Event-related potentials and repetition priming in young, middle-aged and elderly normal subjects

Cognitive Bruin Research, l(1993) 123-134 0 1993 Elsevier Science Publishers B.V. All rights reserved 0926-6410/93/$06.00

123

BRESC 30007

Event-related

potentials and repetition priming in young, middle-aged and elderly normal subjects

Frini Karayanidis

a, Sally Andrews a, Philip B. Ward b and Neil McConaghy b

’ School of Psychology, Uniuersity of New South Wales, Kensington, NSW (Australia) and b School of Psychiatry, Prince of Wales Hospital, Kensington, NSW (Australia)

(Accepted 29 December 1992)

Key words: Aging; Word recognition; Repetition priming; Lag effect; Event-related

potential; Late positive component; N400

Although the structure of semantic memory appears to be unaffected with increasing age, there is evidence that older adults are less efficient at accessing stored memory representations. Aging also results in a decline in the ability to use contextual information effectively, suggesting a deficit in episodic memory processes. The present experiment examines the effects of age on memory retrieval of stored representations and the use of contextual information. Event-related potentials (ERP) were recorded to immediate and delayed word repetition during a lexical decision task. Three groups of subjects were tested: young (mean = 27.3 years), middle (mean = 46.7 years) and old (mean = 67.4 years). Behavioral facilitation due to repetition did not significantly differ across groups. With increasing age, the ERP waveform showed a positive shift which began around 300-400 ms post-stimulus and was apparent across all stimulus types and response conditions. This positive shift may reflect an age-related decrease in cortical excitation. Although the onset of the ERP repetition effect was not affected by age, its duration for both immediate and delayed repetition was significantly prolonged. In the light of recent models of ERP word repetition effects, these results suggest that processes related to accessing stored representations in memory are unaffected by age. The extended duration of the repetition effect and the increase in the magnitude of the effect of delayed repetition with age suggest that aging affects processes related to the retrieval and use of contextual information in integrating a stimulus with its context.

diate than delayed word pronunciation suggests that age has an effect on lexical access over and above its effects on response processes (ref. 2, but also see ref. Although there is ample evidence for a decline in memory performance with increasing age, the cognitive 17). The semantic priming effect also shows a conprocesses underlying this deficit remain unclear. The sistent but statistically non-significant increase with structure of semantic memory and spreading activation Since the size of the semantic priming between related concepts within semantic memory are age 12,14,17,30,39. generally unaffected by age’2~14~‘s~18~19~21~29~30~39~40. There effect is inversely related to the rate of lexical processing 67, this finding is consistent with an age-reis some evidence, however, that lexical access, or the lated delay in lexical processing mechanisms2,39. Fitime required to access a representation in memory, is delayed with increasing age. nally, an effect of age on lexical access is suggested by In semantic priming studies, aging is associated with age-related difficulties in retrieving a word to fit a a significant delay in lexical decision time (i.e. the time specified definition’* and naming line drawings of simple objects”,50. required to decide whether the target is a real or a pseudo_word)‘*,‘4,30,31,39. A sizeable portion of this difIn addition to the evidence that age affects lexical ference in response time may be attributed to a generaccess, there is also evidence that aging produces a specific deficiency in episodic memory processes. In alized slowing of both cognitive and motor processes2962. particular, older subjects appear to be less efficient in However, the fact that age effects are larger for immeINTRODUCTION

Correspondence:

399-6664.

F. Karayanidis, School of Psychology, University of New South Wales, P.O. Box 1, Kensington, NSW 2033, Australia. Fax: (612)

124 recalling contextual information and do not adequately use such information to assist memory performance3,13*22,33*53,65. An age-related deficit on tasks that depend on episodic memory mechanisms (e.g. free recall and recognition memory) has been demonstrated for the same stimuli and in the same subject groups for which semantic priming was found to be intaCt14,15,29,30.39,47

Although the above studies strongly suggest that age specifically affects the efficiency of episodic memory processes, it is possible that these results reflect interactions between age and the effects of task difficulty. The tasks used to assess semantic memory (e.g. semantic priming) are, on the whole, easier and require less effortful processing than tasks used to measure episodic memory (e.g. free recall). Task complexity is an important factor in determining the occurrence of agerelated cognitive deficits1,4s*61,63,71. To investigate the effects of age on lexical and episodic processing mechanisms without the confounding effects of task difficulty, the present study uses ERP recording in a word repetition paradigm. A continuous performance lexical decision paradigm was employed with word repetitions occurring either immediately or with an inter-item lag of four. In word repetition paradigms, the initial presentation of a word enhances behavioral performance to subsequent presentations of that same word23*64.This effect of word repetition has been interpreted within the context of both lexical and episodic memory mechanisms, with recent models advocating the contribution of both mechanisms. Specifically, it has been proposed that the large facilitation produced by immediate word repetition results primarily from repeated access to the same lexical entry, whereas long-delay repetition effects reflect re-accessing of the episodic memory trace that was established during the first presentation of the item25’54. The word repetition effect is reflected in the ERP waveform as an attenuation of the negative deflection that is evident upon the first presentation of a word6*37,55,58,59. This component has been identified as the N400 wave which was initially observed to be evoked by semantic incongruity in semantic priming paradigms34,35. In a recent interpretation of the ERP repetition effect, Van Petten et al. 68 characterize the N400 as “a rather ubiquitous marker of lexical processing” (p. 140). They argue that the behavior of N400 is compatible with abstractionist models of word repetition which emphasize that changes in the activation threshold of the word’s representation are independent of the context in which the word occurs. According to this model,

N400 amplitude is sensitive to a “rather indiscriminate collection of evidence for the presence of a particular word” (p. 140). In the word repetition paradigm, the N400 is followed by a late positive component (LPC) which is also sensitive to repetition. Studies in which words are repeated in list contexts have consistently shown an enhancement of this positivity for repeated words7,32,49*s6-60. The fact that word repetition results in a decreased negativity and an increased positivity has raised the question of whether these two components are indeed separable, or whether a prolonged positivity elicited by repeated items is superimposed on Two lines of evidence argue both components 56*58,59. that the N400 and LPC are separate components. Depth recordings have shown that it is possible to record from sites where only one or the other component is visible@. More recently, Van Petten et a1.68 found that word repetition within text resulted in a biphasic repetition effect reflected in a reduction in the amplitude of both the N400 and the LPC. Van Petten et a1.68 explain the apparent conflict with previous findings by assuming that the LPC increases with demands of retrieval and updating processes. They argue that, in studies examining repetition in word lists or isolated sentences, the first presentation of a word places a light load on working memory, whereas word repetition engages retrieval and updating processes reflected in an increased LPC with repetition. However, when words are repeated in normal text, the working memory load is heavier for the first presentation of the word than when it is repeated and therefore the amplitude of the LPC decreases with repetition. On this basis, Van Petten et a16* propose that the LPC “indexes the updating of working memory with information retrieved from long-term memory” (p. 142). The word repetition task provides an ideal task for assessing age-related changes in lexical access and contextual information processes. The simplicity of the task reduces the number of extraneous variables that may contribute to any observed age effects, such as differential effect of task difficulty, contribution of motor impairment etc. Additionally, the comparison of short and long-lag repetition and the use of ERP recordings allow investigation of the effect of age on lexical access and episodic memory mechanisms using a task that does not explicitly require the use of contextual information. As discussed earlier, dual-process models of word repetition argue that the immediate repetition effect reflects the facilitation of lexical processing as a result of re-accessing the same lexical entry, whereas the

125 long-lag repetition effect depends on the re-instatement of contextual cues associated with the initial occurrence of the word and therefore primarily reflects episodic memory processes. Within this framework, an age-related disruption of lexical activation processes will be reflected in an attenuation of both immediate and delayed repetition effects. If age does not disrupt lexical activation but reduces the efficient use of contextual information, then age effects will be most marked for the delayed repetition condition. Very few studies have examined the effect of age on repetition priming. Cohen et aI.” report that repetition improved free recall equivalently for young and old adults. Balota et al3 examined the effects of age on recall using a list of paired-associates, in which some pairs were repeated at inter-item lags ranging from 0 to 20. Despite an effect of age on recall performance, the effect of repetition lag was equivalent in young and old adults. Though previous studies have not found age differences in the effect of repetition on recall performance3,*’ or on the time required to make an orthographic or semantic discrimination28, it is possible that reaction time is not sensitive to age differences in the processes underlying repetition priming. Hamberger and Friedman28 reported that, although the behavioral facilitation from word repetition was equivalent in young and old adults, the effect of repetition on the ERP waveform had a later onset and longer duration in the older subjects. According to Van Petten’s interpretation of ERP repetition effects, age effects on lexical and episodic processes will be reflected in different ERP components. An age-related delay in lexical access mechanisms will be expected to affect N400 amplitude and resolution. The effect of age on contextual integration processes will be reflected in the LPC by older subjects showing a smaller effect of word repetition on the LPC. This effect is expected to be particularly evident for the delayed repetition condition which is more strongly dependent on the retrieval of episodic information. To investigate the possible contribution of responserelated processes to any observed age differences, performance was compared in two different tasks. One task involved a differential word/non-word button press; in the other task, subjects were simply asked to mentally classify each item but to make no overt response. Since word repetition in the response condition involves the repetition of both stimulus-encoding and response selection processes, it will be more strongly dependent on the retrieval of contextual information relevant to the first presentation of the word and therefore rely more heavily on episodic memory processes. Previous studies have shown that such task-re-

lated parameters primarily affect the development of ERPs to delayed repetition7s3*, supporting the assumption that the delayed repetition effect strongly depends on episodic memory processes. Most aging studies provide a limited picture of the effects of aging on cognitive performance because they only compare two extreme age groups. The omission of an intermediate group may be related to the difficulty of recruiting middle-aged subjects or an implicit assumption that age has a linear effect on performance. The present study compares three groups of subjects aged 20-40,40-60 and 60-80 years. To allow comparison of the present results with previous studies, the analysis included a direct comparison of the young and the old groups. A second comparison of the middle group with the young group provided information regarding the onset of age-related changes. MATERIALS AND METHODS Subjects A total of 62 subjects (20 males) were tested. Subjects included undergraduate students and volunteers from the community ranging in age from 20 to 76 years. Students participated for course credit while volunteers responded to an article in local newspapers. The data from 10 subjects were excluded from the analysis due to very low signal to noise ratio (i.e. as a result of excessive eye movement or very poor performance), failure to complete the task or equipment problems. The remaining 52 subjects were classified into three groups on the basis of age. Group 1 (young) included 20 subjects aged 20-39 years, Group 2 (middle) included 15 subjects aged 40-59 years, and Group 3 (old) included 17 subjects aged 60-76 years. Group 1 was comprised exclusively of students, Group 3 included only community volunteers, whereas Group 2 included both types of subjects. All subjects were administered the Mini-Mental State Examination test (MMSEz41, the Yesavage Geriatric Depression Scale”, and the Vocabulary subtest of the Wechsler Adult Intelligence Scale Revised”. The three groups were relatively well matched on intellectual, educational and mood scores (Table II. However, comparisons between the young group and each of the other groups using a one-way ANOVA revealed some significant differences. The MMSE scores for the old group were significantly lower than those of the young group (F,,49 = 20.16, P < 0.001). However, none of the subjects in the old group scored at or below the cut-off score taken to suggest the existence of a progressing dementing disorderz4. Bleecker et al.” have shown that mean MMSE scores decline with age even in subjects closely matched for educational level and screened against neurological and psychiatric illness suggesting the need for age-adjusted norms. TABLE

I

Demographic data for each age group Education in years; MMSE, Mini-Mental State Examination (max = 30); YGDS, Yesavage Geriatric Depression Scale (max = 30). Standard deviations are in parentheses. ?I

Age

Education

MMSE

YGDS

Vocabulary WA&R

Young

20

Middle

15

Old

17

27.3 (5.4) 46.7 (4.7) 67.4 (4.8)

13.9 (1.8) 15.8 (4.5) 9.8 (2.7)

29.6 (0.6) 29.1 (1.1) 28.2 (1.1)

5.2 (4.4) 4.5 (3.2) 8.8 (8.1)

55.5 (16.5) 56.7 (11.0) 51.5 (9.3)

126 Although the young group had completed more years of formal education than the old group (F,,,s = 15.53, P < 0.000, the two groups did not differ on WAIS-R Vocabulary scores (F,,,, = 3.14, P > 0.05) suggesting a similar broad educational level. On the latter test, the middle group performed significantly better than the young group (F,,,, = 10.10, P < 0.003). Stimuli

One hundred and sixty nouns were selected from Carroll, Davies and Ricbmanlh. All nouns were 5-7 letters long with frequency between 40 and 400 per million (mean = 141, SD.= 85). Eighty pronounceable non-words were selected from a computer-generated list of non-words that were constructed to conform to the letter distributional properties of English. Words and non-words were pseudo-randomly allocated to one of two lists matched for mean word frequency and length. The two lists contained different stimuli structured in the same pseudo-random order which ensured there were no more than two consecutive non-words, no more than two consecutive immediate repetitions and no more than eight consecutive words. Each list consisted of a total of 200 stimuli: 40 words (IMMl) that were repeated immediately (IMM21, 40 words (DEL11 that were repeated with an inter-item lag of 4 (DEL21 and 40 non-words. The list was further divided into three blocks allowing a small break between each block. Two practice lists of twelve items were also constructed. ERP recording and data acquisition

EEG was recorded from six scalp electrodes (Fz, Cz, Pz, Oz, P3, P4) according to the lo/20 system using an electrode cap (ElectroCap International) and was amplified (X 20,000) using a Grass Neurodata (Model 12) system with a bandpass of 0.01-30 Hz (- 6 db down). Horizontal and vertical eye movements were monitored via two additional electrodes situated on the outer canthus and 2 cm below the left eye, respectively. EEG and EOG activity were sampled at 6-ms intervals, beginning 240 ms prior to stimulus onset and for a total of 1536 ms using a PDP 11/23 + computer. All electrodes were referred to linked earlobes. Procedure

All subjects gave written informed consent. Subjects were seated in a reclining chair in a sound attenuated, dimly lit room. Individual items were presented on a monitor screen situated approximately 1.2 m away from the subject. Each item was presented for 740 ms and the inter-stimulus interval was 2.5 s. The two lists were presented in a counterbalanced order under one of two response conditions. In the read task, subjects were asked to silently read each item and decide whether it was a word or a non-word, without making a motor response. In the respond task, subjects were instructed to use their index and middle fingers to press two buttons fixed on either the left or the right armrest. One button corresponded to a ‘word’ response and the other to a ‘non-word’ response. The hand used was counterbalanced across subjects. Subjects were informed that a recognition memory task was to follow at the end of the experimental session. They were also told that many words would be repeated either immediately or with a delay but that no differential action on their part was required. The two response tasks were counterbalanced across subjects and each condition was preceded by a practice run. Subjects were instructed to avoid eye movements as much as possible. Data analysis

Behavioral data were only available for the respond condition. Error rates and reaction time were averaged across item type for each subject. The behavioral data were analyzed using a 3 groups X 2 repetitions (first vs. second presentation)X2 lags (0 vs. 4) mixed design analysis of variance (ANOVA). The EEG and EOG channels were averaged according to stimulus type. For the respond task, the waveforms associated with incorrect behavioral responses were rejected. This was not possible for the read task. However, the small error rates observed in the respond task (see Table I) suggest that the results are not greatly affected.

For both tasks, individual trials were deleted from all channels if the EOG activity (peak to peak) was greater than 64 pV. ERP data for each subject were averaged according to task (read vs. respond), repetition (first vs. second presentation) and lag (0 vs. 4) at each electrode site. To determine the relative effects of repetition and lag over the course of the ERP waveform, mean amplitude measures were calculated for each subject over lOO-ms epochs ranging from 300 to 900 ms. For midline electrodes, mean amplitude data were analyzed using a 3 groups X 2 tasks X 2 repetitions X 2 lags X 4 electrodes (Fz, Cz, Pz, Oz) mixed design ANOVA. Where appropriate, critical values were adjusted using the Greenhouse-Geisser correction for violation of the assumption of sphericity69. Due to the absence of any evidence for hemispheric asymmetry, the lateral parietal electrodes were not included in the statistical analyses. The effects of age were examined by comparing the young group against the middle and old groups, respectively. The comparison between the young and the old groups provided the basis for comparison with previous literature. In addition, comparing the young and the middle groups provided information regarding the onset of any age-related changes. An alpha of 0.01 was used throughout the analysis in order to control for inflation of the type I error rate as a result of multiple comparisons. Significant interactions were examined by calculating multiple comparisons using separate error estimates for each contrast4’. As differences in overall amplitude between electrodes are likely to result in spurious interactions between electrode position and other factors, the interpretation of such interactions was based on analyses of data normalized using a vector resealing procedure43. Interactions between electrode and other factors are presented only if they remained significant following the normalization procedure. Two difference waveforms were created for each subject by subtracting waveforms corresponding to the first presentation of a word from waveforms corresponding to the repetition of that word (e.g. IMM2 - IMMl and DEL2 - DELl). Measures of peak amplitude, peak latency and quarter peak latency were obtained from the difference waveforms at Cz and Pz, where the N400 is maximal, and were analyzed using a 3 groups X 2 tasks X 2 lags x 2 electrodes mixed design ANOVA. Finally, to confirm a differential effect of age on early vs. late sections of the ERP repetition effect, mean amplitude was analyzed over 300-600 ms and 600-900 ms using a 3 group x 2 epochs X 2 tasks X 2 lags mixed design ANOVA at Pz alone. RESULTS

Behavioral data

The repetition of a word resulted in response facilitation, the magnitude of which depended on the interitem lag. Averaged across groups, the immediate repetition effect was 121 ms while the repetition effect for delayed items was 52 ms (Table II). The statistical analysis showed significant effects of repetition (F,,,g = 339.85, P < O.OOl>,lag (F,,,, = 138.66, P < 0.001) and their interaction (F,,,, = 50.16, P < 0.001) indicating that immediate word repetition resulted in greater response facilitation than delayed repetition. Post-hoc analysis revealed significant facilitation of performance for both immediate and delayed repetition (F,,,g = 217.41, P < 0.001; F,,,, = 117.85, P < 0.001, respectively). Word classification was overall very accurate (Table II) and improved further with repetition (F,,,, = 29.12, P < 0.001). The main effect of lag and the interaction between repetition and lag were not significant (F < 1.0).

127 YOUNG

TABLE II Median reaction time and percentage (standard deviation in parentheses)

IMMl and DELl, first presentation; DEL2, delayed repetition.

Reaction Time (ms) Young Middle Old Errors (%) Young Middle Old

errors

on the respond

OLD

task

IMM2, immediate repetition;

IMMl

IMM2

DELI

DEL?

968.8 (122.9) 916.0 (88.3) 1015.7 (84.2)

839.5 (122.1) 806.4 (99.1) 890.6 (93.4)

963.3 (118.51 935.9 (91.7) 1031.5 (88.9)

922.5 (114.11 872.4 (76.3) 977.3 (95.1)

2.37 (3.29) 2.50 (2.671 6.32 (4.25)

MIDDLE

0.87 (2.03) 0.67 (1.141 3.38 (3.64)

3.25 (3.901 1.00 (1.581 6.32 (6.00)

1.50 (2.491 0.50 (1.03) 2.06 (3.33)

Group differences.

There were no significant differences in median RT between young and middle groups or between young and old groups (Table II>. The interactions between the group comparisons and the repeat factors were also not significant. Young and middle groups responded equally accurately, but the old group committed more classification errors than the young group
,I .._

-

.

.

.

.

.

I,,

-_--_

0

IMMl

IMM2

DEL 1

300

500

900

msec

DEL2

Fig. 1. Grand mean waveforms from the READ task. The traces of different word types are superimposed at each electrode position. IMMl and DELl, first presentation; IMM2, immediate repetition; DEL2, delayed repetition. YOUPJG

OLD

MIDDLE

ERP data

The grand average ERPs for the four stimulus types for all electrodes are shown in Fig. 1 for read and Fig. 2 for respond tasks. The waveforms for the first presentation of a word (IMMl and DEL11 exhibit a negative peak at approximately 400-500 ms post-stimulus. The waveforms to immediate and delayed word repetition (IMM2 and DEL2, respectively) show an attenuated negativity around 400-500 ms and an earlier late positivity as compared to the waveforms for first presentation. The main effect of repetition was significant at midline sites for 300-700 ms (300-400: Fi,49 = 34.84, P < 0.001; 400-500: F,,,, = 148.92, P < 0.001; 500-600: F 1,49= 109.33, P < 0.001; 600-700: F,,,, = 29.31, P < 0.001). Thus the divergence of ERP waveforms as a function of word repetition first became apparent around 300 ms at all midline electrodes. The main effect of lag was significant from 400 to

-4””

I IMMl

IMM2

DEL1

DEL2

Fig. 2. Grand mean waveforms from the RESPOND abbreviations see legend Fig. 1.

m*ec

task. For

600 ms and then again between 700 and 900 ms (400500: Fl,49 = 24.49, P < 0.001; 500-600: F,,,, = 19.73, P < 0.001; 700-800: F1,,, = 18.03, P < 0.001; 800-900:

128 F ,,49= 10.01, P < 0.003). The absence of a significant

effect at 600-700 ms appears to reflect the crossing of the waveforms for immediate and delayed repetition as the former is returning to baseline while the latter is still positive-going. The lag by repetition interaction was also significant over the 400-600 and 700-900 ms epochs (400-500: F ,,49 = 58.69, P < 0.001; 500-600: F,,,, = 19.05, P < 0.001; 700-800: F,,,g = 21.20, P < 0.001; 800-900: F,,,g = 13.02, P < 0.001). As shown in Figs. 1 and 2, the effect of immediate repetition occurs earlier and is greater than the delayed repetition effect, especially between 400 and 600 ms. Post-hoc tests showed that the waveform for immediate repetition returns toward baseline at 600-700 ms, whereas the waveform for delayed repetition shows significantly enhanced positivity as late as 900 ms. The interaction between repetition and electrode was significant between 400 and 700 ms (400-500: F 3,,47 = 19.47, P < 0.001, e = 0.565; 500-600: F3,147 = 12.32, P < 0.001, e = 0.630; 600-700: F3,147 = 7.56, P < 0.001, e = 0.694). The interaction between lag and electrode was significant within the 400-500 ms epoch Q&47 = 6.27, P < 0.004, e = 0.601) and marginally significant at 500-600 ms (F3,147 = 4.29, P < 0.026, e = 0.508). Post-hoc tests showed that the effects of both repetition and lag were particularly pronounced at central and parietal electrodes. The effects of repetition and lag did not differ significantly between the two task conditions. In summary, word repetition results in a positive shift in the waveform between 300 and 900 ms poststimulus. The effect is more pronounced for immediate than for delayed repetition and at central and parietal electrodes. Group differences. As shown in Figs. 1 and 2, with increasing age there is an overall positive shift of all waveforms beginning approximately 300-400 ms poststimulus, and a greater persistence of the effects of repetition and lag. These changes are apparent in the middle group but are more pronounced in the old group. Statistical analyses revealed few significant differences between the young and middle age groups. There was a significant group main effect between 600 and 900 ms (600-700: F1,49 = 7.62, P < 0.008; 700-800: F 1,49= 13.60, P < 0.001; 800-900: F1,49 = 17.15, P < O.OOl),reflecting the positive shift of all waveforms for the middle group. This positivity was particularly pronounced at fronto-central sites over 800-900 ms (F3,147 = 5.73, P < 0.006, e = 0.618). Some marginally significant interactions between group and other factors were also observed. As compared to the young group, the

middle group showed a prolonged effect of repetition at 600-700 ms (F,,,, = 4.06, P < 0.049) and of lag at 700-800 ms (group by task by lag: F,,,, = 4.20, P < 0.046) with the latter being apparent primarily in the respond condition. These trends suggest that the effects of repetition and lag on the ERP waveforms have a similar onset latency for both groups, but are more prolonged in the middle group. A similar pattern of differences is observed when comparing the young and the old groups. The overall positive shift of all waveforms for the old group was significant between 600 and 900 ms (600-700: F,,,g = 11.32, P < 0.001; 700-800: F,,,, = 19.05, P < 0.001; 800-900: F,,,g = 32.34, P < 0.001). The interaction between group and electrode was significant over 400-700 ms and 800-900 ms (400-500: F3,147 = 6.01, P < 0.006, e = 0.568; 500-600: F3,147 = 11.18, P < 0.001, e = 0.679; 600-700: F3,,47 = 8.29, P < 0.001, e = 0.590; 800-900: F 3,147= 7.54, P < 0.001, e = 0.618). Post-hoc tests showed that the positive shift with increasing age is most pronounced frontally and gradually diminishes at the more posterior electrode sites. ERP waveforms for both groups show large effects of repetition and lag which appear around 300-400 ms, but the groups differ in the time course of these effects. The group by repetition interaction was significant between 600 and 800 ms (600-700: F,,,, = 17.16, P < 0.001; 700-800: F,,,, = 16.08, P < 0.001) and was still marginally significant at 800-900 ms (F,,,, = 4.83, P < 0.033). Post-hoc tests showed that for the young group, the effect of repetition on the ERP waveforms has dissipated by 600 ms, but it is still evident at 900 ms for the old group. The group by lag interaction was significant at 600700 and 800-900 ms (F1,49 = 10.80, P < 0.001; F,,,, = 8.34, P < 0.001). The three-way interaction between group, repetition and lag was also significant within the latter epoch (F,,,, = 11.33, P < 0.001). Post-hoc tests showed that, for the young group, the effect of both immediate and delayed repetition on the ERP waveform has terminated around 600 ms. For the old group, the effect of immediate repetition dissipates around 700 ms, whereas delayed repetition still results in a significantly enhanced positivity at 900 ms. The significant interaction between group, lag and electrode at 600-700 ms (F3,14, = 5.29, P < 0.008, e = 0.610) reflects the centro-parietal distribution of the prolonged effect of delayed repetition in the old group. Within the 400-600 ms epoch, the read task produced a greater positive shift in the old group than the respond task, particularly at Cz and Pz (400-500: group by task F,,,, = 10.09, P < 0.003; 500-600: group by task by electrode: F3.,47 = 4.67, P < 0.008, e = 0.764).

129 TABLE

III

Peak latency and amplitude measures on difference waveforms averaged across Cz and Pz electrode sites Standard

deviation

in parentheses.

IMM, immediate

effect,

DEL, delayed

repetition

effect.

MIDDLE

YOUNG

Quarter Read

repetition

OLD

ZMM

DEL

IMM

DEL

ZMM

DEL

387.7 (105.1) 424.4 (143.4)

509.2 (133.6) 468.3 (111.4)

414.0 (55.1) 419.0 (114.9)

517.6 (169.5) 533.8 (126.5)

431.6 (72.0) 434.1 (78.0)

573.2 (101.4) 538.9 (99.0)

498.3 (44.2) 533.5 (118.4)

596.8 (109.7) 559.5 (85.2)

509.2 (39.4) 541.2 (101.2)

643.2 (115.6) 640.2 (110.8)

566.1 (83.3) 572.6 (87.7)

683.1 (92.4) 701.3 (118.0)

peak latency

Respond

Peak latency Read Respond

Peak amplitude Read Respond

6.59 (2.56) 8.18 (2.67)

4.62 (2.48) 4.66 (3.31)

6.90 (3.00) 7.36 (3.14)

To summarize, both the middle and the older age groups showed a positive shift of all waveforms over approximately 400 to 900 ms. This positive shift is particularly pronounced at the frontal electrode. In addition, the effect of both lag and repetition on the ERP waveform was prolonged with increasing age. The effects of age are marginally significant for the middle group but highly significant for the old group.

5.18 (2.35) 6.35 (3.15)

7.15 (3.68) 7.66 (3.24)

6.07 (2.87) 5.77 (2.80)

To directly evaluate the differential effects of age on early and late parts of the ERP repetition effect, a final analysis was conducted on the difference waveforms comparing 300-600 ms to 600-900 ms epochs. The significant interaction between epoch and lag (F,,, = 120.51, P < 0.001) shows that the immediate repetition effect occurs primarily within 300-600 ms and has largely terminated within the 600-900 ms

Difference waveforms

In order to interpret the effects of repetition and lag without the confounding effect of the positive shift of all waveforms with age, the difference waveforms for immediate and delayed repetition were constructed. Group differences. The difference waveforms show that the repetition effect begins around 300-400 ms poststimulus for all groups, but the duration of the effect is prolonged in middle and old groups (Fig. 3). Table III presents peak amplitude, peak latency and quarter peak latency measures derived from the difference waveforms for all three groups. Immediate repetition produced a greater effect on the ERP waveform than delayed repetition (F,,, = 27.79, P < 0.001). Age did not significantly affect peak amplitude of the ERP repetition effect. Both quarter peak and peak latencies were significantly earlier for immediate as compared to delayed repetition in all three groups (Pi,, = 59.83, P < 0.001; F1,44 = 70.08, P < 0.001). However, peak latency (i.e. the maximal differentiation between ERPs to first and second word presentations) was significantly earlier in the young as compared to the old group Vi., = 18.78; P < 0.001).

YOUNG

MIDDLE

OLD

READ

RESPOND

-4””

1. 0

IMMI-IMMP

DELI-DEL2

I

*

300

500

I

900

m*eC

Fig. 3. Grand mean difference waveforms for immediate IMM2) and delayed (DEL1 - DEL21 repetition.

(IMMl-

130 TABLE

IV

Correlation coefficients between age and difference waveform measures controlling for age differences in years of education Delayed

Immediate CZ

Pz 0.271 * 0.128

Peak latency Read Respond

0.526 * * * 0.302 *

0.347 ** 0.161

P.?

cz

Quarter peak latency Read 0.161 Respond 0.070

0.054 - .0.107

0.157 0.220

0.339 ** 0.272 *

0.244 * 0.238

0.275 * 0.093

Peak amplitude Read 0.139 Respond - 0.002

0.046 - 0.002

0.267 * 0.136

Mean amplitude 300-600 Read 0.018 Respond - 0.096

ms - 0.080 - 0.192

0.191 0.124

Mean amplitude 600-900 Read 0.311 * Respond 0.248 *

ms 0.225 0.182

0.505 *** 0.356 **

0.173 - 0.012

0.485 * * * 0.315 *

* P < 0.05 * * P < 0.01 *** P
epoch, whereas the effect of delayed repetition is not only smaller but also spreads out across the whole recording interval (Fig. 3). There was no significant difference between young and middle groups. When comparing young and old groups, the group by epoch interaction was significant (F,,,g = 14.11, P < 0.001). As shown in Fig. 3, although the two groups do not differ in the amplitude of the ERP repetition effect over 300-600 ms, in the later epoch, the waveforms have returned to baseline for the young group but the repetition effect is still strong for the old group. Age correlations The correlation between age and ERP measures was estimated using a partial correlation procedure to adjust for age differences in years of education. ERP measures were derived from the difference waveforms to eliminate the overall positive shift seen in the raw waveforms. As shown in Table IV, the latency of maximal differentiation between first and second presentations of a word was significantly longer for older subjects especially in the read task. The size of the maximal differentiation also increased with increasing age but only for delayed repetition in the read task. In accordance with the results of earlier analyses, age was not correlated with mean amplitude over a 300-600 ms epoch but was significantly positively correlated with mean amplitude over 600-900 ms for both tasks and at central and parietal electrodes.

In summary, analyses of the difference waveforms supported the conclusion that age differences are evident mainly in terms of the duration of the repetition effect rather than in its onset or peak amplitude. For the young group, the effect of repetition has dissipated by 600 ms, for the middle group it continues into 700 ms, whereas for the old group, it does not resolve until at least 900 ms after word presentation. The development of the ERP repetition effect also differed with age. There was an increase in both quarter peak and peak latency across age groups, although statistically only the difference in peak latency between young and old groups was significant. Despite these differences in the timing and duration of the repetition effect, the peak amplitude of the effect was not affected by increasing age. DISCUSSION

In accordance with previous studies (e.g. refs. 23 and 64), word repetition resulted in significant response facilitation. The effect of immediate repetition on lexical decision time was twice as large as that of delayed word repetition. Reaction time did not increase significantly with age. However, the old group did commit more errors in word classification than the young group suggesting that the absence of the expected age difference in reaction time may have occurred because of a bias toward speed as opposed to accuracy in the old group. As expected on the basis of earlier studies3,20,28, RT facilitation with word repetition was not affected by age. The finding that the old group showed greater improvement in error rates with repetition is quite likely to have resulted from a ceiling effect in the young group (Table II). In fact, the percentage improvement in error rate with repetition was equivalent between age groups (i.e. young: 36-46%, middle: 2750% and old: 32-53%). Thus, age did not affect the magnitude of behavioral facilitation resulting from either immediate or delayed word repetition suggesting that the lexical and episodic memory processes underlying the word repetition effect25Ys4remain intact. Word repetition resulted in an attenuation of the N400 wave which was elicited by the first presentation of the word, and an increase in the amplitude of the later positivity. The ERP repetition effect had a larger amplitude and shorter duration for immediate than for delayed word repetition. These findings replicate the results of an earlier study using the same paradigm3*. Although overall the ERP waveforms appear qualitatively similar across the three age groups, there were a number of important modifications with age. First,

131 with increasing age there was a slow positive shift of the whole waveform for all stimulus types beginning approximately 300-400 ms after stimulus presentation. This was particularly pronounced at the frontal electrode where it continued throughout the whole recording epoch. This positive shift was greater in the read than the respond task from 300-600 ms. A reduction in a frontal negative slow wave with age has been previously reported in an auditory oddball task34, an auditory choice reaction time task5’ and a visual memory search task 38. In a recent review of slow cortical potentials (SCP), Birbaumer, Elbert, Canavan and Rockstroh’ presented evidence that negative SCPs are associated with increased cortical excitability whereas positive SCPs are associated with decreased cortical activity. Cholinergic and catecholaminergic activity has been implicated in the generation of negative SCPs (see ref. 8 for review). There is ample evidence that both cholinergic and catecholaminergic activity is reduced in aging (e.g. refs. 4, 41, 44 and 46). It is, therefore, possible that the positive shift of the waveform in the elderly may result from a generalized decrease in cortical excitation as a consequence of either cortical cell loss or dysfunction of thalamic or subcortical control of cortical excitation. Although the onset of the ERP repetition effect occurred approximately 300 ms following word presentation for all age groups, the duration of the effect increased with age (Fig. 3). Specifically, the repetition effect for both immediate and delayed repetition has dissipated by 600 ms in the young group. The effect of immediate repetition continues to about 700 and 800 ms for the middle and old groups, respectively, whereas the delayed repetition effect dissipates at around 800 ms for the middle group and is still evident at 900 ms for the old group. Due to the considerable variability across groups in the interval within which the negative and positive components peaked, the slow positive shift in the waveform with age, as well as the fact that for many subjects a clear peak could not be identified, it was not possible to measure peak amplitude and peak latency of N400 and LPC in the original waveforms *. However, measurement of peak amplitude, quarter peak and peak latency in the difference waveforms provides information relating to the magnitude and the timing of the maximal differentiation between the ERP waveforms for first and second presentation.

This analysis confirmed that the overall duration of the ERP repetition effect was prolonged with age. When the effect of the overall shift in the waveform with age is eliminated by calculating the repetition difference waveforms, age-related differences in mean amplitude are not significant within the 300-600 ms epoch but are primarily evident for the 600-900 ms epoch. As shown in Figs. 1 and 2, during the latter epoch the waveform is returning to baseline in young subjects but is still positive going in older subjects. Additionally, although the onset latency of the repetition effect is not significantly affected by age, peak latency is significantly delayed (see Fig. 3). Age was significantly correlated with a delay in the latency of maximal differentiation between first and second word presentations. Despite these age differences in the duration of the effects of word repetition on the ERP waveform, the maximal amplitude of the ERP repetition effect did not differ between age groups. Thus, the present data show that age differences are not apparent within the latency range of the N400. Significant age differences appear around the time of resolution of the N400 and the development of the subsequent positivity. An age-related change in the temporal duration of the ERP repetition effect has also been reported by Hamberger and Friedman2* and Friedman, Hamberger and Ritter26. Using a semantic discrimination task, the latter study also showed an increase in the amplitude of the ERP repetition effect with age. Friedman et a1.26 interpret this as an age-related increase in the amplitude and duration of the slow wave to repeated words, possibly reflecting additional processing of the repeated item. According to the Van Petten et a1.68 model, the present findings suggest that the lexical processing mechanisms that are reflected by the N400 waveform remain intact with increasing age. According to this model, the age differences in the latency of the late positivity suggest that age affects the episodic memory processes involved in the retrieval and integration of contextual information and the updating of working memory. The above interpretation is contingent upon the assumption of a clear-cut dissociation between the cognitive correlates of the N400 and the LPC, with the former reflecting lexical access and the latter reflecting episodic memory processes. However, accumulating evidence casts doubt on the assumption that N400 is

* A principal components analysis (PCA) was conducted in an attempt to isolate these two components and separate their contribution to the ERP repetition effect. PCA was run both across all subjects and within each group. However, the significant shift in the latency of these components and the positive shift of the all waveforms with age precluded a meaningful interpretation of the resulting components.

132 solely a reflection of processes acting on abstract lexical representations. N400 amplitude is modulated by both immediate and delayed word repetition3*, even though, the latter process is believed to depend primarily on re-accessing contextual information established during the first presentation of the word25,54. N400 is also evident for non-lexical stimuli. Immediate repetition of pronounceable non-words results in an attenuation of negativity that is similar to, albeit smaller than, the attenuation associated with word repetition56,59. Both behavioral and ERP repetition effects have also been successfully demonstrated with non-verbal stimuli’. The strongest evidence for episodic influences on N400 comes from a recent study48 which showed that the amplitude of N400 to a repeated word is sensitive to changes in the context within which the word is repeated. Specifically, while the size of the N400 congruity effect (i.e. the difference between N400 amplitude to words completing incongruous as compared to congruous sentences) was significantly reduced when the word was repeated within the same sentence frame, presenting a repeated word in a different sentence context resulted in a smaller attenuation of the N400 congruity effect. Halgren” proposes that the N400 and the subsequent positivity should not be viewed as separate components, but rather as forming a waveform complex, the N400/P300 * *. According to Halgren’s model, this complex “embodies a process that is triggered by lexical encoding of a potentially meaningful stimulus, and is modulated by the ease of integrating the meaning of that stimulus within the cognitive context. These characteristics provide an operational definition for a single process of lexical access and contextual integration” (p. 124). The amplitude and duration of the N400/P300 complex are assumed to reflect the ease of integrating the stimulus into the current cognitive context and are affected by the availability of a pre-existing memory trace for that stimulus. “This memory trace can be remote, recent, or primary and is especially effective if it relates the word to the current context” (p. 1081. Within Halgren’s framework, the present data can be viewed in terms of age-related delay in the resolution of the N400 component and the development of the subsequent positivity (Figs. 1 and 2). The absence of an age-related delay in the onset of N400 suggests that the processes leading up to the initiation of lexical

__

access remain intact. The increase in the duration of N400 and the resultant delay in the subsequent positivity may be interpreted as an age-related disruption of the effective use of remote semantic and/or recent episodic representations to integrate the accessed word with the current context. This conclusion is consistent with the finding that aging results in a larger and longer effect of delayed repetition on the ERP waveform. The waveform corresponding to immediate repetition diverges markedly from the other waveforms in all three age groups (Figs. 1 and 2). The effect of delayed repetition is much less pronounced in the young group but becomes more marked with increasing age. Although the group difference in the size of the delayed repetition effect is apparent when comparing the young and middle groups, the difference is statistically significant only between young and old groups. The effect can be seen more clearly in Fig. 3 which shows the repetition effect for the two lags. Young and old groups differed significantly in mean amplitude over 600-900 ms for delayed but not immediate repetition. As discussed above, recent theories of repetition priming maintain that immediate repetition involves primarily lexical activation processes while delayed repetition depends upon the retrieval of the episodic memory trace relevant to the previous occurrence of the word25,54. When the inter-item lag is zero, the processes involved in context retrieval and updating working memory are minimal. However, after a lag of four items, both the context of presentation and the content of working memory have changed. Information relating to the previous occurrence of the word will need to be retrieved into working memory and integrated with information relating to the second presentation of the word. Some aspects of this process appear to be compromised with increasing age. Thus, the effects of age on the development of the N400/P300 complex and the duration of the ERP repetition effect may reflect an age-related deficit in the retrieval or use of information relating to the prior occurrence of a word. Both the behavioral and psychophysiological data suggest that processes involved in gaining access to stored knowledge about words are not affected by age. This conclusion contradicts that of previous behavioral studies which have been interpreted as demonstrating

* * Halgren“ refers to the positive component of this negative/positive complex as a P300, suggesting that this positivity is identical to the P300 observed to rare target stimuli in tasks requiring stimulus discrimination. However, the rationale is unconvincing. Like Van Petten et a1.68, the present authors use “.. the term ‘LPC’ as a descriptive one.. without suggesting any identification with the P3a, P3b, slow wave, or other components.. . ” (p. 147, note 2).

133

a delay in lexical access with increasing age2,11,12,50. However, the dependent variables employed in these earlier studies (i.e. naming a line drawing”,50; retrieving a word to fit a specified definitioni do not provide a pure measure of lexical access but are affected by a number of other confounding factors. In summary, the present findings suggest that word identification processes are intact in the elderly. There was no effect of age on the onset or amplitude of N400. Age differences became evident approximately 600 ms post-stimulus. The effect of word repetition on the ERP waveform was prolonged with increasing age and this was particularly evident for delayed repetition. Whether interpreted as a delayed LPC or as a prolonged N400, the present findings suggest that lexical access processes remain largely unaffected with increasing age. Aging appears to affect processes related to the use of contextual information and the integration of a stimulus within its context. This conclusion is compatible with that of many behavioral aging studies3*22T33,51,53,65 (for review see ref. 13). Finally, the most pronounced effect of age on the ERP waveform is a widespread positive shift of the whole waveform beginning approximately 400-500 ms post-stimulus. It is suggested that this may reflect an age-related decline in cortical excitability. Acknowledgements. This research was supported by a Commonwealth Postgraduate Research Award to F.K., the National Health and Medical Research Council, and the Rebecca L. Cooper Medical Research Foundation.

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