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Maturational changes in ERPs to orthographic and phonological tasks
Electroencephalography and clinicalNeurophysiology, 88 (1993) 494-507 © 1993 Elsevier Scientific Publishers Ireland, Ltd. 0168-5597/93/$06.00
494
EEP 92192
Maturational changes in ERPs to orthographic and phonological tasks Margot J. Taylor Divisions of Neurology and Neonatology, Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, Ont. M5G 1X8 (Canada) (Accepted for publication: 19 July 1993)
Summary Childrenfrom 7 to 18 years of age (divided into 2 year groupings, i.e., 7-8, 9-10, etc.) and young adults were studied (total of 84 subjects). ERPs were recorded from 19 electrodes during 2 visual oddball tasks: an orthographic task requiring responses to letters with a closed loop (e.g., a, p), and a phonologicaltask, requiring responses to letters that rhymed with 'v' (e.g., c, p). N2 and P3 peak latencies and amplitudes were measured on the difference potentials. RTs decreased with age and between tasks (orth < phon). N2 and P3 latencies decreased with age and were shorter for the orthographic than phonologicaltask. P3 amplitude was lower for the phonologicaltask; the cortical distribution varied significantly as a function of age and task. The task differences in distribution were more marked in the younger age groups. Hemispheric asymmetries in P3 amplitudes were seen in the phonological task. The orthographic task required simple visual feature recognition and the phonological task required a visual-to-auditory translation. The interaction effects suggest that cortical utilization differs for these tasks, with greater age-related changes for the phonological task.
Key words: Event-related potentials; Maturational changes; Orthographic task; Phonologicaltask; N2; P3
Event-related potentials (ERPs) are a sensitive means of assessing the timing and cortical utilization of cognitive processing, and as such offer a valuable means of studying cognitive development and underlying neurophysiological changes. A number studies have shown significant maturational changes in the ERPs that have been related to cognitive development (Courchesne 1983; Mullis et al. 1985; Robaey 1987; Taylor 1988; Johnson 1989; Ladish and Polich 1989; Stauder et al. 1990), associated with various types of cognitive processing such as memory span (Polich et al. 1990), or the development of reading skills (Taylor 1988). Most of these studies show gradual maturational changes in the ERPs, suggesting quantitative changes in cognitive processing with age. Reading appears to be a gradual or continuous acquisition of a skill, without the cataclysmic changes seen in some other aspects of cognitive development. There is some discussion in the literature as to whether children's performance on various reading-related tasks depends upon a general developmental trend in perceptual and attentional abilities (e.g., Walley et al. 1986) or whether specific abilities such as phonemic segmentation depend upon language training (Read et al. 1986; Kirtley et al. 1989). Clearly, both visual and
phonological processing of words and letters is critical to reading. Gattuso et al. (1991) found that phonemic skills were not related to children's ability to attend to aspects of a visual stimulus, suggesting that the two types of cognitive processing were not tied to a single underlying developmental trend. This leaves open the possibility of differing maturational patterns in these tasks. Processing of phonemic information or phonological awareness is, however, very closely tied to children's reading ability (Kirtley et al. 1989; Gattuso et al. 1991), and certainly visual identification of letters is basic to the reading process. Studies with adults have shown that ERPs index differential processing as a function of orthographic or phonological features of stimuli (Polich et al. 1983; Loverich et al. 1986; Rugg and Barrett 1987). Loverich et al. (1986) recorded ERPs in 10 adults from 11 electrodes overlying the left hemisphere. They found topographical differences between orthographic and phonological tasks that used single letter stimuli. Although both tasks had posteriorly located components, there was more of an anterior spread for the phonological task. They suggested that this was due to the visual-to-auditory conversion necessary for the phonological task, which would require cortical involvement
MATURATION IN ORTHOGRAPHIC AND PHONOLOGICALTASKS closer to the auditory regions. There was not a significant latency shift between the two tasks, suggesting that the speed of processing was equal (although there was a tendency for longer latencies in the phonological task). Other studies that have investigated orthographic and phonological aspects of visual language processing have used word stimuli, that are spelled similarly or not, that rhymed or not. Polich et al. (1983) also did not find significant latency differences between ERPs to visual versus rhyming tasks. Rugg (1984) and Rugg and Barrett 1987) have reported a series of studies using rhyme judgments, that show hemispheric asymmetry (R > L) in a negativity at 450 msec, seen to non-rhyming words. Although there are a number of behavioral studies suggesting increasing hemispheric lateralization in reading tasks with age (e.g., Bakker 1981), only a few E R P studies have found asymmetries with reading tasks developmentally (Licht et al. 1988). As ERPs are often more sensitive measures of cognitive processes than are behavioral measures, it might be expected that they would index developing hemispheric asymmetries, given appropriate tasks (Rugg et al. 1986). Reliable hemispheric asymmetries have been reported in adult studies from several centers (e.g., Kutas and Hillyard 1982; Rugg 1984; Neville et al. 1986), with the asymmetry shifting with the task. The orthographic and phonological tasks used by Lovrich et al. (1986) would be suitable for use with children, as young children learning to read know their alphabet and phonemes (Mann 1986). These two tasks also assess different aspects of cognitive processing that precede reading: visual and phonological encoding of letters. We would expect both to show developmental changes, but that these would be less marked in the orthographic task, as simple visual discrimination matures very early, whereas phonological encoding undergoes rapid maturation over the early school age years. The adult studies suggest that there would also be distributional differences in these two tasks, and given the differing maturational patterns, it was expected that these would show task-
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Fig. 1. Grand average ERPs at Oz to target and non-target stimuli in the orthographic task for the 7 age groups. Clear target/non-target
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TABLE I Mean values for the two tasks by age. Age 7- 8 9-10 11-12 13-14 15-16 17-18 Adult
N2 latency(msec)
P3 latency(msec)
Orth
Phon
Orth
Phon
RT (msec) Orth
Phon
P3 amplitude (mV) Orth Phon
422 5:37 408 _+38 352 _+43 360 _+25 332 _+25 323 _+36 337 5:31
542 _+46 475 _+70 414 _+48 434 _+40 374+ 61 356_+38 385 5:53
641 _+38 643 _+32 571 _+44 553 _+40 530_+52 514_+39 482+ 43
766 _+56 682 _+51 638 _+53 649 _+49 587 _+25 567 _+53 543 5:49
781+ 98 703+ 83 637_+ 66 540-+ 53 5725:128 516_+ 69 524_+ 59
1002+114 798+126 792-+ 147 721_+ 98 679 5:140 657_+126 620_+ 56
7.8+10 10.5±12 12.3-+ 16 11.1_+12 10.5_+ 8 8.0_+ 8 6.5 _+ 6
1.6_+ 8 7.7_+ 9 9.6-+ 11 9.8_+10 4.6_+ 6 10.0_+ 7 4.7_+ 7
496
M.J. T A Y L O R
specific age-related changes. Thus, the present study recorded ERPs in subjects from 7 to 30 years of age in these two reading-related tasks, to investigate the rela-
Orthographic Task
tive maturational pattern of these tasks via ERPs, and possible distributional differences as a function of task a n d / o r age.
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MATURATION
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PHONOLOGICAL
Methods
Subjects Children aged 7 - 1 8 years of age (divided into 2 year groupings: i.e., 7 - 8 (7.1-8.5, m = 7.98 + 0.49 years, n = 12), 9 - 1 0 (9.0-10.5, m = 9.68 + 0.54 years, n = 10), 1112 (11.1-12.8, m = 11.84 + 0.60 years, n = 14), 13-14 (13.0-14.8, m = 13.8 + 0.77 years, n = 12), 15-16 (15.0-16.9, m = 15.8 + 0.68 years, n = 10), 17-19 years (17.3-19.4, m = 18.4 + 0.68 years, n = 10)) and young adults (20-30 years, m = 26.6 + 2.1, n = 16) (total of 84 subjects) were studied. The male:female ratio was 40:44 and the ratio was balanced within age groups. None had a history of neurological or psychiatric disorders, and the children were performing appropriately for their ages in school. Subjects had normal or corrected to normal vision. All subjects spoke English as their first language. All subjects would have exposure to French as a second language; French fluency was not assessed.
Procedure ERP recording. E R P s were recorded using a P D P 11/73 system from 19 electrodes (Fpz, Fz, Cz, Pz, Oz, F3, F4, F7, F8, C3, C4, P3, P4, T3, T4, T5, T6, O1, 0 2 ) using a balanced non-cephalic spine-to-clavicle reference pair. The electrode impedance was always below 5 kO. E O G was monitored with two electrodes, placed at the outer canthus and on the supraorbital ridge. The E R P s were recorded with a bandpass of 0.1-30 Hz and a 1.5 sec sweep, starting 50 msec prior to stimulus
TASKS
497
presentation. All trials in which E O G or E M G artifact exceeded 90% of full-scale deflection were automatically rejected. The rejection rate decreased with age, but did not vary w i t h task. Tasks. Two tasks were run with each subject, the order of presentation varied across subjects. Two semantic tasks were also run and will be presented separately. In the orthographic task, lower case letters (visual angle = 0.8 °) were presented one at a time and targets were those which had a closed loop as part of the configuration (i.e., a, b, d, e, g, o, p, q). In the phonological task, the same stimuli were presented but the targets were letters that rhymed with ' v ' (including v; i.e., b, c, d, e, g, p, t, v). The letter 'z' was not presented in this task as it was considered an ambiguous stimulus, since its pronunciation varies. Stimuli were presented using a Macintosh computer for 0.2 sec with a 2.5 sec interstimulus interval. Target and nontarget stimuli were randomly interspersed, with targets occurring with a probability of 20%; subjects pressed a button to the designated target stimuli. Subjects made the button press with their dominant hand; 9 were left-handed, 1 or 2 in each age group, except 7 - 8 year olds. There were short breaks of 2 - 3 rain between the tasks. The tasks were explained carefully, and practice trials were not used. The rate of misses (the only errors tabulated) was low across age groups ranging from 9% ( 7 - 8 year olds) to 1.6% (17-19 year olds). The miss rate was higher for the phonological than orthographic task across age groups (9.3% vs. 1.3%); the errors in the phonological task were constant (12.7%) across the 4 youngest groups. Each task continued until 15 artifact-free target trials had been collected. We have found this to be a large enough number of trials for
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498
M.J. TAYLOR
Fig. 4. Topographical maps of the P3 distribution for the two tasks over the first 4 age groups. The peaks were picked at the most marked positivity in the latency range from the grand averages (for the 7 - 8 year olds in the phonological task, this was a relative positivity, as the peak was still below baseline). This produces the marked frontal negativity in the 7 - 8 year olds in the phonological task note also the hemispheric asymmetry with this task. In both tasks, the frontal negativity decreases and there is an anterior movement of the P3 with increasing age.
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Fig. 6. The task by electrode interaction for transformed P3 amplitudes, showing the larger amplitudes anteriorly for the phonological task, and posteriorly for the orthographic task. This effect did not interact with age.
TABLE II Correlations between P3 latencies and RTs (r values). Age
Orthographic task
Phonological task
7- 8 9-10 11-12 13-14 15-16 17-19 20-30
0.53 0.42 0.36 0.80 a 0.16 0.12 0.37
0.22 0.45 0.46 0.43 0.29 0.41 0.14
Across all 7 age groups
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reliable ERPs in children, and that longer recording sessions are too tiring for the younger subjects. The entire procedure required approximately one and a quarter hours. Data analyses. Non-target trials were subtracted from target trials (the relative pattern of these is similar across ages (Fig. 1)), and all analyses were completed on the difference potentials. Difference potentials allow clearer, less ambiguous identification of cognitive components in children and also eliminate age-related changes in absolute amplitudes (which tend
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Fig. 7. Transformed amplitude distribution over the lateral electrodes for the two tasks (plotted by homologous electrode pairs), showing the left > right asymmetry at the temporal sites for N2 (a) and at the temporal, parietal and occipital sites for P3 (b). lh, left hemisphere; rh, right hemisphere.
M A T U R A T I O N IN O R T H O G R A P H I C A N D P H O N O L O G I C A L TASKS
to be larger in younger children). Grand averages were compiled for each task and for each age group (i.e., 14 grand averages). These grand averages then served as templates for peak detection within individual's data. Individual's ERP peaks were taken within 100 msec of a peak's latency in the appropriate grand average. N2 and P3 peak latencies and amplitudes (from the prestimulus baseline) were measured across electrode sites for the two tasks. The P3 peak measured is the same as what is also referred to in the literature as the P3b. The data were submitted to repeated measured MANOVAs (using Greenhouse-Geisser adjusted df) and analyzed as a function of age, task and distribution, and then hemisphere. The amplitudes were analyzed first for main effects and then the transformed amplitudes were analyzed for interaction effects (McCarthy and Wood 1985).
Results
N2 and P3 latencies showed significant effects of age (N2: F (6, 76)= 23.5, P < 0.001; P3: F (6, 76)= 38.1, P < 0.001) and task (N2: F (1, 76)= 125.9 P < 0.001; P3: F (1, 76)= 158.7, P < 0.001) (Fig. 2), decreasing in latency with age and between tasks (orth < phon) (Table I and Fig. 3a). There was an age by task interaction for both latencies (N2: F (6, 76)= 3.6, P < 0.003; P3: F (6, 76) = 3.6, P < 0.003) as the age-related decreases were steeper for the phonological task. For N2, there were no significant differences in latency
501
between the 11-12 year olds and the adults. For P3 latency, age differences were still present between 1516 year olds and adults (F (1, 24) = 9.7, P < 0.005) but were no longer significant when only the 17-19 year olds and adults were compared (F (1, 24)= 3.2, P < 0.08). There were also distributional effects for both N2 and P3 latencies; for N2 latencies were shorter posteriorly, and for P3 were shorter anteriorly (N2: F (7, 560)=6.7, P < 0 . 0 0 1 ; P3: F (6, 511)=4.1, P < 0.001). N2 amplitude varied with age ( F (6, 76) = 2.2, P < 0.049), with electrode (i.e., distribution over the head ( F (4, 323) = 5.2, P < 0.001)) and with transformed N2 amplitudes there was an age by electrode interaction ( F (36, 458) = 2.9, P < 0.001). This change in distribution with age was due to N2 being largest (i.e., more negative) anteriorly and smallest posteriorly in the youngest groups, but a reversal of this by adulthood. For P3 amplitude there were effects of task ( F (2, 146) -- 8.7, P < 0.004), electrode ( F (45, 347) = 98.2, P < 0.001), and age by electrode ( F (27, 347)= 2.8, P < 0.001) and task by electrode ( F (5, 382)= 19.5, P < 0.001) interactions (Fig. 4). The task main effect was due to lower P3 amplitudes for the phonological task. There was not an age main effect as amplitudes increased over the young ages, and then decreased thereafter (Fig. 5). With the transformed amplitudes there was also a task by electrode ( F (7, 523)= 7.3, P < 0.001) interaction. Thus, the cortical distribution varied significantly as a function of task; P3 was larger posteriorly for the orthographic task, and larger anteriorly for the phonological task (Fig. 6). This effect was seen until 16 years of age (F (5, 167) = 2.4, P < 0.037); there were no differences between the 17-18 year olds
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RT RT Fig. 8. Scattergrams of P3 and R T latencies across the 7 age groups for the two tasks. Although the correlations were high when all the ages are included (both RT and P3 show decreases in latencies with age), within each age group the correlations were usually low (see Table II).
502
and adults. Also with the transformed amplitudes, there was a sex main effect ( F (1, 69) = 8.1, P < 0.006), due to larger P3s for females. When the data were analyzed by hemisphere, there were no significant hemispheric differences in latencies of N2. P3 latency showed a sex by hemisphere interaction ( F (1, 69)= 8.8, P < 0.004), due to males having slightly shorter latencies over the right than left hemisphere (591 vs. 595 msec), and females having little latency difference between hemispheres (595 vs. 594 msec). There were no significant hemispheric main effects for N2 or P3 amplitude. There was a task by hemisphere interaction on the transformed P3 amplitudes ( F (1, 76) = 4.1, P < 0.046). This interaction was due to differences between the left and right hemisphere amplitudes for the phonological task (left > right (0.51 vs. 0.47 /zV), while there were no hemispheric asymmetries present for the orthographic task (0.49 vs. 0.49/zV). This effect did not interact with age. Both N2 and P3 transformed amplitudes showed significant hemisphere by electrode interactions (N2: F (4, 323) = 3.9, P < 0.004; P3: F (4, 338) = 5.6, P < 0.001). For N2 there was a left > right (i.e., more negative over the left hemisphere) for temporal sites (Fig. 7a). For P3 these effects were due to left > right (i.e., more positive over the left hemisphere) at the posterior sites (Fig. 7b). The adult data were also analyzed separately for comparison with the Lovrich et al. (1986) paper. There were no distributional differences between tasks, when only the adult data were used, but the N2 and P3 latencies were longer for the phonological than the orthographic task (N2: F (1, 15) = 22.5, P < 0.001; P3: F (1, 15) = 31.3, P < 0.001). Reaction times decreased significantly with age ( F (6, 76) = 9.3, P < 0.001) and between the tasks (orth < phon) (F (1, 76) = 63.9, P < 0.001; Fig. 3b), but showed a steeper decrease across age for the phonological task (age by task interaction (F (6, 76)= 2.7, P < 0.02)). Scattergrams of RTs versus P3 latencies showed a significant correlation between these two measures across age groups (Fig. 8); however, within each age group, the correlations were not high (see Table II).
Discussion
The tasks in this study required distinct types of cognitive processing although the stimuli for the tasks were the same. The orthographic task required only visual feature recognition (although the feature was not uniform across letters). The phonological task required visual-to-auditory translation (subjects had to 'hear' the letters, before matching to target). The ERPs reflected differential processing as a function of task.
M.J. TAYLOR
The latencies decreased more steeply for the phonological task, the P3 amplitudes showed an inverted U with age and, most interestingly, the distribution changed as a function of age and task. The most rapid changes were seen in the younger age groups, when there are also the largest changes in cognitive development. The steady decreases in latency of the N2 and P3 components are consistently found over childhood, although some studies have found little change in the teenage years (e.g., Friedman et al. 1984). Certainly, the age-related changes are steepest in the youngest age groups; significant age effects for P3 were not found after 16 years of age and after 11 years for the N2. There is a large series of behavioral studies that have shown systematic developmental increases in apparent speed of processing with increasing age over childhood years (Kail 1991). This is thought to be due to increases of visual processing efficiency (Enns and Cameron 1987). However, some authors have suggested that the slower behavioral responses in young children may not be due entirely to slower cognitive processes, but to task-related factors, and that perceptual attentional processes develop very young (e.g., Tipper et al. 1989). If this were the case, then one may also see dissociations between ERPs and RT measures. This is the case in some auditory ERPs, such as the mismatch negativity (an early indication of stimulus incongruity that is considered an endogenous component which shows no maturational change over the school age years (Kraus et al. 1992)). However, the components N2 and P3 show systematic decreases in latency until adolescence, and this finding is ubiquitous in the developmental ERP literature (e.g., Courchesne 1978; Howard and Polich 1985; Mullis et al. 1986; Taylor 1988). In adults the time relations between N2 and P3 are stable (i.e., they usually covary (Ritter et al. 1983)); this was not the case in these in developmental data. N2 latency decreases are less steep after 11-12 years of age, suggesting that the cognitive processes associated with N2, namely stimulus evaluation and categorization, are largely mature by that age. This was regardless of task. Thus, even in the more difficult phonological task, the young adolescents were classifying the stimuli as rhyming or not, as quickly as the adults. This asymptote of N2 by early adolescence has also been reported with other visual tasks (Friedman et al. 1984; Taylor 1988). In studies where linear regressions were fitted to N2 and P3, the rate of change of N2 was much lower than that of P3 (Goodin et al. 1978; Johnson 1989). The processing associated with P3, namely final stimulus evaluation and memory updating, continued to show developmental changes virtually until adulthood. This is consistent with other developmental data utilizing specifically memory tasks, that show developmental latency changes in all of the memory-related
MATURATION IN ORTHOGRAPHICAND PHONOLOGICALTASKS components (N4, P3, P4) until adulthood (Taylor and Smith 1992). Thus, the age-related decreases in processing speed seen in the behavioral data cannot be due simply to developing speed of motor responses. There clearly are increases in speed of cognitive processing as well, and the age at which they reach adult values varies with the process (e.g., stimulus categorization or memory updating) a n d / o r task. The task main effect in P3 amplitude is consistent with the phonological task being more difficult than the orthographic task (Fitzgerald and Picton 1983). There was not a task by age interaction, suggesting that the relative difficulty of the phonological and orthographic tasks did not change with age, although the younger children did have a higher miss rate and longer RTs to the phonological task. Practice trials may have decreased the error rate and RTs. However, it is not obvious that this would have affected the ERPs. The most marked changes in the ERPs for the phonological task were in the 3 youngest age groups, and the error rate was constant across the 4 youngest groups. Latency decreases in both ERPs and RTs are ubiquitous in the literature, although the interaction effect (due to more rapid RT decreases in the phonological than orthographic tasks) may have been reduced by practice trials. All age groups found the phonological task the more difficult of the two, and practice may have reduced the latencies across the range, but it would be unlikely to have affected the relative amplitudes or the distributions, due to the differences in cognitive development for these two tasks, as discussed below. The inverted-U P3 amplitude changes with age, seen in this study, do not fit with current interpretations of P3 amplitude. Pelosi et al. (1992) found that increases in amplitude between easy and difficult tasks covaried with improved performance. In the current study, performance (as measured by RT) improved steadily across age. The suggestion of Pelosi et al. (1992) of increased amplitude reflecting more effective cognitive processing would imply that the 11-12 or 13-14 year olds had the most effective processing. Similarly, these developmental data do not fit well with the model of ERP amplitude proposed by Kok (1990), where expended energy correlates inversely with amplitude. Johnson (1986) suggested that subjective probability, stimulus meaning and information transmission all contribute to P3 amplitude. The probability of stimuli presentation did not change with age, although perhaps children's perception of probability changes in an inverted-U fashion with age. Stimulus meaning, or task complexity, might also change with age, but would not likely produce the inverted-U amplitude change, but more likely a steady decrease in amplitude as seen in other tasks (e.g., Taylor and Smith 1992). Information transmission, or one of its factors in Johnson's
503
model, attention, was also not purposefully manipulated, and there are no a priori reasons for it to increase and then decrease with age. The explanation of these age related amplitude changes (seen also in earlier visual ERP studies (Taylor 1987, 1988)) seems to require two factors. The first, may be that task difficulty decreases steadily over the early age range 7-12 years, and hence amplitude increases (Fitzgerald and Picton 1983). Thereafter, the task is so easy that less and less attention need be allocated, perhaps task performance becomes automatic, and thus amplitude decreases over this age range. Some developmental series have found these same amplitude/age effects (e.g., Taylor 1988; Polich 1991), while other studies have found a gradual increase (Mullis et al. 1985; Ladish and Polich 1989) or decrease in amplitude with age (Courchesne 1990; Taylor and Smith 1992). These differences may be task-related, although given the number of variables that differ among studies and labs, a number of factors could be producing these discrepancies. Although age-related distributional differences have been noted since the early studies on developmental ERPs (Courchesne 1978; Mullis et al. 1985) only more recent studies have documented the widespread topographical changes that occur with age (Taylor 1987, 1988; Wijker et al. 1989; Wijker 1991; Stauder 1992). Wijker et al. (1989) and Taylor (1987, 1988) found age-related distributional differences that were more marked in the off-midline electrodes. Stauder et al. (1990) found that distributional differences (and the dipole sources based on these distributions) varied with cognitive development a n d / o r age; the basic cognitive processes were age-related, while more complex cognitive functions were associated with the stage of cognitive development. Wijker (1991) has argued that the age-related changes in ERPs during childhood are largely a result of task-specific demands, but that if tasks encouraged qualitatively different processing in different ages, more marked age-related changes may be seen. This was the case in studies that used a Piagetian task and blocked children on the basis of their achieved Piagetian stage (Stauder 1992). Distributional changes were seen with age for both N2 and P3 in the present study; this is consistent with other developmental series that have included sufficient electrodes for topographical analyses. A change in the distribution of ERP components is thought to indicate changes in strategy or mode of processing (Courchesne 1983; Donchin et al. 1986; Robaey 1987; Stauder 1992), while latency decreases with age are believed to reflect increased efficiency (Howard and Polich 1985; Ladish and Polich 1989; Friedman 1991). The present data, which show distributional age effects only when the younger subjects (< 16 years) are included, would suggest that these are due, at least in
504
part, to changes in strategy with cognitive maturation. Within the younger age range, qualitative differences in task performance would be expected (e.g., Piaget 1977). However, the children in this study were not assessed in terms of the Piagetian stages of development, and the tasks utilized were not known to give evidence of step functions in cognitive development. Thus, the separation between age and cognitive stage as done by Stauder (1992) was not possible. Nevertheless, there were topographical changes in the orthographic task that were similar to those seen in other visual oddball tasks (Taylor 1987, 1988; Wijker et al. 1989; Wijker 1991). These same maturational changes are not seen in children with cognitive disabilities (Taylor and Keenan 1990; Taylor 1991). Wijker (1991) noted the antero-posterior distributional changes with a simple target/non-target task, but argued that these data suggested a continuity in cognitive development across childhood. The distributional change in the phonological task between the two youngest age groups was remarkable, however, and suggests that a significant stage was crossed at the boundary between these age groups. Studies that replicate the current investigation but use children that were or were not taught phonemic aspects of reading may tell us whether there is a stage related to reading at this age, and whether it is affected by instruction (re: Read et al. 1986; Walley et al. 1986). The marked frontal negativity seen with these tasks is widely reported in other developmental series (e.g., Courchesne 1978, 1990; Taylor 1988; Wijker et al. 1989). This negativity has been associated with investment of attentional resources in children (e.g., Robertson et al. 1990), who also suggested that its age-related decreases were related to increased automaticity. The exaggerated form of this frontal negativity in the youngest children for the phonological task (the posterior spread was such that virtually the entire head was negative) could be accounted for by the greater difficulty (and hence greater attention being paid to the task) for these subjects. This was also reflected in their very long RTs to this task (mean 1002 msec). By 9-10 years of age, when the children are reading easily, this negativity is dramatically reduced. This is in accordance with other literature on phonemic development. The distributional differences between tasks were not unexpected, as the cognitive demands differ, and in earlier studies distributional differences were found as a function of task (Taylor 1988). Some adult series have also found task-specific P3 components, that varied in their distribution (e.g., Ruchkin et al. 1990), and this has been reported in other developmental series. In the study by Lovrich et al. (1986), they found a more anterior P3 distribution for the phonological than orthographic task. This was the case for the current
M.J. TAYLOR
study, across age groups, but was not evident when the adult ERPs were analyzed separately. Both Courchesne (1990) and Johnson (1989) found developmental changes to be modality-specific, suggesting that the auditory and visual P3s have different generators. Although in the present study both tasks were visual, one required only visual processing while the other required phonological (auditory) processing as well, and thus may mimic the modality effects. Baddeley and Hitch (1974) and Hitch et al. (1989) have shown that working memory for visual stimuli appears to contain two subsystems, one relying on visual and the other on phonological/verbal coding. They have shown that there is a shift in utilization of these parts of working memory from visual codes in the younger children to phonological codes by 11 years of age, due to young children's inability to use phonological encoding. There is a rapid transition from visual to phonological processing over the early school years when children are learning to read. The current data would support the view of two working memory subsystems in that (1) there were distributional differences in P3 between the tasks, suggesting different cortical utilization that did not interact with age, and (2) the presence of more marked changes, in both distribution and latencies, in the phonological than orthographic task. A strong correlation between phonological awareness and the development of reading has been frequently demonstrated. But, although phonological processing in terms of awareness of rhyming and alliteration begins very early and precedes learning to read (Kirtley et al. 1989; Goswami 1990), phonemic identification of letters begins only after individuals have started to learn to read (Read et al. 1986). Single phoneme identification is very difficult for children up to 7 years of age. Thus, as phonetic associations of letters are learned only in the process of learning an alphabetic language, then it is not surprising that the youngest age group, who are in the early stages of this learning process, did not yet have the same cognitive processes (as reflected in the ERPs) for performing this task as the older children. Walley et al. (1986) found little difference between 5-6 and 7-8 year olds in classifying speech sounds that consisted of several phonemes, but 7-8 year olds could classify on single phonemes better than the younger children. Thus, children who have begun to read based on an alphabet system can perform some phonemic identification tasks. By 9-10 years of age, however, normal children, regardless of language training, can easily perform phonemic tasks (Mann 1986). This transition was certainly seen in the ERPs and is also consistent with a switch to phonological encoding, as discussed above. A hemisphere by task interaction was seen only in P3 amplitude, due to greater (L > R) asymmetry in the
MATURATION IN ORTHOGRAPHIC AND PHONOLOGICAL TASKS
phonological task. The lack of significant asymmetries in the orthographic task is consistent with other studies in the literature (Taylor 1988; Wijker et al. 1989; Altenmuller et al. 1990). However, across tasks there were asymmetries seen in N2 and P3. For N2 the increased negativity was over the left temporal sites, suggesting greater involvement in the underlying cortical region in stimulus classification. This suggests that the letters were processed as verbal stimuli, even in the simple orthographic task. Kok and Rooijakkers (1985) also found an L > R negative component in children over temporal and parietal sites to visual and verbal tasks. P3 appeared to reflect greater involvement with memory updating at the left posterior sites, consistent with the visual/verbal nature of the tasks. In adults series, hemispheric asymmetry was either not investigated (due to the use of only midline electrodes (Polich et al. 1983) or unilaterally located electrodes (Lovrich et al. 1986)) or was noted only in a negative component (N450) and only for non-rhyming pairs (Rugg 1984; Rugg and Barrett 1987). This asymmetry was R > L, unlike the asymmetry in the current study; the stimuli, tasks and population were quite different between these studies and may account for the differing results. Licht et al. (1988) reported age-related changes in lateralization in several ERP components, that were related to reading ability. They proposed that this reflected a developmental shift in hemispheric activation as children learn to read. Earlier studies have also reported changes in lateralization with age (e.g., Kurtzberg et al. 1979). In the current study, no hemispheric effects interacted with age and do not demonstrate utility of ERPs for investigating the question of shifting lateralization. Instead, antero-posterior shifts with age are more pervasive. Sex differences are found occasionally in adult ERP studies (e.g., Picton et al. 1984; Taylor et al. 1990), but are rare in developmental series. Mullis et al. (1985) reported shorter ERP latencies for females, but their study included more adults than children, as their age range was from 8 to 82 years. Friedman et al. (1984) reported sex differences in the N100 and P200 only, due mainly to a difference between 15-year-old males and females, and warned against over-interpreting these findings, due to the small numbers when the age groups were also broken down by sex. In our earlier developmental series with reading tasks (Taylor 1987, 1988), sex differences were not found, and with a memory task (Taylor and Smith 1992) only few sex effects were seen. Thus, the robust sex differences found in the sensory EPs (e.g., Allison et al. 1983) appear to be less marked in developmental ERPs, although the pattern is similar (e.g., a larger P3 for females) when it is found. In summary, these data suggest that the ERPs are indexing underlying cognitive differences both in terms
505
of task requirements and changes in those processes as a function of age. The changing distribution across age groups suggest maturational changes in the sources of the ERP components, and that these are task-specific.
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M.J. TAYLOR effects of age on human event-related potentials. Psychophysiology, 1984, 21: 312-325. Polich, J. P300 and the development of cognition. Paper presented at The Developmental and Behavioral Neurosciences Program. University of Illinois, Chicago, 1991. Polich, J., McCarthy, G., Wang, W.S. and Donchin, E. When words collide: orthographic and phonological interference during word processing. Biol. Psychol., 1983, 16: 155-180. Polich, J., Ladish, C. and Burns, T. Normal variation of P300 in children: age, memory span, and head size. Int. J. Psychophysiol., 1990, 9: 237-248. Read, C., Yun-Fei, Z., Hong-Yin, N. and Bao-Qing, D. The ability to manipulate speech sounds depends on knowing alphabetic writing. Cognition, 1986, 24: 31-44. Ritter, W., Simson, R. and Vaughan, Jr., H.G. Event-related potential correlates of two stages of information processing in physical and semantic discrimination tasks. Psychophysiology, 1983, 20: 168-179. Robaey, P. Apport des potentiels endog~nes ~ l'6tude du d6veloppement cognitif chez l'enfant: revue de la litt6rature. Rev. EEG Neurophysiol. Clin., 1987, 17: 247-258. Robertson, A.L., Mahensan, K. and Campbell, K.B. Lexical, object and reality decisions: development changes in ERPs. In: C.H.M. Brunia, A.W.K. Gaillard and A. Kok (Eds.), Psychophysiological Brain Research. Tilburg University Press, Tilburg, 1990: 303-307. Ruchkin, D.S., Johnson, Jr., R., Canoune, H.L., Ritter, W. and Hammer, M. Multiple sources of P3b associated with different types of information. Psychophysiology, 1990, 27: 157-176. Rugg, M.D. Event-related potentials and the phonological processing of words and non-words. Neuropsychology, 1984, 22: 435-443. Rugg, M.D. and Barrett, S.E. Event-related potentials and the interaction between orthographic and phonological information in a rhyme-judgment task. Brain Lang., 1987, 32: 336-361. Rugg, M., Kok, A., Barrett, G. and Fischler, I. ERPs associated with language and hemispheric specialization. A review. In: W.C. McCallum, R. Zappoli and F. Denoth (Eds.), Cerebral Psychophysiology: Studies in Event-Related Potentials (EEG Suppl. 38). Elsevier Science Publishers, Amsterdam, 1986: 273-300. Stauder, J.E.A. Event Related Brain Potentials and Cognitive Development during Childhood. Doctoral Dissertation, University of Amsterdam, 1992: 1-135. Stauder, J.E.A., Molenaar, P.C.M., Van der Molen, M.W. and Kok, A. ERP scalp topography and stage transitions in cognitive development. In: C.H.M. Brunia, A.W.K. Gaillard and A. Kok (Eds.), Psychophysiological Brain Research, Vol. 2. Tilburg University Press, Tilburg, 1990: 161-166. Taylor, M.J. Developmental changes in cognitive ERPs to linguistic and nonlinguistic stimuli. In: C. Barber and T. Blum (Eds.), Evoked Potentials III. Butterworth, London, 1987: 337-341. Taylor, M.J. Developmental changes in ERPs to visual language stimuli. Biol. Psychol., 1988, 26: 321-338. Taylor, M.J. Reading-related cortical potentials in normal and dyslexic children. Can. J. Neurol. Sci., 1991, 18: 269. Taylor, M.J. and Keenan, N.K. Event-related potentials to visual and language stimuli in normal and dyslexic children. Psychophysiology, 1990, 27: 318-327. Taylor, M.J. and Smith, M.L. Developmental maturation of ERPs to verbal and nonverbal recent memory tasks. ICON V, Jerusalem, Israel, June 1992. Taylor, M.J., Smith, M.L. and Iron, K.S. Event-related potential evidence of sex differences in verbal and nonverbal memory tasks. Neuropsychologia, 1990, 28: 691-705. Taylor, M.J., Voros, J.G., Logan, W.J. and Malone, M.A. Changes in event-related potentials with stimulant medication in children with attention deficit hyperactivity disorder. Biol. Psychol., 1993, submitted. Tipper, S.P., Bourque, T.A., Anderson, S.H. and Brehaut, J.C.
MATURATION IN ORTHOGRAPHIC AND PHONOLOGICAL TASKS Mechanisms of attention: a developmental study. J. Exp. Child Psychol., 1989, 48: 353-378. Walley, A.C., Smith, L.B. and Jusczyk, P.W. The role of phonemes and syllables in the perceived similarity of speech sounds for children. Mem. Cogn., 1986, 14: 220-229. Wijker, W. ERP Ontogenesis in Childhood. Doctoral Dissertation,
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Psychology Department, University of Amsterdam, Amsterdam, 1991. Wijker, W., Molenaar, P.C.M. and Van der Molen, M.W. Agechanges in scalp distribution of cognitive event-related potentials elicited in an oddball task. J. Psychophysiol., 1989, 3: 179-189.
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Maturational changes in ERPs to orthographic and phonological tasks Margot J. Taylor Divisions of Neurology and Neonatology, Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, Ont. M5G 1X8 (Canada) (Accepted for publication: 19 July 1993)
Summary Childrenfrom 7 to 18 years of age (divided into 2 year groupings, i.e., 7-8, 9-10, etc.) and young adults were studied (total of 84 subjects). ERPs were recorded from 19 electrodes during 2 visual oddball tasks: an orthographic task requiring responses to letters with a closed loop (e.g., a, p), and a phonologicaltask, requiring responses to letters that rhymed with 'v' (e.g., c, p). N2 and P3 peak latencies and amplitudes were measured on the difference potentials. RTs decreased with age and between tasks (orth < phon). N2 and P3 latencies decreased with age and were shorter for the orthographic than phonologicaltask. P3 amplitude was lower for the phonologicaltask; the cortical distribution varied significantly as a function of age and task. The task differences in distribution were more marked in the younger age groups. Hemispheric asymmetries in P3 amplitudes were seen in the phonological task. The orthographic task required simple visual feature recognition and the phonological task required a visual-to-auditory translation. The interaction effects suggest that cortical utilization differs for these tasks, with greater age-related changes for the phonological task.
Key words: Event-related potentials; Maturational changes; Orthographic task; Phonologicaltask; N2; P3
Event-related potentials (ERPs) are a sensitive means of assessing the timing and cortical utilization of cognitive processing, and as such offer a valuable means of studying cognitive development and underlying neurophysiological changes. A number studies have shown significant maturational changes in the ERPs that have been related to cognitive development (Courchesne 1983; Mullis et al. 1985; Robaey 1987; Taylor 1988; Johnson 1989; Ladish and Polich 1989; Stauder et al. 1990), associated with various types of cognitive processing such as memory span (Polich et al. 1990), or the development of reading skills (Taylor 1988). Most of these studies show gradual maturational changes in the ERPs, suggesting quantitative changes in cognitive processing with age. Reading appears to be a gradual or continuous acquisition of a skill, without the cataclysmic changes seen in some other aspects of cognitive development. There is some discussion in the literature as to whether children's performance on various reading-related tasks depends upon a general developmental trend in perceptual and attentional abilities (e.g., Walley et al. 1986) or whether specific abilities such as phonemic segmentation depend upon language training (Read et al. 1986; Kirtley et al. 1989). Clearly, both visual and
phonological processing of words and letters is critical to reading. Gattuso et al. (1991) found that phonemic skills were not related to children's ability to attend to aspects of a visual stimulus, suggesting that the two types of cognitive processing were not tied to a single underlying developmental trend. This leaves open the possibility of differing maturational patterns in these tasks. Processing of phonemic information or phonological awareness is, however, very closely tied to children's reading ability (Kirtley et al. 1989; Gattuso et al. 1991), and certainly visual identification of letters is basic to the reading process. Studies with adults have shown that ERPs index differential processing as a function of orthographic or phonological features of stimuli (Polich et al. 1983; Loverich et al. 1986; Rugg and Barrett 1987). Loverich et al. (1986) recorded ERPs in 10 adults from 11 electrodes overlying the left hemisphere. They found topographical differences between orthographic and phonological tasks that used single letter stimuli. Although both tasks had posteriorly located components, there was more of an anterior spread for the phonological task. They suggested that this was due to the visual-to-auditory conversion necessary for the phonological task, which would require cortical involvement
MATURATION IN ORTHOGRAPHIC AND PHONOLOGICALTASKS closer to the auditory regions. There was not a significant latency shift between the two tasks, suggesting that the speed of processing was equal (although there was a tendency for longer latencies in the phonological task). Other studies that have investigated orthographic and phonological aspects of visual language processing have used word stimuli, that are spelled similarly or not, that rhymed or not. Polich et al. (1983) also did not find significant latency differences between ERPs to visual versus rhyming tasks. Rugg (1984) and Rugg and Barrett 1987) have reported a series of studies using rhyme judgments, that show hemispheric asymmetry (R > L) in a negativity at 450 msec, seen to non-rhyming words. Although there are a number of behavioral studies suggesting increasing hemispheric lateralization in reading tasks with age (e.g., Bakker 1981), only a few E R P studies have found asymmetries with reading tasks developmentally (Licht et al. 1988). As ERPs are often more sensitive measures of cognitive processes than are behavioral measures, it might be expected that they would index developing hemispheric asymmetries, given appropriate tasks (Rugg et al. 1986). Reliable hemispheric asymmetries have been reported in adult studies from several centers (e.g., Kutas and Hillyard 1982; Rugg 1984; Neville et al. 1986), with the asymmetry shifting with the task. The orthographic and phonological tasks used by Lovrich et al. (1986) would be suitable for use with children, as young children learning to read know their alphabet and phonemes (Mann 1986). These two tasks also assess different aspects of cognitive processing that precede reading: visual and phonological encoding of letters. We would expect both to show developmental changes, but that these would be less marked in the orthographic task, as simple visual discrimination matures very early, whereas phonological encoding undergoes rapid maturation over the early school age years. The adult studies suggest that there would also be distributional differences in these two tasks, and given the differing maturational patterns, it was expected that these would show task-
495
Non-TargetI _ 7-8yr.
9-10yr.
11-12yr.
~ 1 ~ 1 6
yn
~
17-18yr.
~
Adult ,
S
,
aoo
800
ms
960
12 o
IL.~r~a,, v
Fig. 1. Grand average ERPs at Oz to target and non-target stimuli in the orthographic task for the 7 age groups. Clear target/non-target
differences are evident at all ages.
TABLE I Mean values for the two tasks by age. Age 7- 8 9-10 11-12 13-14 15-16 17-18 Adult
N2 latency(msec)
P3 latency(msec)
Orth
Phon
Orth
Phon
RT (msec) Orth
Phon
P3 amplitude (mV) Orth Phon
422 5:37 408 _+38 352 _+43 360 _+25 332 _+25 323 _+36 337 5:31
542 _+46 475 _+70 414 _+48 434 _+40 374+ 61 356_+38 385 5:53
641 _+38 643 _+32 571 _+44 553 _+40 530_+52 514_+39 482+ 43
766 _+56 682 _+51 638 _+53 649 _+49 587 _+25 567 _+53 543 5:49
781+ 98 703+ 83 637_+ 66 540-+ 53 5725:128 516_+ 69 524_+ 59
1002+114 798+126 792-+ 147 721_+ 98 679 5:140 657_+126 620_+ 56
7.8+10 10.5±12 12.3-+ 16 11.1_+12 10.5_+ 8 8.0_+ 8 6.5 _+ 6
1.6_+ 8 7.7_+ 9 9.6-+ 11 9.8_+10 4.6_+ 6 10.0_+ 7 4.7_+ 7
496
M.J. T A Y L O R
specific age-related changes. Thus, the present study recorded ERPs in subjects from 7 to 30 years of age in these two reading-related tasks, to investigate the rela-
Orthographic Task
tive maturational pattern of these tasks via ERPs, and possible distributional differences as a function of task a n d / o r age.
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MATURATION
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PHONOLOGICAL
Methods
Subjects Children aged 7 - 1 8 years of age (divided into 2 year groupings: i.e., 7 - 8 (7.1-8.5, m = 7.98 + 0.49 years, n = 12), 9 - 1 0 (9.0-10.5, m = 9.68 + 0.54 years, n = 10), 1112 (11.1-12.8, m = 11.84 + 0.60 years, n = 14), 13-14 (13.0-14.8, m = 13.8 + 0.77 years, n = 12), 15-16 (15.0-16.9, m = 15.8 + 0.68 years, n = 10), 17-19 years (17.3-19.4, m = 18.4 + 0.68 years, n = 10)) and young adults (20-30 years, m = 26.6 + 2.1, n = 16) (total of 84 subjects) were studied. The male:female ratio was 40:44 and the ratio was balanced within age groups. None had a history of neurological or psychiatric disorders, and the children were performing appropriately for their ages in school. Subjects had normal or corrected to normal vision. All subjects spoke English as their first language. All subjects would have exposure to French as a second language; French fluency was not assessed.
Procedure ERP recording. E R P s were recorded using a P D P 11/73 system from 19 electrodes (Fpz, Fz, Cz, Pz, Oz, F3, F4, F7, F8, C3, C4, P3, P4, T3, T4, T5, T6, O1, 0 2 ) using a balanced non-cephalic spine-to-clavicle reference pair. The electrode impedance was always below 5 kO. E O G was monitored with two electrodes, placed at the outer canthus and on the supraorbital ridge. The E R P s were recorded with a bandpass of 0.1-30 Hz and a 1.5 sec sweep, starting 50 msec prior to stimulus
TASKS
497
presentation. All trials in which E O G or E M G artifact exceeded 90% of full-scale deflection were automatically rejected. The rejection rate decreased with age, but did not vary w i t h task. Tasks. Two tasks were run with each subject, the order of presentation varied across subjects. Two semantic tasks were also run and will be presented separately. In the orthographic task, lower case letters (visual angle = 0.8 °) were presented one at a time and targets were those which had a closed loop as part of the configuration (i.e., a, b, d, e, g, o, p, q). In the phonological task, the same stimuli were presented but the targets were letters that rhymed with ' v ' (including v; i.e., b, c, d, e, g, p, t, v). The letter 'z' was not presented in this task as it was considered an ambiguous stimulus, since its pronunciation varies. Stimuli were presented using a Macintosh computer for 0.2 sec with a 2.5 sec interstimulus interval. Target and nontarget stimuli were randomly interspersed, with targets occurring with a probability of 20%; subjects pressed a button to the designated target stimuli. Subjects made the button press with their dominant hand; 9 were left-handed, 1 or 2 in each age group, except 7 - 8 year olds. There were short breaks of 2 - 3 rain between the tasks. The tasks were explained carefully, and practice trials were not used. The rate of misses (the only errors tabulated) was low across age groups ranging from 9% ( 7 - 8 year olds) to 1.6% (17-19 year olds). The miss rate was higher for the phonological than orthographic task across age groups (9.3% vs. 1.3%); the errors in the phonological task were constant (12.7%) across the 4 youngest groups. Each task continued until 15 artifact-free target trials had been collected. We have found this to be a large enough number of trials for
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498
M.J. TAYLOR
Fig. 4. Topographical maps of the P3 distribution for the two tasks over the first 4 age groups. The peaks were picked at the most marked positivity in the latency range from the grand averages (for the 7 - 8 year olds in the phonological task, this was a relative positivity, as the peak was still below baseline). This produces the marked frontal negativity in the 7 - 8 year olds in the phonological task note also the hemispheric asymmetry with this task. In both tasks, the frontal negativity decreases and there is an anterior movement of the P3 with increasing age.
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Fig. 6. The task by electrode interaction for transformed P3 amplitudes, showing the larger amplitudes anteriorly for the phonological task, and posteriorly for the orthographic task. This effect did not interact with age.
TABLE II Correlations between P3 latencies and RTs (r values). Age
Orthographic task
Phonological task
7- 8 9-10 11-12 13-14 15-16 17-19 20-30
0.53 0.42 0.36 0.80 a 0.16 0.12 0.37
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reliable ERPs in children, and that longer recording sessions are too tiring for the younger subjects. The entire procedure required approximately one and a quarter hours. Data analyses. Non-target trials were subtracted from target trials (the relative pattern of these is similar across ages (Fig. 1)), and all analyses were completed on the difference potentials. Difference potentials allow clearer, less ambiguous identification of cognitive components in children and also eliminate age-related changes in absolute amplitudes (which tend
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Fig. 7. Transformed amplitude distribution over the lateral electrodes for the two tasks (plotted by homologous electrode pairs), showing the left > right asymmetry at the temporal sites for N2 (a) and at the temporal, parietal and occipital sites for P3 (b). lh, left hemisphere; rh, right hemisphere.
M A T U R A T I O N IN O R T H O G R A P H I C A N D P H O N O L O G I C A L TASKS
to be larger in younger children). Grand averages were compiled for each task and for each age group (i.e., 14 grand averages). These grand averages then served as templates for peak detection within individual's data. Individual's ERP peaks were taken within 100 msec of a peak's latency in the appropriate grand average. N2 and P3 peak latencies and amplitudes (from the prestimulus baseline) were measured across electrode sites for the two tasks. The P3 peak measured is the same as what is also referred to in the literature as the P3b. The data were submitted to repeated measured MANOVAs (using Greenhouse-Geisser adjusted df) and analyzed as a function of age, task and distribution, and then hemisphere. The amplitudes were analyzed first for main effects and then the transformed amplitudes were analyzed for interaction effects (McCarthy and Wood 1985).
Results
N2 and P3 latencies showed significant effects of age (N2: F (6, 76)= 23.5, P < 0.001; P3: F (6, 76)= 38.1, P < 0.001) and task (N2: F (1, 76)= 125.9 P < 0.001; P3: F (1, 76)= 158.7, P < 0.001) (Fig. 2), decreasing in latency with age and between tasks (orth < phon) (Table I and Fig. 3a). There was an age by task interaction for both latencies (N2: F (6, 76)= 3.6, P < 0.003; P3: F (6, 76) = 3.6, P < 0.003) as the age-related decreases were steeper for the phonological task. For N2, there were no significant differences in latency
501
between the 11-12 year olds and the adults. For P3 latency, age differences were still present between 1516 year olds and adults (F (1, 24) = 9.7, P < 0.005) but were no longer significant when only the 17-19 year olds and adults were compared (F (1, 24)= 3.2, P < 0.08). There were also distributional effects for both N2 and P3 latencies; for N2 latencies were shorter posteriorly, and for P3 were shorter anteriorly (N2: F (7, 560)=6.7, P < 0 . 0 0 1 ; P3: F (6, 511)=4.1, P < 0.001). N2 amplitude varied with age ( F (6, 76) = 2.2, P < 0.049), with electrode (i.e., distribution over the head ( F (4, 323) = 5.2, P < 0.001)) and with transformed N2 amplitudes there was an age by electrode interaction ( F (36, 458) = 2.9, P < 0.001). This change in distribution with age was due to N2 being largest (i.e., more negative) anteriorly and smallest posteriorly in the youngest groups, but a reversal of this by adulthood. For P3 amplitude there were effects of task ( F (2, 146) -- 8.7, P < 0.004), electrode ( F (45, 347) = 98.2, P < 0.001), and age by electrode ( F (27, 347)= 2.8, P < 0.001) and task by electrode ( F (5, 382)= 19.5, P < 0.001) interactions (Fig. 4). The task main effect was due to lower P3 amplitudes for the phonological task. There was not an age main effect as amplitudes increased over the young ages, and then decreased thereafter (Fig. 5). With the transformed amplitudes there was also a task by electrode ( F (7, 523)= 7.3, P < 0.001) interaction. Thus, the cortical distribution varied significantly as a function of task; P3 was larger posteriorly for the orthographic task, and larger anteriorly for the phonological task (Fig. 6). This effect was seen until 16 years of age (F (5, 167) = 2.4, P < 0.037); there were no differences between the 17-18 year olds
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502
and adults. Also with the transformed amplitudes, there was a sex main effect ( F (1, 69) = 8.1, P < 0.006), due to larger P3s for females. When the data were analyzed by hemisphere, there were no significant hemispheric differences in latencies of N2. P3 latency showed a sex by hemisphere interaction ( F (1, 69)= 8.8, P < 0.004), due to males having slightly shorter latencies over the right than left hemisphere (591 vs. 595 msec), and females having little latency difference between hemispheres (595 vs. 594 msec). There were no significant hemispheric main effects for N2 or P3 amplitude. There was a task by hemisphere interaction on the transformed P3 amplitudes ( F (1, 76) = 4.1, P < 0.046). This interaction was due to differences between the left and right hemisphere amplitudes for the phonological task (left > right (0.51 vs. 0.47 /zV), while there were no hemispheric asymmetries present for the orthographic task (0.49 vs. 0.49/zV). This effect did not interact with age. Both N2 and P3 transformed amplitudes showed significant hemisphere by electrode interactions (N2: F (4, 323) = 3.9, P < 0.004; P3: F (4, 338) = 5.6, P < 0.001). For N2 there was a left > right (i.e., more negative over the left hemisphere) for temporal sites (Fig. 7a). For P3 these effects were due to left > right (i.e., more positive over the left hemisphere) at the posterior sites (Fig. 7b). The adult data were also analyzed separately for comparison with the Lovrich et al. (1986) paper. There were no distributional differences between tasks, when only the adult data were used, but the N2 and P3 latencies were longer for the phonological than the orthographic task (N2: F (1, 15) = 22.5, P < 0.001; P3: F (1, 15) = 31.3, P < 0.001). Reaction times decreased significantly with age ( F (6, 76) = 9.3, P < 0.001) and between the tasks (orth < phon) (F (1, 76) = 63.9, P < 0.001; Fig. 3b), but showed a steeper decrease across age for the phonological task (age by task interaction (F (6, 76)= 2.7, P < 0.02)). Scattergrams of RTs versus P3 latencies showed a significant correlation between these two measures across age groups (Fig. 8); however, within each age group, the correlations were not high (see Table II).
Discussion
The tasks in this study required distinct types of cognitive processing although the stimuli for the tasks were the same. The orthographic task required only visual feature recognition (although the feature was not uniform across letters). The phonological task required visual-to-auditory translation (subjects had to 'hear' the letters, before matching to target). The ERPs reflected differential processing as a function of task.
M.J. TAYLOR
The latencies decreased more steeply for the phonological task, the P3 amplitudes showed an inverted U with age and, most interestingly, the distribution changed as a function of age and task. The most rapid changes were seen in the younger age groups, when there are also the largest changes in cognitive development. The steady decreases in latency of the N2 and P3 components are consistently found over childhood, although some studies have found little change in the teenage years (e.g., Friedman et al. 1984). Certainly, the age-related changes are steepest in the youngest age groups; significant age effects for P3 were not found after 16 years of age and after 11 years for the N2. There is a large series of behavioral studies that have shown systematic developmental increases in apparent speed of processing with increasing age over childhood years (Kail 1991). This is thought to be due to increases of visual processing efficiency (Enns and Cameron 1987). However, some authors have suggested that the slower behavioral responses in young children may not be due entirely to slower cognitive processes, but to task-related factors, and that perceptual attentional processes develop very young (e.g., Tipper et al. 1989). If this were the case, then one may also see dissociations between ERPs and RT measures. This is the case in some auditory ERPs, such as the mismatch negativity (an early indication of stimulus incongruity that is considered an endogenous component which shows no maturational change over the school age years (Kraus et al. 1992)). However, the components N2 and P3 show systematic decreases in latency until adolescence, and this finding is ubiquitous in the developmental ERP literature (e.g., Courchesne 1978; Howard and Polich 1985; Mullis et al. 1986; Taylor 1988). In adults the time relations between N2 and P3 are stable (i.e., they usually covary (Ritter et al. 1983)); this was not the case in these in developmental data. N2 latency decreases are less steep after 11-12 years of age, suggesting that the cognitive processes associated with N2, namely stimulus evaluation and categorization, are largely mature by that age. This was regardless of task. Thus, even in the more difficult phonological task, the young adolescents were classifying the stimuli as rhyming or not, as quickly as the adults. This asymptote of N2 by early adolescence has also been reported with other visual tasks (Friedman et al. 1984; Taylor 1988). In studies where linear regressions were fitted to N2 and P3, the rate of change of N2 was much lower than that of P3 (Goodin et al. 1978; Johnson 1989). The processing associated with P3, namely final stimulus evaluation and memory updating, continued to show developmental changes virtually until adulthood. This is consistent with other developmental data utilizing specifically memory tasks, that show developmental latency changes in all of the memory-related
MATURATION IN ORTHOGRAPHICAND PHONOLOGICALTASKS components (N4, P3, P4) until adulthood (Taylor and Smith 1992). Thus, the age-related decreases in processing speed seen in the behavioral data cannot be due simply to developing speed of motor responses. There clearly are increases in speed of cognitive processing as well, and the age at which they reach adult values varies with the process (e.g., stimulus categorization or memory updating) a n d / o r task. The task main effect in P3 amplitude is consistent with the phonological task being more difficult than the orthographic task (Fitzgerald and Picton 1983). There was not a task by age interaction, suggesting that the relative difficulty of the phonological and orthographic tasks did not change with age, although the younger children did have a higher miss rate and longer RTs to the phonological task. Practice trials may have decreased the error rate and RTs. However, it is not obvious that this would have affected the ERPs. The most marked changes in the ERPs for the phonological task were in the 3 youngest age groups, and the error rate was constant across the 4 youngest groups. Latency decreases in both ERPs and RTs are ubiquitous in the literature, although the interaction effect (due to more rapid RT decreases in the phonological than orthographic tasks) may have been reduced by practice trials. All age groups found the phonological task the more difficult of the two, and practice may have reduced the latencies across the range, but it would be unlikely to have affected the relative amplitudes or the distributions, due to the differences in cognitive development for these two tasks, as discussed below. The inverted-U P3 amplitude changes with age, seen in this study, do not fit with current interpretations of P3 amplitude. Pelosi et al. (1992) found that increases in amplitude between easy and difficult tasks covaried with improved performance. In the current study, performance (as measured by RT) improved steadily across age. The suggestion of Pelosi et al. (1992) of increased amplitude reflecting more effective cognitive processing would imply that the 11-12 or 13-14 year olds had the most effective processing. Similarly, these developmental data do not fit well with the model of ERP amplitude proposed by Kok (1990), where expended energy correlates inversely with amplitude. Johnson (1986) suggested that subjective probability, stimulus meaning and information transmission all contribute to P3 amplitude. The probability of stimuli presentation did not change with age, although perhaps children's perception of probability changes in an inverted-U fashion with age. Stimulus meaning, or task complexity, might also change with age, but would not likely produce the inverted-U amplitude change, but more likely a steady decrease in amplitude as seen in other tasks (e.g., Taylor and Smith 1992). Information transmission, or one of its factors in Johnson's
503
model, attention, was also not purposefully manipulated, and there are no a priori reasons for it to increase and then decrease with age. The explanation of these age related amplitude changes (seen also in earlier visual ERP studies (Taylor 1987, 1988)) seems to require two factors. The first, may be that task difficulty decreases steadily over the early age range 7-12 years, and hence amplitude increases (Fitzgerald and Picton 1983). Thereafter, the task is so easy that less and less attention need be allocated, perhaps task performance becomes automatic, and thus amplitude decreases over this age range. Some developmental series have found these same amplitude/age effects (e.g., Taylor 1988; Polich 1991), while other studies have found a gradual increase (Mullis et al. 1985; Ladish and Polich 1989) or decrease in amplitude with age (Courchesne 1990; Taylor and Smith 1992). These differences may be task-related, although given the number of variables that differ among studies and labs, a number of factors could be producing these discrepancies. Although age-related distributional differences have been noted since the early studies on developmental ERPs (Courchesne 1978; Mullis et al. 1985) only more recent studies have documented the widespread topographical changes that occur with age (Taylor 1987, 1988; Wijker et al. 1989; Wijker 1991; Stauder 1992). Wijker et al. (1989) and Taylor (1987, 1988) found age-related distributional differences that were more marked in the off-midline electrodes. Stauder et al. (1990) found that distributional differences (and the dipole sources based on these distributions) varied with cognitive development a n d / o r age; the basic cognitive processes were age-related, while more complex cognitive functions were associated with the stage of cognitive development. Wijker (1991) has argued that the age-related changes in ERPs during childhood are largely a result of task-specific demands, but that if tasks encouraged qualitatively different processing in different ages, more marked age-related changes may be seen. This was the case in studies that used a Piagetian task and blocked children on the basis of their achieved Piagetian stage (Stauder 1992). Distributional changes were seen with age for both N2 and P3 in the present study; this is consistent with other developmental series that have included sufficient electrodes for topographical analyses. A change in the distribution of ERP components is thought to indicate changes in strategy or mode of processing (Courchesne 1983; Donchin et al. 1986; Robaey 1987; Stauder 1992), while latency decreases with age are believed to reflect increased efficiency (Howard and Polich 1985; Ladish and Polich 1989; Friedman 1991). The present data, which show distributional age effects only when the younger subjects (< 16 years) are included, would suggest that these are due, at least in
504
part, to changes in strategy with cognitive maturation. Within the younger age range, qualitative differences in task performance would be expected (e.g., Piaget 1977). However, the children in this study were not assessed in terms of the Piagetian stages of development, and the tasks utilized were not known to give evidence of step functions in cognitive development. Thus, the separation between age and cognitive stage as done by Stauder (1992) was not possible. Nevertheless, there were topographical changes in the orthographic task that were similar to those seen in other visual oddball tasks (Taylor 1987, 1988; Wijker et al. 1989; Wijker 1991). These same maturational changes are not seen in children with cognitive disabilities (Taylor and Keenan 1990; Taylor 1991). Wijker (1991) noted the antero-posterior distributional changes with a simple target/non-target task, but argued that these data suggested a continuity in cognitive development across childhood. The distributional change in the phonological task between the two youngest age groups was remarkable, however, and suggests that a significant stage was crossed at the boundary between these age groups. Studies that replicate the current investigation but use children that were or were not taught phonemic aspects of reading may tell us whether there is a stage related to reading at this age, and whether it is affected by instruction (re: Read et al. 1986; Walley et al. 1986). The marked frontal negativity seen with these tasks is widely reported in other developmental series (e.g., Courchesne 1978, 1990; Taylor 1988; Wijker et al. 1989). This negativity has been associated with investment of attentional resources in children (e.g., Robertson et al. 1990), who also suggested that its age-related decreases were related to increased automaticity. The exaggerated form of this frontal negativity in the youngest children for the phonological task (the posterior spread was such that virtually the entire head was negative) could be accounted for by the greater difficulty (and hence greater attention being paid to the task) for these subjects. This was also reflected in their very long RTs to this task (mean 1002 msec). By 9-10 years of age, when the children are reading easily, this negativity is dramatically reduced. This is in accordance with other literature on phonemic development. The distributional differences between tasks were not unexpected, as the cognitive demands differ, and in earlier studies distributional differences were found as a function of task (Taylor 1988). Some adult series have also found task-specific P3 components, that varied in their distribution (e.g., Ruchkin et al. 1990), and this has been reported in other developmental series. In the study by Lovrich et al. (1986), they found a more anterior P3 distribution for the phonological than orthographic task. This was the case for the current
M.J. TAYLOR
study, across age groups, but was not evident when the adult ERPs were analyzed separately. Both Courchesne (1990) and Johnson (1989) found developmental changes to be modality-specific, suggesting that the auditory and visual P3s have different generators. Although in the present study both tasks were visual, one required only visual processing while the other required phonological (auditory) processing as well, and thus may mimic the modality effects. Baddeley and Hitch (1974) and Hitch et al. (1989) have shown that working memory for visual stimuli appears to contain two subsystems, one relying on visual and the other on phonological/verbal coding. They have shown that there is a shift in utilization of these parts of working memory from visual codes in the younger children to phonological codes by 11 years of age, due to young children's inability to use phonological encoding. There is a rapid transition from visual to phonological processing over the early school years when children are learning to read. The current data would support the view of two working memory subsystems in that (1) there were distributional differences in P3 between the tasks, suggesting different cortical utilization that did not interact with age, and (2) the presence of more marked changes, in both distribution and latencies, in the phonological than orthographic task. A strong correlation between phonological awareness and the development of reading has been frequently demonstrated. But, although phonological processing in terms of awareness of rhyming and alliteration begins very early and precedes learning to read (Kirtley et al. 1989; Goswami 1990), phonemic identification of letters begins only after individuals have started to learn to read (Read et al. 1986). Single phoneme identification is very difficult for children up to 7 years of age. Thus, as phonetic associations of letters are learned only in the process of learning an alphabetic language, then it is not surprising that the youngest age group, who are in the early stages of this learning process, did not yet have the same cognitive processes (as reflected in the ERPs) for performing this task as the older children. Walley et al. (1986) found little difference between 5-6 and 7-8 year olds in classifying speech sounds that consisted of several phonemes, but 7-8 year olds could classify on single phonemes better than the younger children. Thus, children who have begun to read based on an alphabet system can perform some phonemic identification tasks. By 9-10 years of age, however, normal children, regardless of language training, can easily perform phonemic tasks (Mann 1986). This transition was certainly seen in the ERPs and is also consistent with a switch to phonological encoding, as discussed above. A hemisphere by task interaction was seen only in P3 amplitude, due to greater (L > R) asymmetry in the
MATURATION IN ORTHOGRAPHIC AND PHONOLOGICAL TASKS
phonological task. The lack of significant asymmetries in the orthographic task is consistent with other studies in the literature (Taylor 1988; Wijker et al. 1989; Altenmuller et al. 1990). However, across tasks there were asymmetries seen in N2 and P3. For N2 the increased negativity was over the left temporal sites, suggesting greater involvement in the underlying cortical region in stimulus classification. This suggests that the letters were processed as verbal stimuli, even in the simple orthographic task. Kok and Rooijakkers (1985) also found an L > R negative component in children over temporal and parietal sites to visual and verbal tasks. P3 appeared to reflect greater involvement with memory updating at the left posterior sites, consistent with the visual/verbal nature of the tasks. In adults series, hemispheric asymmetry was either not investigated (due to the use of only midline electrodes (Polich et al. 1983) or unilaterally located electrodes (Lovrich et al. 1986)) or was noted only in a negative component (N450) and only for non-rhyming pairs (Rugg 1984; Rugg and Barrett 1987). This asymmetry was R > L, unlike the asymmetry in the current study; the stimuli, tasks and population were quite different between these studies and may account for the differing results. Licht et al. (1988) reported age-related changes in lateralization in several ERP components, that were related to reading ability. They proposed that this reflected a developmental shift in hemispheric activation as children learn to read. Earlier studies have also reported changes in lateralization with age (e.g., Kurtzberg et al. 1979). In the current study, no hemispheric effects interacted with age and do not demonstrate utility of ERPs for investigating the question of shifting lateralization. Instead, antero-posterior shifts with age are more pervasive. Sex differences are found occasionally in adult ERP studies (e.g., Picton et al. 1984; Taylor et al. 1990), but are rare in developmental series. Mullis et al. (1985) reported shorter ERP latencies for females, but their study included more adults than children, as their age range was from 8 to 82 years. Friedman et al. (1984) reported sex differences in the N100 and P200 only, due mainly to a difference between 15-year-old males and females, and warned against over-interpreting these findings, due to the small numbers when the age groups were also broken down by sex. In our earlier developmental series with reading tasks (Taylor 1987, 1988), sex differences were not found, and with a memory task (Taylor and Smith 1992) only few sex effects were seen. Thus, the robust sex differences found in the sensory EPs (e.g., Allison et al. 1983) appear to be less marked in developmental ERPs, although the pattern is similar (e.g., a larger P3 for females) when it is found. In summary, these data suggest that the ERPs are indexing underlying cognitive differences both in terms
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of task requirements and changes in those processes as a function of age. The changing distribution across age groups suggest maturational changes in the sources of the ERP components, and that these are task-specific.
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