominance, 27; selected tests from Halstead-Reitan battery]*. Each subject evidenced reading retardation at least 18 months below the child’s age norm [54] and had been classified as dyslexic with specific visual cognitive disabilities. There was a preponderence of reading and spelling errors in their reading that reflected poor visual but good phonetic analysrs. Errors include phonetically accurate misreadings of words (e.g. “hat” or “hurt” for “heart”); misplaced stress in phonetic word (e.g. “a-ni-mal” for “animal”) and letter and word reversals. Following Boder’s classification these children could be labelled as dyseidetics [4]. The control subjects (C) were selected from the Manchester school district and matched with the experimental group on the basis of age, sex, handedness and overall intelligence levels. The control subjects, however, were not retarded in reading (i.e. no more than 4 months below age norm) and had no familial history of dyslexia. All participants had normal intelligence (IQ >90, were right-handed (with three individuals in each group having left-handed first degree relatives)and had normal or corrected-to-normal vision. Children with peripheral visual or auditory deficits, or histories of neurological, emotional problems and histories of hyperactivity were excluded. There were eight males and two females in each group. It should be noted that there was no control group of subjects matched on the basis of their reading level, as the present paradigm did not use verbal reading material, but rather required empirical matching based upon equivalent levels of performance in the experimental visual-spatial task. Stimuli The stimuli consisted of six amoeboid shapes similar to each other in complexity and perceptual discriminability. Examples of such patterns are shown in Fig. 1(a). Stimuli were projected for a duration of 66 msec on a 30 x 30 screen as white figures (4.3 cd/m’) against a dark background (I.8 cd!m2) in blocks of 32 trials. Within a block, there were eight trials of the target amoeboid figure, and 24 trials of the non-target figures (25% targets and 75”/, non-targets). The figure spanned 40’ visual angle horizontally and 1 15’ vertically. The stimuli were presented 3 30 to the left or right of a red LED that served as a central fixation. Procedure
Subjects participated in one introductory session and two ERP-recording sessions. During the Introductory session the child was trained in the task described below. After training, the error rates in both groups were on average 889% and reaction times (RTs) averaged 70&950 msec across subjects: there was a similar distribution of RTs within each group. The stimuli used during the initial training were similar but not identical to those used in the recording sessions. In front ofeach subject there were three response buttons arranged in a vertical line: BI, B2 and B3 [as illustrated in Fig. l(b)] The picture of the target stimulus was placed above button Bl. The subject’s right forefinger rested
*The results of detailed
neuropsychological
assessment
are to be reported
elsewhere.
K. T. ‘&XL
(a3
LSKI
Ib3
A
831
0
FIG. I (a) Examples of non-verbal amoehoid patterns. B. dashed lines show elements of the pattern whxh were used for assessing the correctness of pattern reproduction during the training session. (b) The response table with three buttons BI, B2, B3 and the target pattern placed in front of the BI button.
betncen BI and 82, and the left forefinger between B2 and B3. All stimuli required simultaneous button presses with both forefingers. Whenever a target was presented. each subject was required to move both forelingers forward to press Bl and B2. In contrast, whenever a non-target has presented. each subject was required to mobe both forelingers backwards to press 82 and 83. Each subject sat in an armchair in a dimly lit room m front of a screen with his head supported. Eye movements tierc monitored via a specially designed glass frame with an infrared detector [I]. Trials contaminated by eye movements were discarded. First. each subject was asked to concentrate on the pattern placed on the response table. then to lixatc red light (LED) in the center ofthe screen. Following a warning click (3 5 set preceding presentation) the Subject was instructed to focus his eyes on the LED while the pattern was presented randomly to the right or left visual held. His task wits to slide his two forefingers forward as quickly as possible when the target was presented, and backward when a non-target was presented. The inter-trial intervals were about 20 sec. For the first ERP recording session. three stimuli were designated as targets and three as non-targets. The target and non-target were pared so that a given target was always presented with the same non-target. Each subject received 32 stimulus presentations of a given targct,‘non-target pair. Each block of 32 stimuli cons&cd of 4 target and I2 non-target stimuli for each ofthe left and the right visual field. presented in random order. After each block. a ncu turgct!nontarget pair was introduced. To ensure that onI4 the wavcforms collected during the performance of assigned tasks \*erc included in the data. ERP waveforms were averaged onI4 after four consecutive correct response\ here obtained four times. Each averaged brain wave for each subject was the average of I6 raw waveforms. At the end ofthc first ER P recording session, each subject wah required to memorire two randomly chosen shapes from the SIX used previously. The trainmg procedure Involved short presentations of a pattern which the subjects were required to draw from memory. Presentations were repeated until each subject was able to reproduce the ligurc correctly twenty consecutive timea. The criteria for correct reproductions were the correct number of element5 withln the ligurc and their relative six (see Fig. I (a)B). It has to be noted that some children on occasions attempted to associate the patterns with familiar pictures of animals or herds. After learning both patterns. each sub_jcct was Inrtructcd to review them several tlmcs daily in anticipation of the next cxperimcntal session. The second FRP session was held 6 daya after the first. At the bepmning ofthis session, each subject v,as asked to draw the previously learned patterns. If they were unable to do so. the experiment LC:L~ terminated and the auhjcct replaced (two SVCD children and three control5 wcrc excluded). The procedure ofthc second xssion \%as essentially the same as that in the first. ewccpt that the target and non-target pattern\ were used only from among the previously mcmorircd pair of patterns.
Silver silver-chloride cup electrodes were placed at 1’3 (left parietal I and P4 (right parietal) according to the IO 20 \\i\tern L34]. and hcrc referenced to linked earlobe electrodes. The parietal scalp distribution of the N? and P3 responses to the identical task in\olvlng amoeboid shapes has been estahllshed previously 177. Because 01 equipment limitations. recordings could only he recorded from two channels at a time. Stimuli were randomlq presented to both visual fields from trial to trial. Sixteen haveforma to target hits wcrc averaged In each visual lield. Brain Ggnalr were amplified with Fylde Electronic Amplifers with a frequency band 0.7 30.0 Hz and averaged (I6 wa\cforms per trial) hj: a Mcdelec Averager. Ideally one would used a wider frequency band (e.g. 0.1 30 Hz) than the prcscnt one, to avoId diatortlons of P3 amplitude [IX]. Howc\er. as the conclusions in this study are based on comparison bct\\ocn difliircnt euperlmental conditions uhich were equally affected b> the shorter time constant and as this htudy does not pertain to description ofthc nature of individual components. such posslhle distortions due to the high-pass cut-off of the amplifiers do not Intlucnce the major lindtngs of the study.
ERPs IN CHILDKFY
Wll’H
307
SVCD
Only ERPs elicited by correct recognitions were analyzed. Two components were selected for analysis: N2 (peak latency between 16&400 msec) and P3 (peak latency between 290-500 msec) (Fig. 2). These component\ \+crc measured by two independent judges blind to the experimental conditions. The amphtudes for each of thcsc components were obtained by peak-to-peak measurements of the distance along the voltage axis bettieen the peak of the preceding component and the measured peak. Table I shows mean latencies and amplitudes for N7 and 1’3 in both groups of subjects
SVCD
Control
Subject
CK
13Y
FT
UFT
FT
Famlllar
UFT
Unfamllfar
RIghI
Targets
Let!
Targets
Hemtsphere Hemisphere
FIG. 2. Cognitive event-related responses (ERPs) [or a representative subject during direct stimulation of the right (dashed line) and left (solid line) hemtspheres recorded durtng discriminatton of the familiar (FT) and unfamiliar (UFT) targets. The components were measured peak to peak. The midpoint in each component was selected as a mark for peak ampliiude and peak latency reference.
Table 1. Mean latency and amplitude for N2 and P3 recorded over the left (LH) and right (RH) hemispheres during presentation of well memorized, familiar patterns (Familiar) and unfamiliar patterns (Unfamihar)
Unfamiliar La LH N2
SVCD Children targets Familiar Am La
targets Am
Unfamiliar La
Controls targets Am
Familiar La
targets Am
286 (50)
4.3 (1.8)
291 (52)
4.2 (1.0)
234 (32)
5.3 (1.8)
220 (27)
6.1 (I.31
284 (56) 401 (37)
3.9 (1.6) 6.3 (2.6)
281 (42) 406 (35)
3.9 (1.3) 6.4 (2.5)
229 (35) 352 (42)
5.4 (1.7) X.0 (2.5)
71 I (30) 347 (47)
6.X (1.7) (3.4)
400 (38)
6.0 (2.2)
398 (33)
6.3 (1.3)
350 (44)
9.4 (3.9)
337 (45)
12.6 (3.8)
’ RH LH
IO.9
P3 RH
LH, left hemisphere;
RH, right hemisphere;
La, latency:
Am, amplitude
RESULTS Group effects Data were analyzed by profile analysis for two independent groups as described in Morrison [37, pp. 153.-1601. The accepted level of significance was 0.05. Three hypotheses
308
K. T. CIESIELSKI
are tested using this technique: (i) a test of parallelism of the profiles, i.e. is an interaction present? (ii) a test of mean levels (equality of means), i.e. do the groups differ in overall level of responses, (iii) a test of equal condition levels, i.e. a test of differences across conditions (e.g. familiar vs unfamiliar targets). Table 2 presents the results of profile analysis. Significant interaction was observed only for P3 amplitude by group of subjects [F (3, 16)= 3.5, P
Factor
for two independent
Factor by group interaction
groups:
SVCD children
Tests Differences between levels of responses in groups*
and Controls
Differences across conditions: Familiar-Unfamiliart
F(3, 16)~2.9
F(1. 1X)=8.9:
F(3, 16)=2.3
N2 latency
F(3, 16)=2.1
F(1, 18)=16.4$
F(3, 16)=3.7$
P3 amplitude
F(3, 16)=3.5:
F(1, 18)= 12.7:
F(3, 16)=3.6:
P3 latency
F(3, 16)=0.4
F(1, 1X)= 10.2$
F(3. 16)=2.0
N2 amplitude
*Levels = the average of the response across conditions. This hypothesis is analogous to the test of overall group differences in the analysis of variance. tThis hypothesis is analogous to the repeated measures factor in the analysis of variance. IStatistical significance on at least 0.05 level.
lJnfamiliar-;familiar
task effects
Unfamiliar task differences were examined within each group of subjects independently using paired r-test ([37] pp. 141-143). The significantly shorter N2 latencies for familiar task than for unfamiliar were observed within the left and right brain hemispheres for Controls (L:t=-3.37; D=-18, PcO.005; R:t=-4.39, d-18, PO.O5; R: t=0.28; d=2.5,P>O.O5);(drepresents the mean difference between conditions; df=9 for all results). N2 amplitude of Controls was also found to be higher for familiar than unfamiliar task when collected over the right brain (t = 3.44, d = 1.55, PO.O5;R: t=0.35,d=0.30, P>O.O5).
ERPs IN CHILDREN
Left-right
WITH
SVCD
309
difSerence
Left-right hemisphere differences within each group were examined using paired t-tests ([37], pp. 141-143). Significantly higher mean amplitudes (see Table 2) over the right brain than the left were observed for P3 amplitude in Controls (t = - 4.6, d = - 1.7 P < 0.001) when familiar stimuli were perceived. It was not the case for SVCD children (t = 0.56, d = 0.50 P>O.O5). The L-R differences for N2 and P3 latencies were approaching statistical significance pointing towards shorter values over the right brain than the left, again in the task with familiar stimuli (N2: t = 2.7, 0=4.5, P=O.O57; P3: t = 2.1, d= 10.0, P=O.O6). There were no signs of such trends in SVCD children either for N2 latency (t = 0.77, d = - 55, P>O.O5) or P3 latency (t = 1.2, d = 7.5, P>O.O5). No other significant L-R differences were observed.
DISCUSSION The major finding in the Control group was the effect of familiarity of patterns reflected in the shorter N2 latencies and larger P3 amplitudes for familiar than for unfamiliar targets. The trend to cerebral dominance in Controls is reflected by shorter N2 and P3 latencies, and by higher P3 amplitudes over the right scalp than the left. The ERPs of SVD children in comparison to normal controls revealed: (i) longer latencies particularly for the N2 component, (ii) lower N2 and P3 amplitudes, (iii) no differences in latency or amplitude as a function of stimulus familiarity and (iv) no evidence of a lateralization effect. It is important to note that SVCD children and Cs elicited different evoked responses although, for both, recordings were taken only to correctly recognized stimuli; thus the ERP group differences support the view that the efficiency of neurophysiological processing of visual-spatial patterns could be different in children with specific visual disabilities and reading deficits than in normal reading children [6]. It has been suggested that the visual perception of dyslexic children and good readers differ in the extent to which their performance is automated. For example, LABERC;Eand SAMUELS [36] have suggested that in stimulus naming, dyslexic children need to invest a larger share of processing capacity to task performance than control children. Insofar as less automation of visual recognition processes leads to the decreased availability of selective attentional resources in dyslexic readers, this hampers their efficiency in determining the imperative features of the figures and coding them into a memory template. This lower degree of automation may be reflected in lower recognition confidence which in turn has been shown 1.0be related to decreases in P3 amplitude 116, 331. While considering the significance of generally longer N2 latencies in SVCD children, it is worth noting that N2 has been described as a component which relates to visual pattern feature discrimination in normal subjects [7,10,29]. Thus, one may speculate that the longer latency of N2 in SVCD compared to C children may be related to a difficulty in pattern feature discrimination and interpreted as reflecting the abnormality of processes involving the selection of stimuli on the basis of pre-set physical features (see description of processing negativity by N~;~T;~NEN, [39]). One possible explanation of such deficiency is derived from GIBSON’S work [26] on the selectivity of visual pattern perception. In particular, Gibson found that correct and effective pattern recognition in children depends on an ability to utilize the imperative properties of figures. In the context of the present study, this suggests that SVCD children may not extract the most important pattern features but, instead,
analyse ail features whether or not these are important for final pattern categorization. Such redundant analyses of features require more time, and may result in difficulties in forming a selective (in terms of features) short-term “attentional trace” [39] needed for comparison with a stimulus template. Hence, the prolonged N2 latency may relate to less efficient processing and a higher degree of perceptual difficulty with the stimulus. This interpretation of the delayed N2 in SVCD children is comparable to and consistent with the extended N2 latencies elicited by more complex visual patterns in normal adults [SO]. Considering that the cognitive nature of N2 and P3 is still in scientific dispute, the above conclusion should be kept in mind as a useful working hypothesis. With practice the recognition of well familiarized objects becomes more automatic, identification of features becomes parallel and shorter processing time is required than for the initial perception ofnon-familiar objects 123,561. It is tempting to speculate that the increase in P3 amplitude and some decrease in its latency observed in the right hemisphere for Control children as a function of pattern familiarity may reflect this tendency to change from serial processing of visual sensory information to more parallel, global processing [S]. This mode of processing has been previously described as predominant in the right hemisphere [ 171. Such effects of learning were not observed in SVCD children: their ERP latencies and amplitudes do not differ as a function of stimulus familiarity. Ifthis line of reasoning is correct it suggests again a possible failure in selecting the imperative stimulus features and in applying them to develop a parallel and thus more effective model of information processing. DONCHIN et al. 119,201 have proposed that P3 reflects an updating of working memory, and that events that elicit larger P3 are remembered more effectively than events that elicit smaller P3. COURCHESNE [ 11, 121 suggested that parietal P3 was related to the processing of stimuli that have readily available categories or categorization schemds. Perhaps, therefore, the differences in P3 amplitudes between new and trained patterns predict the integrity and strength of the memory template. The increased amplitudes of P3 with pattern familiarity in our Control population is consistent with this view of P3. The absence of this effect in SYCD children may be related to deficit in their memory updating as a consequence of their perceptual dithculties. Decreased P3 has been related elsewhere to less effective memory coding due to the difficulty in selecting the imperative stimulus cues [53] and with stimuli that are less discriminable 1541. There was a different lateralization pattern of results for P3 amplitude in both tested populations. While the Control group showed an increased P? amplitude to familiar stimuli over the right hemisphere, such an effect was not observed in the SVCD group. This may suggest an incomplete right hemisphere specialization for visualLspatia1 patterns in SVCD children which is consistent with other data on the sub-group of dyseidetic dyslexics [ 14,571. DALRY and GIBSON [ 143 showed that dyseidetic dyslexics display bilateral representation for verbal functions, and right lateralization for spatial functions. According to their results, this sharing of space in the right hemisphere for verbal and spatial functions may decrease its efftciency. The former can not be verified in the present work as verbal material was no1 used. It would be particularly valuable for clinical purposes to develop research on brain lateralization using experimental paradigms that elicit the N4 component 1351, which has been shown to reflect semantic visualLverba1 processing. The present study suggests as a working hypothesis, that children with specific visual cognitive disability, leading to reading disorders, may have a basic right-hemispheric impairment in selective information processing of the imperative features of con~plex visual patterns. Such difftculties can lead to less effective visual memory cuding. Within this general
ERPs IN (‘HILDKEN
WITH
311
SVCD
framework, incomplete brain lateralization of SVCD children considered secondary to more basic visual cognitive deficits.
relative to controls
could be
Acknowledgements--This work was supported, in part, by the grant from the Faculty of Medlcinc. IJntvcr\jty. of Alberta. I am indepted to the Department of Ophthalmic Optics University of Manchester. England. for provldlng me with research facilities. I thank Eric Courchesne. Robert ElmasIan, Marta Kutas and Dona Carlson for their caluable comments.
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