Event-Related Brain Potentials Elicited during Phonological Processing Differentiate Subgroups of Reading Disabled Adolescents

62, 163–185 (1998) BL971893

BRAIN AND LANGUAGE ARTICLE NO.

Event-Related Brain Potentials Elicited during Phonological Processing Differentiate Subgroups of Reading Disabled Adolescents W. B. McPherson, P. T. Ackerman, P. J. Holcomb, and R. A. Dykman Center for Applied Research and Evaluation, Arkansas Children’s Hospital, University of Arkansas for Medical Sciences Visual and auditory rhyme judgment tasks were administered to adolescent dyslexics and normal readers while event-related brain potentials were recorded. Reading disabled subjects were split into two groups based on a median split of scores on a visual non-word decoding test. The better decoders were called Phonetics and the poorer decoders were referred to as Dysphonetics. Single syllable, real word stimuli were used, and both rhyming and non-rhyming targets had a 50% chance for matching orthography. In the visual paradigm the normal readers exhibited a left frontal CNV before targets, a large reduction in frontal N400 for matching orthography (orthographic priming), and a large reduction in parietal N400 for rhyming targets (phonological priming). Dysphonetics had an intact CNV and orthographic priming, but the group’s phonological priming was very reduced. Phonetics showed both orthographic and phonological priming but had a marked reduction in their CNV. In the auditory task, controls showed a left parietal N400 priming effect for rhyming targets. Dysphonetics showed a similar bilateral effect. The Phonetics did not show a normal priming effect, but produced evidence for priming at a longer latency. Additionally, the Phonetic group responded more slowly than either of the other two groups, who responded with similar latencies. These results support the separation of the reading disabled into a group that has difficulty translating orthography into phonology, and a group that is slower functioning and has reduced capacity in preparing for a response.  1998 Academic Press Key Words: N400; CNV; phonological processing; reading disability. This research was part of a doctoral dissertation by the first author completed at Tufts University. The research received partial funding from a research scholarship to the first author from the Donald D. Hammill Foundation. The research was also supported in part by Grant HD24634 from the National Institute of Child Health and Human Development to the fourth author. The authors are indebted to co-workers Nancy Weir, Dianne Metzler, and Mike Oglesby for their help in data collection. They are also indebted to Carol Holloway and other colleagues at the Child Study Center who assisted in recruitment and psychological testing of subjects. Address correspondence and reprint requests to W. Brian McPherson, Dept. Of Pediatrics, Slot 512/26, Arkansas Children’s Hospital, 800 Marshall Street, Little Rock, AR 72202. 163 0093-934X/98 $25.00 Copyright  1998 by Academic Press All rights of reproduction in any form reserved.

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In the past 15 years, starting with the seminal work of Kutas and Hillyard (1980), the event-related brain potential (ERP) component known as the N400, a negative peak usually occurring approximately 400 msec post-stimulus, has been used as a measure in numerous studies of human memory and cognition. The early work on the N400 focused on semantic processing of language, both verbal and written (see Kutas & Van Patten, 1988, for a review), and produced the generalized finding of a reduction in the amplitude of the N400 for a word that is semantically primed, i.e., a target word that is preceded by another word or part of a sentence that is semantically congruous with the target. Not all studies on the N400 have focused on semantic processing. Some have shown a negative peak at approximately 400 msec post-stimulus to be modulated by phonological information as well (e.g., Barrett & Rugg, 1987; Forbes & Connelly, 1995; Rugg, 1984a, 1984b; Praamstra & Stegeman, 1993; Praamstra, Meyer, & Levelt, 1994). Rugg (1984a, 1984b) demonstrated that when the second of two visual, sequentially presented words rhymed with the first there was a reduction in this negativity compared to that for non-rhyming words. Praamstra and Stegeman (1993) and Praamstra, Meyer, and Levelt (1994) demonstrated a similar effect for auditory stimuli. This priming effect for rhyming words has a similar scalp distribution to the N400 semantic priming effect, and both Rugg and Praamstra and Stegeman suggested that the negativity modulated by rhyming stimuli belonged to the same general class of negativities as the N400 reported by Kutas and Hillyard. One issue that has surfaced in the ERP studies of rhyming and non-rhyming word pairs is the relative influence of orthographic and phonological information. Polich, McCarthy, Wang, and Donchin (1983), Kramer and Donchin (1987), and Rugg and Barret (1987) used similar paradigms to examine this issue. Polich et al. examined the P300 component instead of the N400, but the other two studies involved the N400. Kramer and Donchin used a pair of tasks in which subjects had to either discriminate between rhyming and non-rhyming targets or discriminate between target words with endings that were similar or different than the endings of priming words. These tasks both employed four types of sequentially presented word pairs, including: 1) word pairs that rhymed and had orthographically similar endings, e.g., ring-king, 2) word pairs that rhymed but had different ending orthography, e.g., dune-moon, 3) non-rhyming word pairs with similar endings, e.g., bomb-tomb, 4) non-rhyming word pairs with different endings, e.g, wood-tape. They reported that the amplitude of the N4001 was inversely related to the degree of match between the prime and 1 Kramer and Donchin labeled the negativity peaking at 400 msec post-stimulus the N200 rather than the N400. They did this because they believed the component belonged to a family of negativities that are elicited by a stimulus mismatch. The original work with this mismatch

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the target. Thus, the N400 was largest for targets that differed from primes on both phonology and orthography. For targets matching the prime on a single dimension, either a rhyme with differing orthography or an non-rhyming orthographic match, an N400 of intermediate size appeared. The N400 was smallest for targets that matched the prime in both phonology and orthography. Kramer and Donchin claimed that their data supported the position that the N400 reflected the operation of a unitary process, sensitive to some general measure of ‘‘stimulus mismatch’’. One problem with the ERP conclusions from Kramer and Donchin (1987) was the lack of lateral recordings in their experiment. Rugg and Barrett (1987), who used bilateral recordings in an identical rhyme judgment task, gained additional information that allowed them to conclude that ‘‘two relatively independent sets of processes may be active during rhyme-judgments . . . those sensitive to orthographic relationships between word pairs . . . (and) other processes sensitive to the phonological relationships . . . (p. 354).’’ Rugg and Barrett found that the priming for orthography appeared to peak before 400 msec while the priming effect for rhymes appeared to peak after 400 msec. Additionally, the greatest amount of orthographic priming occurred over right frontal electrodes whereas the greatest rhyme priming appeared over parietal electrodes. Further evidence supporting the observations of Rugg and Barrett (1987) came from Forbes and Connolly (1995). These experimenters had subjects read sentences that ended with one of four categories, including: 1) semantically congruous, e.g., The planets circle the sun. 2) homophone foil of most probable ending, e.g., The planets circle the son. 3) orthographically similar to most probable ending, e.g., The planets circle the sea. 4) orthographically dissimilar from most probable ending, e.g., The planets circle the beach. Forbes and Connolly reported two separate priming effects, an N270 and an N400. Sentence ending words that were congruous or orthographically similar to congruent ending words produced smaller N270s over right frontal and right anterior temporal sites than orthographically dissimilar words. Sentence ending words that were phonetically appropriate (both correct endings and homophone foils) produced smaller N400s than phonetically inappropriate words. This effect was strongest over parietal and central sites. Thus, both Rugg and Barrett (1987) and Forbes and Connelly (1995) provide some evidence for a right anterior orthographic priming occurring somewhat earlier than a more posterior phonological priming effect. With the establishment of the N400 as a reliable index of normal brain functioning, researchers logically have begun to use this measure to examine language processing issues in various clinical populations. Since one of the most frequently cited deficits associated with specific reading disability is family found that a simple stimulus mismatch elicited a negativity at approximately 200 msec post-stimulus.

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phonological processing (e.g., Ackerman, Dykman, & Gardner, 1990; Wagner & Torgesen, 1987), this laboratory has recently engaged in a series of ERP studies utilizing rhyming stimuli to investigate phonological processing of disabled readers. In the first such study, Ackerman, Dykman, and Oglesby (1994) compared reading disabled subjects (average age 10 years) with similar aged normal readers in a task that required subjects to judge whether two sequentially presented visual stimuli did or did not rhyme. The first stimulus was always a word and the second stimulus was either an orthographically similar word or non-word. In order to ensure that subjects could read the word stimuli, simple three-letter, first-grade-level, words were used. Normal reading subjects did show a reduction in the N400 component for rhyming compared to non-rhyming stimuli. This N400 reduction for rhyming targets was widely spread across the scalp, but was strongest over parietal sites. The reading disabled subjects, however, failed to show this N400 priming effect for rhyming words. This provided the first ERP evidence of a possible phonological processing deficit in reading disabled subjects. However, this study did not manipulate the orthographic dimension. Therefore, the lack of N400 priming on the part of the reading disabled subjects might have been due to a deficit in phonological memory capacity, a poor ability to decode orthographic information into phonological information or perhaps even an orthographic deficit. McPherson, Ackerman, Oglesby, and Dykman (1996) followed this initial ERP investigation of phonological processes with a study that required adolescent reading disabled subjects to decide whether two sequentially presented pictures were of objects with names that rhymed or did not rhyme. Because no reading was necessary, entanglement of the orthographic and phonological dimensions was avoided. In order to address the issue of subtypes of reading disability, McPherson et al. divided the reading disabled subjects of the study into two categories based on their ability to decode non-words. The better decoders were called Phonetics and the poorer decoders were referred to as Dysphonetics. The Phonetics presented a facilitation, or N400 priming effect, but the Dysphonetics did not show such an effect. This priming effect was manifested as a reduction in the N400 component elicited by targets with names that rhymed with names of priming pictures, compared to target objects with non-rhyming names. The Phonetics’ N400 reduction for phonological matches was greatest over the left parietal site. These results provided ERP evidence for distinct sub-types of reading disability, a conclusion previously reached by many behavioral researchers (e.g., Wolf & Obregon, 1992). In an effort to better understand specific deficits in reading disabled individuals, the current study added three important dimensions to the rhyme judgment task of Ackerman et al. (1994), while keeping the sub-typing of reading disabled subjects adopted by McPherson et al. (1996). First, the or-

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thographic dimension was addressed through the use of rhyming and nonrhyming stimuli that vary on the orthographic dimension. Thus, like Kramer and Donchin (1987) and Rugg and Barrett (1987), four distinct target types occurred with equal probability. The recent results from Forbes and Connolly (1995) and the earlier report from Rugg and Barrett (1987) indicate that orthographic and phonological dimensions each contribute uniquely to ERPs of reading processes. Examining these separate dimensions in reading disabled subjects should provide a more specific locus for their poor ability to decode orthographic information into phonological code. The second addition to this study was the use of a separate block of auditory trials. The use of the auditory stimuli eliminated the reading factor and allowed a purer comparison between phonological processing in normal and disabled readers. If disabled readers’ phonological deficit was simply a difficulty in decoding orthographic information into a phonological code, then their ERPs to auditory phonological processing should be similar to normal readers’ auditory ERPs under similar conditions. However, if the phonological deficit of disabled readers was related to a problem in the phonological system itself, then disabled readers’ ERPs to auditory items should produce a similar pattern of differences as seen with visual materials. The final new development that this study provided was to include ERPs to the priming stimuli. Data from the primes provide information on prime storage and response preparation. Rugg (1984a) found evidence for a negative component just before the onset of visual targets (labeled a contingent negative variation, or CNV) that was greater over left anterior sites. Some researchers (e.g., Ruchkin, Canoune, Johnson, & Ritter, 1995) have suggested that this component may index short-term memory storage, since it has been shown to be modulated by memory load. However, others have claimed that the component simply reflects response preparation, because it appears before an imperative stimulus that follows a warning stimulus even when there is no memory load placed on the subject (e.g., Rockstroh, Muller, Wagner, Cohen, & Elbert, 1993). A deficit that involves storage and/or response preparation may present an ERP pattern that is distinct from a deficit in decoding orthographic information. The following predictions were made. For visual primes, the CNV may be reduced, especially at left anterior sites, in either or both of the reading disabled subgroups compared to normal controls (Rugg, 1984a). If the CNV is an index of short-term memory processes (Ruchkin et al., 1995), then the Dysphonetics might show a reduction in this component, provided their phonological deficit is due in some part to short term storage of phonological information. On the other hand, if the CNV is simply an index of response preparedness (Rockstroh et al., 1993), then the Phonetics may show a reduction. This prediction is based on reaction times found in McPherson et al. (1996), When making phonological decisions about picture names, the Pho-

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netics exhibited slower reaction times than the Dysphonetics, even though the Phonetics and not the Dysphonetics exhibited phonological priming. This suggests a deficit in response preparation on the part of the Phonetics. Based on the results of Rugg and Barrett (1987) and Forbes and Connelly (1995), in the visual task normal subjects should exhibit an anterior orthographic N400 priming effect and a more posterior N400 priming effect for phonology. Results from McPherson et al. (1996) suggest the Phonetics’ visual target ERPs should not differ from the Controls, but the Dysphonetics should show a deficit in phonological priming and perhaps a deficit in orthographic priming, depending upon the locus of the phonological decoding deficit. Given that this is the first study to contrast auditory rhyming in children, the ERP predictions for auditory stimuli are less specific than those for the visual paradigm. Examination of the CNV in auditory rhyme judgment paradigms has not been reported (Praamstra & Stegeman, 1993; Praamstra et al., 1994). However, the relative ease of the auditory paradigm, in comparison to the visual counterpart, may significantly reduce the CNV to these stimuli (Andreassi, 1995). Certainly, based on the work of Praamstra (Praamstra & Stegeman, 1993; Praamstra et al., 1994), normal readers should exhibit a posterior N400 priming effect for rhyming targets, but the issue of orthographic priming is unclear, due to the lack of ERP work investigating both the orthographic and phonological factors for auditory stimuli. In behavioral rhyme judgment studies (e.g., Zecker, Tanenhaus, Alderman, & Siqueland, 1986) researchers have shown that rhyming targets that share the same orthography as a prime are responded to more quickly than rhyming targets that have an orthography that differs from primes. It is unclear whether ERPs will prove sensitive to this manipulation. The matter of ERP priming for the reading disabled subjects is likewise less obvious for the auditory stimuli than for the visual. The two reading disabled groups were selected on the basis of their ability to pronounce written non-words, and thus the predictions for the groups on written material are straightforward. However, in the case of the auditory task predictions are less clear. One possibility is that the auditory ERP difference between the reading groups may not be great. METHODS

Subjects Thirty-two subjects participated, mean age 151/2 years, range 13 to 18 years. One-half of the subjects were diagnosed with a specific reading disorder, i.e., they read at least two years below age level but had a normal I.Q. These individuals had been referred to the study through the Child Study Center of Arkansas Children’s Hospital. The other subjects were controls age matched to the reading disabled group and with no reading deficits. They were recruited through advertising at Arkansas Children’s Hospital. To ensure that the students were either normal or disabled readers, the Woodcock Reading Mastery Test was administered (see Table

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TABLE 1 Group Ages and Test Scores Dysphonetic Woodcock Reading SS mean (se) Age in years/months mean (se–yrs) Decoding Skills Test mean (se) Bradley Oddity Test errors mean (se)

Phonetic

Control

76 (3.3)

77 (2.2)

103 (1.7)

15/4 (0.5)

15/2 (0.6)

15/4 (0.3)

25 (3.3)

39 (2.7)

not available

3.6 (1.1)

1.3 (0.5)

not available

Note. Test scores include Woodcock Reading Mastery Test standardized scores, Decoding Skills Test correct responses, and Bradley Oddity Test errors. Bradley Oddity Test (t[16] ⫽ 1.85, p ⬍ 0.10). Decoding Skills Test (t[16] ⫽ 9.75, p ⬍ 0.0001).

1). Subjects were paid a base rate of $20.00 plus 5 cents for each correct answer (see procedure). All subjects were native English speaking, and had normal or corrected-to-normal vision and normal hearing. Prior to enrollment into the study subjects were asked which hand they wrote with. Only right-handed subjects, as assessed in this manner, were included into the study. The running of subjects began in late October, 1993, and ran through early January, 1994. The order of reading disabled and normal readers was random. The reading disabled subjects were split at the median into two groups based on their total number of correct responses to pronouncing 60 nonwords on the Decoding Skills Test (Richardson & DiBenedetto, 1985). The lower scoring group was labeled Dysphonetic, and the group with a greater number correct was labeled Phonetic (see Table 1). However, the Phonetic group label only denotes relative superiority, since the average score for this group was lower than for younger (mean age 10) normal readers (Ackerman, & Dykman, 1993). Reading disabled subjects were also given the Bradley Oddity Test (Bradley, 1984), an oral assessment of sensitivity to rhyme and alliteration (i.e., which of four words does not sound like the other three). The Dysphonetic group, as expected, made more errors than the Phonetic group (see Table 1). The average reading level of the two reading disabled groups did not significantly differ, nor did the average ages of the three groups differ (see Table 1). There were 3 females in the Dysphonetic group, 2 females in the Phonetic group, and 4 females in the Control group.

Procedure Subjects were seated in a comfortable chair in an electrically isolated and sound attenuating room, as they completed rhyming tasks in separate auditory and visual blocks. One-half of the subjects in each of the groups completed the auditory tasks first and the others completed the visual portion first. The subjects were given a 10 minute break with a chance to move around and get a drink after the first block was completed. Additionally, short (approximately one minute) breaks were given during each block after approximately every 40 trials. Two push buttons for entering responses were located on the arms of the chair in which the subjects were seated. Subjects were instructed to place their index fingers over these buttons. Participants were told that they would hear (or see) two words, one word followed one-half second later by a second word. Half in each group were instructed to press the right button whenever two words rhymed and to press the left button whenever the two words did not rhyme. The other half received opposite instructions (left for rhyme, right for non-rhymes). Examples of rhyming and non-rhyming words were verbally given. It was emphasized to each

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subject that some rhyming words did not have the same ending letters (e.g., chew-true), and that some non-rhyming words has the same ending letters (e.g., hood-food). Examples of such exception rhyming and non-rhyming word pairs were verbally given (i.e., the words were spoken and then spelled). After these examples the subjects were told to ‘‘remember to make your response based on the way the word sounded and not necessarily on the way it was spelled.’’ Subjects were also told to respond as soon as they were able to determine the right answer, and that if they had not responded by the end of three seconds the computer would count that as a wrong response. Finally, subjects were told that for each correct response within 3 seconds, 5 cents would be added to the total amount of money to be paid to them, but for a wrong response their money total would remain the same. At the end of the 3 seconds after the second word, the computer put a message on the screen as to whether a correct response had or had not been given. For each block of trials subjects were given a group of 12 practice trials. No ERPs were recorded to these trials, although subjects were rewarded for correct responses. In the visual task a stimulus presentation program running under a 68030 Compupro microcomputer presented pairs of words. Each pair of words was preceded by a warning signal (a green cross) which appeared 1 sec before the first word onset and lasted 500 msec. The words had a duration of 800 msec. The individual word onsets were separated by an interval of 1300 msec., and trials were separated by 5 sec. The words were presented on a computer monitor at a distance of 6 ft. in front of the subject. The words subtended a visual angle of approximately 1° on the vertical and 3° on the horizontal. In the auditory task the Compupro microcomputer strobed a i486 based IBM compatible microcomputer which presented the auditory words through a Sound Blaster sound card. The words were output over a speaker placed in the ceiling of the room approximately 4 ft directly over the subject’s head. The volume level of all auditory words was approximately 75 dB. The words were spoken by a male speaker at a normal conversational rate. The timing of the presentation of the auditory words followed a pattern similar to visual words. A green cross appeared on the computer monitor 1 sec before the first word. The onset of the second word began 1300 msec after the first. Average duration of the spoken words was 580 msec, and the range was from 390 msec to 820 msec. For each task one of two lists of rhyming words was used. One-half of the subjects in each group had List 1 in the auditory modality and List 2 in the visual modality. For the other subjects the lists reversed modalities. Both lists consisted of 160 pairs of common one syllable words listed as first through six grade (Johnson, Moe, & Baumann, 1983) with the average being 2.4. Many of these pairs appeared in Polich, McCarthy, Wang, and Donchin, (1983), Zecker et al. (1986), and Rugg and Barrett (1987). The second word, or target, fell with equal probability into one of the following four relationships with the first word: (1) an orthographically similar rhyming word, e.g., gift-lift, (2) an orthographically dissimilar rhyming word, e.g., dirt-hurt, (3) an orthographically dissimilar non-rhyming word, e.g., sing-door, and (4) an orthographically similar non-rhyming word, e.g., most-lost. The practice list contained 3 words from each of the four conditions. Word lists and sub-lists of primes and targets differentiated by target conditions were balanced for familiarity (frequency of occurrence), length and grade level. ERP recording. Subjects were fitted with an electrode cap (Electrode-Cap International) to hold the 10 active electrodes to the scalp. The locations for these electrodes included six standard international 10–20 system locations. These six consist of three pairs, F3 and F4, P3 and P4, and O1 and O2. The remaining four non-standard scalp sites were temporal-centralparietal (TCP1 and TCP2), and frontal-temporal-central (FTC1 and FTC2). TCP1 and TCP2 were located approximately over Wernicke’s area and its right hemisphere homologue. FTC1 and FTC2 were located approximately over Broca’s area and its right hemisphere homologue. These were used because of their connection to language processing. All sites were referenced to the left mastoid, and the impedance between each recording site and the reference was reduced to below 5K ohms. Two final electrodes were placed on the skin to monitor for eye movements. One, placed beneath the left eye, checked for eye blinks and vertical eye move-

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TABLE 2 Behavioral Results

Visual Reaction Times (in msec) mean (se) Auditory Reaction Times mean (se) Visual % Error Mean (se) Auditory % Error Mean (se)

Dysphonetic

Phonetic

Control

1360 (49) 1125 (58) 17.5 (4.5) 6.2 (2.8)

1615 (77) 1370 (83) 18.9 (3.6) 6.9 (2.2)

1122 (41) 1059 (35) 3.1 (0.8) 2.0 (0.6)

Note. A summary of behavioral results including reaction times and error rates for the three groups in the two separate paradigms.

ments, and the other, placed to the right of the subject’s right eye, checked for lateral eye movements. EEG was recorded for 21/2 sec of each trial including the 100 msec before the presentation of the prime and running continuously until 1100 msec after target onset. The EEG signal was amplified by a Grass Model 12 Neurodata Acquisition system using a bandpass filter with ⫺3dB cutoffs of 0.3 Hz and 100 Hz. The amplified EEG was then sent to a Compupro 68000 microcomputer equipped with an analog to digital converter. The computer digitized the EEG at a rate of 256 Hz and stored the data on magnetic tape, as well as displayed the EEG for each trial on a computer monitor after each trial. On-line checking for eye artifact provided feedback on the quality of the data. Correctness and reaction time of responses were recorded and stored by the computer. EEG epochs for each target condition were averaged separately using a digital low-pass filter with ⫺3dB cutoff of 30 Hz to form the ERPs for the respective condition. All target epochs free from artifact due to eye movements and for which a correct answer was provided between 300 and 3000 msec after the onset of the response signal were included in the data analyses. Separate averages of artifact free primes for each of the two separate modalities were also formed.

Behavioral Data The complete behavioral data are reported elsewhere (McPherson et al., 1997), but a brief review of the significant relevant findings are included here. Both reading disabled groups committed a significantly greater number of errors than the normal reading group for both modalities. The Phonetic group responded significantly slower than both of the other groups in both of the tasks. The Dysphonetic group was slower than the Control group in the visual but not the auditory task (see Table 2).

Data Analysis Data analyses were performed using BMDP’s 4V ANOVA program for analyses with repeated measures. For all repeated measures with greater than 1 degree of freedom, the GeisserGreenhouse correction (Geisser & Greenhouse, 1959) was applied to correct for any violations of the sphericity of variance assumption. Within subjects factors included: 1) modality (df ⫽ 1), visual and auditory, 2) hemisphere (df ⫽ 1), left and right, 3) electrode site (df ⫽ 4), frontal, FTC, TCP, parietal, occipital, and for targets 4) orthography (df ⫽ 1), similar and dissimilar ending letters, and 5) phonology (df ⫽ 1), rhyming and non-rhyming. Since the ERP data differed greatly between the two modalities, two separate analyses were completed, one on the visual ERPs and one on the auditory ERPs. All ERP epochs were referenced to the average values from 50 msec pre-stimulus to 50 msec post-stimulus. Since ERP waveforms naturally vary a great deal from one electrode site to another, a main effect for electrode site is almost always present in any ERP analysis. These main effects are not reported.

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FIG. 1. ERPs elicited by primes in the visual rhyme judgment task. Waveforms show the average for the three separate groups from 100 msec prior to prime onset until target onset for five bilateral pairs of scalp sites, including Occipital (O1, O2), Parietal (P3, P4), Wernicke’s area and its right hemisphere homologue (TCP1, TCP2), Broca’s area and its right hemisphere homologue (FTC1, FTC2), and frontal (F3, F4). Recordings from the left side of the scalp are shown on the left. For follow-up analyses that involved a group interaction with a single measure, BMDP’s 7D program for pairwise group comparisons (t-tests) was used. The Bonferoni adjustment was used to reduce Type I errors. Thus, with 3 group comparisons the ‘‘p’’ value of significance was 0.05/3 ⫽ 0.02. ERPs to priming words. The auditory primes revealed no statistically reliable differences for the N400 (300 to 500 msec post stimulus) or CNV (200 msec prior to target onset). For the visual primes, the only significant difference came immediately before target onset during the epoch that is typically labeled the CNV (see Figure 1). The analysis of the mean amplitude during the 200 msec prior to the target stimulus produced a main effect for group (F[2,29] ⫽ 7.66, p ⬍ 0.005). Since there were no significant interactions with the electrode site factor, the follow-up analysis compared group mean amplitudes of this epoch, averaged across all sites. The comparisons indicated a significant difference between the Controls and Phonetics (t[29] ⫽ 2.91, p ⬍ 0.01), and a trend in the same direction between Dysphonetics and Phonetics (t[29] ⫽ 1.92, p ⫽ 0.06). The Controls produced the most negative CNV and the Phonetic group had the only positive mean CNV (see Figure 1). ERPs to the targets in the visual rhyme paradigm. For normal reading control subjects, the morphology of the ERPs evoked by the target stimuli in the visual rhyme paradigm closely follows that reported by Kramer and Donchin (1987) and Rugg and Barrett (1987) (see Figure 2). Starting somewhere between 200 to 250 msec the ERPs to the various conditions begin to diverge. All conditions begin to get more negative beginning with the frontal sites and proceeding later with posterior sites. This negativity peaks at approximately 350 msec. The targets orthographically and phonetically different than the primes become negative sooner

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FIG. 2. ERPs elicited by targets in the visual rhyme judgment task. Waveforms show the average for normal reading Controls in the four separate conditions: (1) P⫹O⫹, orthographically similar rhymes; (2) P⫹O⫺, orthographically different rhymes; (3) P⫺O⫹, orthographically similar non-rhymes; (4) P⫺O⫺, orthographically different non-rhymes. and to a much greater extent than targets that are primed on both dimensions i.e., orthographically and phonetically similar to primes. Targets primed on a single dimension show a negativity that is somewhere between that elicited by the unprimed stimuli and the doubly primed stimuli. As in Rugg and Barrett (1987) and Forbes and Connelly (1995), the data analyses of the targets were broken into two separate epochs, one to measure the orthographic priming and the other to measure rhyme or phonological priming. The best window for measuring these separate effects appeared to be from 270 to 400 msec post-stimulus for the orthographic effect, labeled N350, and 400 to 500 msec post-stimulus for the phonological effect, labeled N450. The mean amplitudes for these epochs were used as the dependent measure in separate ANOVAS. For the normal readers the greatest orthographic priming appeared over the right frontal site and the greatest phonological priming appeared over the left parietal site. Figure 3 shows the difference waves that succinctly display these priming effects for all three groups at these sites. N350 analysis. Greater negativity to non-rhyming targets as well as to orthographically nonmatching targets produced two main effects, one for phonology (F[1,29] ⫽ 14.05, p ⬍ 0.001) and one for orthography (F[1,29] ⫽ 24.18, p ⬍ 0.0001). The main effect for orthography was tempered by several important interactions. A strong orthography by electrode site interaction (F[4,116] ⫽ 13.23, p ⬍ 0.0001) developed as a result of a greater orthographic priming over anterior sites compared to the posterior sites (see Figure 4). Additionally, there was an orthography by hemisphere (F[1,29] ⫽ 5.52, p ⬍ 0.05) interaction brought on by greater orthographic priming over the right hemisphere. This last effect is mediated by a three-way interaction between orthography, hemisphere, and group (F[1,29] ⫽ 4.19, p ⬍ 0.05) caused by the Phonetic group’s reversal over central sites. Over left central sites the Phonetics show the strongest

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FIG. 3. Difference waves for the three groups showing phonological priming effect over the left parietal site, P3 (left) and orthographic priming effect over the right frontal site, F4 (right). The phonological priming effect is the average difference between ERPs to targets rhyming with the prime and ERPs to targets that did not rhyme with the prime. The orthographic priming effect is the average difference between ERPs to targets with an orthography (ending spelling) similar to the prime and ERPs to targets with an orthography different than the prime.

orthographic priming but over the right hemisphere they have little more than the Dysphonetics, who show the weakest priming. The phonology factor was also involved in two key interactions. An interaction between phonology and group (F[2,29] ⫽ 4.42, p ⬍ 0.02) developed because Dysphonetics exhibited significantly less priming than the other groups, based on mean N350 of rhyming targets subtracted from non-rhyming targets averaged across all sites (Dysphonetics ⬍ Phonetics, t[29] ⫽ 2.62, p ⬍ 0.02; Dysphonetics ⬍ Controls, t[29] ⫽ 2.58, p ⬍ 0.02). Additionally, greater phonological priming over the right hemisphere produced a phonology by hemisphere interaction (F[1,29] ⫽ 9.18, p ⬍ 0.01). N450 analysis. The N450 analysis revealed a main effect for phonology (F[1,29] ⫽ 19.15, p ⬍ 0.001) due to larger negativities for non-rhyming targets. Several significant interactions modulated this effect, including an interaction of phonology and group (F[1,29] ⫽ 4.65, p ⬍ 0.05). Based on the mean N450 of rhyming targets subtracted from non-rhyming targets averaged across all sites, the Dysphonetics exhibited significantly less rhyme priming than Controls (t[29] ⫽ 2.87, p ⬍ 0.01), and somewhat less priming than the Phonetics (t[29] ⫽ 2.40, p ⬍ 0.03). Additionally, there was a phonology by electrode site interaction effect (F[1,29] ⫽ 3.95, p ⬍ 0.05) caused by stronger phonological priming over parietal sites (see Figure 5). The only significant effect involving orthography was a four-way interaction between phonology, orthography, hemisphere, and group (F[1,29] ⫽ 4.89, p ⬍ 0.01). In order to better understand this complex interaction effect, a separate analysis was run for each group. The Dysphonetic subjects revealed no significant effects. The Phonetics’ N450 did produce both a main effect for phonology (F[1,6] ⫽ 10.17, p ⬍ 0.05), and an interaction effect for orthography and hemisphere (F[1,29] ⫽ 25.35, p ⬍ 0.005). Greater negativity for non-rhymes (rhyme priming) produced the phonology effect. The orthography by hemisphere interaction resulted from a lack of any significant right hemisphere orthographic priming (F ⬍ 1, p ⬎ 0.35), but near significant left hemisphere orthographic priming (F[1,6] ⫽ 4.60, p ⬍ 0.10). An examination of the Control data also revealed a main effect for phonology (F[1,15] ⫽ 9.36, p ⬍ 0.05) caused by rhyme priming, and the interaction effect of orthography by hemisphere (F[1,15] ⫽ 5.88, p ⬍ 0.05). However, this interaction indicated a different pattern than the Phonetics’ analysis. Orthographically primed targets were somewhat more negative (more ‘‘reverse’’ priming) over the right hemisphere compared to the left hemisphere (see Figure 5).

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FIG. 4. The phonological and orthographic priming effects, mean ERP values from 270 to 400 msec post target onset, in the visual rhyme judgment paradigm. Values for the separate hemispheres and sites are shown for the individual groups.

ERPs to targets in the auditory rhyme judgment paradigm. The morphology of the target ERP waveforms for the Controls shows a reduced N400 over frontal sites compared to the primes (see Figure 6). The phonological priming effect appears to start at approximately 300 msec post-stimulus over parietal and occipital sites and somewhat later at other sites. The auditory phonological priming effect is smaller than the equivalent visual effect. The epoch selected to measure the effect was the same as in the visual paradigm, 400 to 500 msec. The

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FIG. 5. The phonological and orthographic priming effect, mean ERP values from 400 to 500 msec post target onset, in the visual rhyme judgment paradigm. Values for the separate hemispheres and sites are shown for the individual groups.

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FIG. 6. ERPs elicited by targets in the auditory rhyme judgment task. Waveforms show the average for normal reading Controls in the four separate conditions: (1) P⫹O⫹, orthographically similar rhymes; (2) P⫹O⫺, orthographically different rhymes; (3) P⫺O⫹, orthographically similar non-rhymes; (4) P⫺O⫺, orthographically different non-rhymes.

overall analysis on the mean amplitude for this epoch revealed a main effect for phonology (F[1,28] ⫽ 6.86, p ⬍ 0.01) caused by a greater negativity elicited to non-rhyming targets compared to rhyming targets. Even though a reaction time orthographic priming effect occurred for all groups (McPherson, Ackerman, & Dykman, 1997; see also Zecker, 1991), no such ERP effect materialized (F[1,29] ⫽ 0.01, p ⬎ 0.90). A significant interaction between phonology, hemisphere, and group (F[2,29] ⫽ 3.81, p ⬍ 0.05) justified separate group analyses. Figure 7 shows the difference waves illustrating the auditory phonological priming effect. The analysis of the Dysphonetic group produced a main effect for phonology (F[1,8] ⫽ 11.80, p ⬍ 0.01). The Control group produced a significant phonology by hemisphere interaction (F[1,15] ⫽ 6.44, p ⬍ 0.05). Two follow-ups, one for each hemisphere, revealed no significant right hemisphere effects for Controls, and a near significant left hemisphere main effect for phonology (F[1,15] ⫽ 4.05, p ⬍ 0.06). Phonologically primed targets were less negative than unprimed targets. The Phonetics produced no significant phonological priming. This group actually had a trend in the opposite direction of the normal N400 priming effect for anterior sites. Table 3 gives a summary of important ERP results.

DISCUSSION

The results from the ERPs elicited during the visual rhyme judgments support Rugg and Barrett’s (1987) and Forbes and Connelly’s (1995) position for separate ERP components for orthographic and phonological processing. Normal reading Controls and the reading disabled Phonetic group

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FIG. 7. ERP difference waves showing the priming effect for rhymes in the auditory rhyme judgment task over P3, P4, TCP1, and TCP2 sites (the later two are Wernicke’s area and its right hemisphere homologue). Waveforms show group average differences between ERPs to targets that rhymed with the prime and ERPs to targets that did not rhyme with the prime.

both show visual orthographic and phonological ERP priming. However, the data that strengthens the claim that these ERP orthographic and phonological priming effects reflect independent cognitive processes is the Dysphonetic group’s display of strong frontal orthographic priming, but lack of left posterior phonological priming. A reduction in the amplitude of the N400 of a primed stimulus has been interpreted within different frameworks, including spreading activation within a memory network and a post-lexical integrative process. One early conceptualization of the N400 priming (e.g., Kutas & Hillyard, 1984) theorized that when subjects read a word (e.g., ring), other words with a close semantic or phonological relationship, (e.g., semantic–finger, bell; phonological–sing, king), presumably receive some degree of activation; consequently if the priming word is followed by a related word, less activation is necessary for recognition, i.e., a reduction in the N400 component, compared TABLE 3 ERP Results Summary Dysphonetic Mean Visual CNV F3&4, FTC1&2 Mean Visual N350 ortho priming, F4 Mean Visual N450 phono priming, P3 Mean Auditory N450 phono priming, FTC1&2, P3&P4

⫺1.1 3.4 0.8 2.0

(0.5) (1.2) (0.6) (0.5)

Phonetic 1.5 5.3 2.6 0.6

(1.2) (2.1) (0.8) (0.7)

Control ⫺1.3 4.3 3.3 1.2

(0.6) (0.9) (0.6) (0.8)

Note. A summary of important ERP results including CNV, N350 orthographic priming and N450 phonological priming to visual stimuli, and the N450 phonological priming for auditory stimuli. All values are in microvolts with the standard error of the mean shown in parentheses.

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to whenever the prime is followed by a non-related word. More recently the amplitude of the N400 has been characterized as reflecting effort in a postlexical integration process (e.g., Brown & Hagroot, 1993; Holcomb, 1993). This concept is easily applied to explain the reduction of N400 as context builds in a sentence. The final words elicit the smallest N400 because the context for these words has been fully developed and they are easily integrated. Middle words have an intermediate N400 because context is only partially developed, and beginning words, in absence of any context development, have the largest N400. In this experiment the explicit context was a decision of whether two words did or did not rhyme, and a reduction in N400 elicited by rhyming words might be explained by easier integration into this context. However, the orthography provided no useful information about the decision (50% of orthographically matching and 50% of orthographically mis-matched word pairs rhymed). Yet orthographically matching targets elicited smaller frontal N400s than orthographically mismatched targets. Perhaps the orthographic priming took place at a lexical level, through the activation of words with similar orthographic endings. The semantic representation of these primed words may also have been activated and thus easier to integrate. The N350 reduction could reflect this easier integration. In other words even though the ‘‘context’’ did not require semantic evaluation, such evaluation may have automatically occurred. The differential ERP effects of orthography and phonology revealed in the visual paradigm allow a portrayal of the cognitive processes involved in reading for phonological content. The orthographic priming pattern witnessed suggests that the recognition of orthography is controlled or modulated through frontal processes, perhaps associated with sub-vocal articulations (Carr & Posner, 1991). The connection between frontal activity and orthographic processing has been reported by other researchers (e.g., Barkley & Grodzinsky, 1990; Denckla, 1996; Rugg & Barrett, 1987; Forbes & Connelly, 1995). For normal readers, the information from the orthographic processing is then apparently transferred to an area adjacent to temporalcentral-parietal in the left hemisphere, or perhaps both hemispheres, where presumably phonological decoding then takes place (Posner, Petersen, Fox, & Raichle, 1988; Wood, Flowers, Buchsbaum, & Tallal, 1991, but see Crossman & Polich, 1988 & Gazzaniga, Kutas, Van Petten, & Fendrich, 1989). The investigation of auditory ERP rhyming effects did not prove as elucidating as the visual analogue. No orthographic priming was evident for auditory targets and the phonological priming was reduced in comparison to visual rhyme priming. One problem that may have contributed to the less significant auditory findings may be ERP variability due to age differences. Holcomb, Coffey, and Neville (1992) have shown some developmental differences in the N400 component between ages 13 and 18 for ERPs elicited

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by auditory verbal stimuli. Thus, it would seem prudent to reserve judgment about possible ERP effects due to orthographic priming in auditory rhyme judgments. A more homogeneous sample would be better suited for detecting what might be a small effect (Zecker et al., 1986). Even though ERP rhyme priming was reduced for auditory stimuli, it still differentiated the groups, although in a manner not expected. The Phonetics’ slightly better performance at the Bradley Oddity Task (Table 1) indicated that this group could process auditory phonological information somewhat better than the Dysphonetics. However, the Bradley Oddity Task invokes a greater memory load than the rhyme judgment task (four stimuli compared to two), and the easier rhyme judgments might have been within the Dysphonetics’ capacity. That could account for the presence of auditory rhyme priming in the ERP records of the Dysphonetics, but it does not explain the lack of such effects for the Phonetics. Although no clear explanation exists for this lack, it may be coupled in some way to the slow processing exhibited by the Phonetics. The Phonetics displayed a constellation of findings that distinguished the group as lacking resources for a timely response. The reduced CNV before visual targets, the slower reaction times for both the visual and auditory rhyme judgments of this study, as well as reduced CNV in a visual alliteration judgment task, and slower reaction times in both visual and auditory alliteration judgment tasks (McPherson, 1995) are all part of this pattern. Furthermore, the Phonetic group’s reduction in CNV and increased response latencies are not just in relationship to normal reading Controls, but in comparison to the Dysphonetic group as well. Additional support for a reduction in processing speed for the Phonetic group is shown in the ERPs to the visual targets of this study. This slowness of processing is manifest in the prolonged priming effects for both orthographic and phonological priming. Figure 3 clearly shows the continuation of the phonological priming effect for the Phonetic group over the left hemisphere compared to the other groups, and the ANOVA of the 400 to 500 msec target epoch, revealing orthographic priming only for the Phonetics, supports this slowness interpretation. All three groups exhibit orthographic priming in the earlier epoch (270 to 400 ms) but only the Phonetics continue this priming into the later time period. This is not the first study to show a possible processing delay in orthographic information for dyslexics. Salmelin, Service, Kiesila¨, Uutela, and Salonen (1996) reported missing or delayed processing of visual word information in left inferior temporo-occipital cortex based on a magnetoencephalography (MEG) study of a small group of dyslexics. This discrepancy from normal MEG started at approximately 180 ms post stimulus. ERPs to the visual priming words in the present study (see Figure 1) do suggest a difference between normal and dyslexics at this point over parietal sites; however,

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these differences were not statistically significant. The nature of ERP technology (i.e., surface recordings) may account for the differences between these ERP and MEG findings. The Phonetics showed no significant phonological priming between 400 and 500 ms of the auditory target epoch, but there does appear to be a modest delayed posterior priming effect peaking at 725 ms. It is not clear why the Phonetics failed to show normal priming, since they did exhibit normal visual priming, but their slower processing rate could be involved. The reduced auditory priming effect appears to be slow to start and reach a peak. However, by itself, this does not account for the total reduction in the magnitude of the priming, and the reversal of the effect over left anterior sites. Another factor that may be involved is the comparative ease of the auditory task. All groups had fewer errors and faster reaction times for the auditory task compared to the visual task (see Table 2). Both the Phonetic and Dysphonetic group had 1/3 fewer errors and responded, on average, approximately 240 msec faster to the auditory targets. Why an easier task would reduce priming effects is uncertain; however, the area that seems to be most affected in the Phonetics, i.e., left anterior (see Figure 7), does have links with response preparation (Rugg, 1984a). The relationship, if any, between reduced auditory phonological priming and easier response preparation is, however, uncertain. In contrast to the Phonetics, the Dysphonetics exhibited significant auditory ERP phonological priming, but no visual ERP phonological priming. The lack of phonological priming in the visual paradigm for the Dysphonetics was expected, since this group was defined by its poorer ability to decode orthography to phonological code, and their ERPs provided evidence for the locus of the deficit. The presence of orthographic priming indicated that the orthographic code was being adequately stored and/or activated. A lack of phonological priming in the presence of orthographic activation suggests either poor decoding ability, or perhaps a reduced capacity to hold phonological codes in working memory. However, the presence of phonological priming in the auditory paradigm would indicate that these subjects could adequately hold phonological code in working memory. Thus, the combined results of the two paradigms point to a decreased proficiency at decoding orthography into phonology, as the locus of the phonological processing deficit in this group. Differential group results also allowed inferences on the nature of the cognitive processing responsible for the CNV component. The current results appear to support the position that the CNV is a marker of response preparation (e.g. Rockstroh, et al., 1993), rather than the claim that this component is an index of memory load (Ruchkin et al., 1995). If the CNV is an index of response preparation, then other factors being equal, a reduction of this component would mean a reduction in response preparation, and conse-

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quently an increased response latency.2 The Phonetic group’s CNVs elicited before visual targets and the reaction times for responses to these targets fit this pattern. If the CNV were an index of memory load, then the smaller CNV of Phonetics, compared to Dysphonetics, would reflect a smaller memory activation. However, the Phonetic’s greater reduction in the N400 for the rhyming stimuli, compared to Dysphonetics, suggests greater activation, based on the above argument about the nature of the N400. CONCLUSION

Recent behavioral studies (Ackerman & Dykman, 1993, 1996; Wolf & Obregon, 1992) have reported that phonological processing ability and speed of processing, as indexed by rapidly naming items, contribute separately to reading disability. This study supports these findings and provides ERP evidence for two distinct abnormal brain processes in a reading disabled population, one associated with a phonological processing deficit and a separate one connected with a speed of processing deficit. The reading disabled subjects who did poorly on decoding non-words (i.e., the Dysphonetics) exhibited ERP orthographic priming that indicated adequate orthographic processing capabilities. However, their subsequent lack of normal phonological priming points to a deficit in decoding orthographic material into phonological code. The disabled readers with better phonological decoding ability (i.e., the Phonetic group) presented several pieces of evidence for a deficit in processing speed, including increased response latencies, prolonged and/or delayed priming, and a reduction in the CNV component. This latter component apparently indexed response preparation. These results also provide fodder for ongoing debates about normal brain processes. The tenet that orthographic and phonological processing manifest distinct ERP patterns has been given strong support. If they were not independent, the Dysphonetics could not manifest one, but not the other of these patterns. Additionally, the Phonetic’s reduction in CNV, coupled with the significant N400 priming and increased response latencies, associates the CNV component found in the visual paradigm not with memory activation, but rather with response preparation. Finally, an important implication of these results concerns reading remediation programs. Such programs, when designed for primarily a phonological processing deficit, may not provide proper procedures or drills for those with a speed of processing deficit. Future ERP work conducted on a larger reading disabled population and employing more extensive behavioral testing should 2 This relationship, i.e., longer reaction times and smaller CNV, is only assumed true within a given task. For different tasks, this may not be the case. For example, the CNV in the auditory task was reduced compared to the visual task, but the reaction times were shorter. In this case the reduced CNV indicated an easier task, and this was reflected by shorter reaction times.

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