Effects of age on retrieval cue processing as revealed by ERPs

Neuropsychologia 42 (2004) 1525–1542

Effects of age on retrieval cue processing as revealed by ERPs Alexa M. Morcom∗ , Michael D. Rugg1 Institute of Cognitive Neuroscience and Department of Psychology, University College London, London, UK Received 20 May 2003; accepted 16 March 2004

Abstract The electrophysiological correlates of retrieval cue processing were investigated in healthy young (18–30 years) and older (63–75 years) subjects (n = 16 per group). Retrieval orientation—the differential processing of cues according to the form of the sought-for information—and retrieval difficulty were manipulated in a factorial design. In separate study-test cycles, subjects studied either words or pictures, and performed a yes/no recognition memory task with words as the test items. ERPs elicited by correctly classified new words differed markedly according to study material in the young subjects, replicating previous findings. In the older subjects, this effect was smaller than in the young, and had a later onset and earlier offset. The scalp topography of the effect was however statistically indistinguishable in the two groups. These age-related ERP differences were unmodulated by task difficulty, and remained reliable when recognition performance was matched across the groups. By contrast, the magnitude and timing of ERP difficulty effects were unaffected by age. The findings suggest that older subjects are less able than young individuals to vary their processing of retrieval cues in response to different retrieval demands. © 2004 Elsevier Ltd. All rights reserved. Keywords: Memory; Recognition; Retrieval orientation; Ageing; ERPs

1. Introduction Healthy ageing is associated with a decline in the ability to remember recently experienced events (Craik & Jennings, 1992; Light, 1991). This is found predominantly in tasks requiring intentional retrieval (Light & Singh, 1987), and is associated with a greater impairment of ‘recollection’ than ‘familiarity’ (Yonelinas, 2001) and, consequently, a greater difficulty in remembering details of the context in which items were encountered than in remembering the items themselves (Spencer & Raz, 1995). It remains uncertain to what extent this age-related impairment in episodic memory is due to changes in the capacity to encode new information (e.g. Craik & Rabinowitz, 1985; Glisky, Rubin, & Davidson, 2001; Perfect, Williams, & Anderton-Brown, 1995), as opposed to changes in processes operating at the time of retrieval (e.g. Burke & Light, 1981; Craik & McDowd, 1987; Craik & Rabinowitz, 1985).

∗ Corresponding author. Present address: Department of Psychiatry, Box 189, Addenbrooke’s Hospital, Cambridge CB2 2QQ, UK. Tel.: +44-1223-336598; fax: +44-1223-336581. E-mail address: [email protected] (A.M. Morcom). 1 Present address: Center for the Neurobiology of Learning and Memory, University of California Irvine, Irvine, CA 92697-3800, USA.

0028-3932/$ – see front matter © 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2004.03.009

With regard to retrieval, ageing might influence one or more of a number of functionally distinct component processes. Aspects of a prior event are reconstructed via an interaction between a ‘retrieval cue’ (either self-generated or provided by the environment) and the memory representation of the episode (Tulving, 1983). Rugg and Wilding (2000) identified three kinds of putative ’pre-retrieval’ process which precede this interaction. Firstly, ’retrieval mode’ establishes a cognitive state enabling events to be processed specifically as episodic retrieval cues (Wheeler, Stuss, & Tulving, 1997). Secondly, ‘retrieval effort’ mobilises attentional and processing resources in support of a retrieval attempt. Thirdly, ‘retrieval orientation’ biases the processing of retrieval cues so as to meet the demands of a specific retrieval task (for example Robb & Rugg, 2002; Rugg, Allan, & Birch, 2000). Pre-retrieval processes are held to operate regardless of whether a retrieval attempt is successful. Other, ‘post-retrieval’ processes are then brought to bear whenever a cue has initiated contact with stored information about a prior episode (‘synergistic ecphory’; Tulving, 1983). These post-retrieval processes support the representation and subsequent evaluation of retrieved episodic information. It has been suggested previously that older subjects have difficulty with episodic retrieval because they cannot effectively specify the necessary mental operations (‘self-generation’ of retrieval cues) unless the test stimuli

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provide ‘environmental support’ for such operations (Craik, 1983, 2000). As has frequently been pointed out, this is consistent with the generally better performance of older adults on recognition compared with free recall tests, and on data-driven indirect memory tests than on both of the latter (La Voie & Light, 1994). However, other data suggest that older adults’ difficulty may instead be with deliberate recollection, regardless of the strength of external cues (Park & Shaw, 1992; see Light, 1996). This fits with evidence that although overall recognition performance is relatively preserved with increasing age, this reflects a predominance of familiarity-based responding (Yonelinas, 2001). Thus even when retrieval cues are identical to to-be-retrieved items, recollection is markedly impaired, indicating a possible difficulty in the processing of episodic retrieval cues themselves. To study the different categories of retrieval processes, it is necessary to distinguish them from each other and from factors that influence encoding. Scalp-recorded event-related potentials (ERPs) are particularly valuable in this context, allowing the dissociation of the neural correlates of pre-retrieval processes from those of ‘retrieval success’, and providing detailed information about their temporal characteristics. ERP studies of the effects of ageing on episodic retrieval have so far focused on processing associated with retrieval success, and their results provide some, although not unequivocal, support for the notion that its neural correlates differ according to age (for review see Friedman, 2000). Age-related differences have been reported in two principal ERP correlates of retrieval success, both of which take the form of positive-going deflections in the waveforms elicited by correctly identified old items relative to correctly identified new items. The ‘left parietal old/new effect’, which onsets around 400–500 ms post stimulus, persists for about 400 ms, and is maximal over the left parietal scalp, is thought to be a neural correlate of the retrieval and representation of episodic information (e.g. Wilding & Rugg, 1996). A reduction in its magnitude in older compared with younger adults has been found in some studies using simple recognition judgements (Rugg, Mark, Gilchrist, & Roberts, 1997; Swick & Knight, 1997), but not where procedures are employed to ensure that ERP differences between young and older do not simply reflect a greater reliance in the latter on familiarity-based responding (e.g. Mark & Rugg, 1998; Trott, Friedman, Ritter, & Fabiani, 1997). The second, ‘right frontal’ old/new effect onsets later, exhibits a more sustained time-course (>1 s), and has a maximum over the right frontal scalp. This effect is apparent particularly in tests of source memory (see Rugg, Otten, & Henson, 2002). The right frontal effect also has been reported to be attenuated in older individuals, and it has been claimed that this reflects an age-related reduction in the engagement of frontally-mediated evaluative and monitoring processes (e.g. Trott et al., 1997; Wegesin, Friedman, Varughese, & Stern, 2002; but see Mark & Rugg, 1998 for contradictory findings).

The present study goes beyond previous work to investigate the possibility that ageing affects the neural correlates of retrieval orientation. If the differential processing of retrieval cues is attenuated or altered in older adults, this could contribute to age-related retrieval difficulties independently of any changes in the processes that follow successful retrieval. The present study takes as it starting point recent findings in young subjects which demonstrate that ERPs elicited by recognition memory test items vary according to the nature of the sought-for information (Herron & Rugg, 2003; Robb & Rugg, 2002). In Robb and Rugg’s (2002) experiment, participants studied lists of pictures or words, followed in each case by recognition memory tests in which all items were words. ERPs elicited by unstudied items (i.e. ‘new’ test words) were more positive-going when participants were trying to retrieve words than pictures (see Herron & Rugg, 2003, for replication and extension of this finding). The effect onset around 250 ms post-stimulus, lasted for around 1000 ms, and was diffusely distributed over the scalp. Since the effect was elicited by correctly classified new items, it could not have been due to differences in the content of retrieved information. Importantly, Robb and Rugg (2002) factorially crossed study material (and task) with a manipulation of task difficulty, and demonstrated that the effect of material did not interact with the effects of difficulty. Accordingly, they concluded that the material effect was a neural correlate of the adoption of different retrieval orientations, reflecting differences in the processing accorded ostensibly identical retrieval cues. The design and procedure of the present study closely followed Robb and Rugg (2002). ERPs elicited by recognition test items (words) were compared after study of lists of words or pictures, in both ‘easy’ and ‘hard’ tests. By including a difficulty manipulation, it was possible to unconfound effects of age from those of difficulty on group differences in ERP effects (c.f. Morcom, Good, Frackowiak, & Rugg, 2003; see Rugg & Morcom, in press, for discussion of this issue). The principal question was whether, relative to those of younger subjects, the ERPs of older subjects would show evidence of a reduced capacity to process retrieval cues differentially according to the requirements of the two recognition tasks (retrieving pictures versus retrieving words). A secondary question was whether differences between ERP old/new effects in the two age groups, and the influence on such differences of study material, might shed light on the relationship between age-related effects on retrieval orientation and on retrieval success. 2. Method 2.1. Subjects Subjects were 32 healthy, right handed adults. Sixteen were aged between 18 and 30 years (four male), and 16 between 63 and 75 years (four male). Data from a further

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Table 1 Subject characteristics by age group, and performance on standardised neuropsychological tests

Age Years of education (from 16 years) NART FSIQ estimate Raven’s advance progressive matrices II Mini mental state Warrington–McKenna graded naming WAIS digit span Verbal paired associates (WMS)—immediate Verbal paired associates (WMS)—delayed Short story recall (AMIPB)—immediate Short story recall (AMIPB)—delayed FAS verbal fluency

Younger

Older

P

22 5 112 11 – 24 10 22 8 45 44 45

69 4 118 9 29 26 9 20 7 39 37 48

– n.s. <0.05 <0.05 – <0.05 n.s. <0.05 <0.05 <0.05 <0.01 n.s.

(2.9) (1) (8.3) (0.8) (3.7) (1.7) (2.5) (0.3) (5.3) (3.9) (12.4)

(2.9) (1) (8.3) (2.3) (1) (2.0) (2.2) (2.14) (0.9) (7.3) (8.3) (13.4)

Mean scores are shown, with standard deviations in brackets. P values reflect the results of t tests, except in the case of years of education, Raven’s, digit span and paired associates measures, where they reflect the results of Mann–Whitney U tests.

four younger and seven older subjects were rejected because there were too few (<16) artifact-free trials in one or more critical experimental conditions. All subjects in both age groups were native speakers of British English, and had normal or corrected-to-normal vision. All subjects were high-functioning, healthy individuals, with no history of significant neurological, cardiovascular, or psychiatric illness, or other serious systemic condition. Volunteers were also excluded if they were taking any neurotropic or vasoactive medication. As Table 1 indicates, the two groups were matched for level of education. Informed consent was obtained prior to participation, and the experimental procedures were approved by the Joint UCL and UCLH Committees on the Ethics of Human Research, and by the Institute of Neurology and National Hospital for Neurology and Neurosurgery Joint Research Ethics Committee. 2.2. Neuropsychological testing All subjects completed a battery of standardised neuropsychological tests to assess intelligence, memory, and language functioning, targeting certain cognitive functions that are generally impaired with age, and others that are usually found to be spared. These tests were administered in a separate 1.5 h session. Older subjects were first given the Folstein Mini Mental State test (MMS; Folstein, Folstein, & McHugh, 1975) as a screening measure, and a minimum score of 26/30 was required for inclusion in the study (Lezak, 1995). The test battery, described in more detail in Morcom et al. (2003), comprised the National Adult Reading Test (NART) Nelson, 1982), the Raven’s Advanced Progressive Matrices II (Raven, Raven, & Court, 1994), the Digit Span Forward and Verbal Paired Associates tests from the WMS-R (Wechsler, 1987), the Adult Memory and Information Processing Battery (AMIPB) short story recall test (Coughlan & Hollows, 1985), the Warrington-McKenna Graded Naming test (see Clegg & Warrington, 2000), and the FAS verbal fluency test (Lezak, 1995).

2.3. Materials Items were 406 colour pictures of nameable objects and the corresponding single word names of these objects. 288 object pictures and words with unanimous or near-unanimous name agreement among younger and older pilot subjects were selected as critical items (the majority of these were the same items as those employed by Robb and Rugg (2002), obtained primarily from images published in a variety of sites on the World Wide Web, and the set is available from the first author on request). The remaining 118 items of each type were employed as fillers. 16 sets of study and test lists were created, by randomly assigning the 288 critical items to each of four study lists of 36 items, and four lists of 36 unstudied items. Therefore in each set, a given item was equally likely to appear in the study-picture or the study-word condition, the easy or the hard condition, and to be studied or unstudied. Study lists comprised either pictures or words, whereas test lists contained words only. For each picture study list, the test list consisted of the 36 names corresponding to those pictures and 36 unstudied names. For each word study list, the test list comprised the 36 studied words and 36 unstudied ones. All lists were randomly ordered, and buffered with filler items at the beginning of the list and immediately after the mid-list pause (see below). For the ’hard’ study lists, 90 additional items (not later shown at test) served as filler items at randomly chosen locations to increase the length of the word lists (36 items) and picture lists (54 items), respectively. Pilot work indicated that these numbers of filler items were appropriate for equating recognition performance in the younger group in each of the hard conditions with that of the older group in each easy condition. 2.4. Procedure All stimuli were presented within a white frame in the centre of a black monitor screen. This frame subtended a

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visual angle of 2.25◦ × 2.25◦ . Pictures were shown in colour on a light grey background, and words in white upper case Arial font (vertical visual angle approximately 0.5◦ ) on a black background. In each study phase, the fixation character ‘+’ was presented for 500 ms, and an item then shown for 1500 ms. For pictures, the study task was to decide whether the item would, in real life, fit into a shoebox. For words, participants judged whether the referent would be more likely to be found indoors or outdoors. These tasks were chosen to encourage imagery-based encoding for pictures, and more ‘functional’ encoding for words, the aim being to maximize differences between the memory representations formed for the two classes of study material. Participants indicated their decisions by pressing a key with their left or right index finger. Each test trial began with the display of the fixation character ‘+’ for 1200 ms. The test item was then displayed for a duration of 500 ms. Following this, a second fixation character, ‘×’, remained on the screen for 2444 ms. The screen was then blanked for 200 ms before the start of the next trial. When pictures had been studied, participants were instructed to decide whether or not each word was the name of a studied picture. When words had been studied, they judged whether each test word had been shown at study. These judgements were signalled by either a left or a right hand key press. For the two easy study-test blocks the study-test interval was 30 s, and for the two hard blocks it was 5 min. There was a brief rest break half way through each test phase, and half way through the study lists in the hard conditions. Subjects practiced the study-word and study-picture conditions with short study and test lists prior to the start of the experiment proper. Each of the 16 sets of item lists (see above) was allocated to a matched pair of one younger and one older subject. Each subject performed all four combinations of the easy and hard, and study-picture and study-word conditions. In order to counterbalance task order and response hand, every possible order of these four conditions was rotated across the subject pairs, as was the hand used to signal old and new judgements.

Fig. 1. Electrode montage and sites analysed. Sites 48/38, 47/39 and 46/40 constitute the inferior set, sites 33/22, 31/24 and 30/25 the middle set, and sites 19/9, 17/11 and 29/26 the superior set.

were 2048 ms in length, with a 128 ms pre-stimulus baseline. Prior to averaging, the EEG was digitally smoothed (3 dB down at 19.4 Hz). A linear regression technique was then applied to correct the contribution of blink artifact, in which blinks are first identified using an automatic procedure, then the contribution of the vertical EOG to the blink signal on each channel is estimated, generating blink weights (betas), and finally the vertical EOG is multiplied by the blink weight for each channel and this component of the signal is removed (see e.g. Rugg et al., 1998; Tsivilis, Otten, & Rugg, 2001, for previous uses of this technique). Trials containing horizontal or vertical eye movements other than blinks were rejected, as were trials with A/D saturation or baseline drift exceeding ±55 ␮V. ERPs were formed for correctly classified new test items, and studied (old) test items, from each condition, and quantified by measurement of the mean amplitude (with respect to mean pre-stimulus baseline) of selected latency regions.

2.5. ERP recording and preprocessing 2.6. ERP analysis strategy EEG was recorded with silver/silver chloride electrodes from 31 sites. Twenty-nine of these electrodes were embedded in an elasticated cap (see Fig. 1), and represented a subset of the ‘montage 10’ described by the manufacturer (http://www.easycap.de/english/easycap/english/schemae. htm). The two remaining electrodes were placed on each mastoid process. Vertical and horizontal EOG were recorded from bipolar electrode pairs placed above and below the left eye and on the outer canthi of both eyes. EEG recordings were made with reference to a mid-frontal electrode (Fz), and subsequently re-referenced to linked mastoids. EEG and EOG were amplified with a bandwidth of 0.03–35 Hz (3 dB points) and digitized at 125 Hz. Recording epochs

The principal analyses of the ERP data, for new trials, were conducted on five latency regions (300–500, 500–800, 800–1100, 1100–1400, and 1400–1700 ms post-stimulus), selected on the basis of visual inspection to capture apparent effects of study material, difficulty and age group. Latency regions for the analyses of old/new effects were chosen to correspond as far as possible to those chosen for the new trials analysis, but were restricted to time windows characteristic of old/new effects described in the literature on recognition memory: 300–500, 500–800, and 1100–1700 ms post-stimulus. These were chosen to highlight possible early frontal, left parietal, and late right frontal old/new effects.

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Three sets of separate magnitude analyses were conducted on the ERP data, each in two parallel stages. These were motivated by the primary concern of the present study, which was with possible age-related differences in previously reported ERP ‘retrieval orientation’ effects. Other effects were of interest only inasmuch as they might inform the interpretation of such differences. The first set of analyses therefore investigated the effects of age on the processing of retrieval cues, unconfounded by the effects of retrieval success, following Robb and Rugg (2002); see also Herron and Rugg (2003). To do this, study material effects on ERPs elicited by correctly rejected new items were examined for the word compared with the picture condition. The second set of analyses were then conducted in order to characterise the ERPs of both age groups in terms of known neural correlates of successful recognition, by examining ERPs elicited by correctly classified old versus new items (old/new effects). These aimed to highlight age-related differences in old/new effects and any modulation of these by study material or task difficulty. A third, more restricted set of analyses were concerned with the characterisation of the effects of task difficulty and are described below. For the main two sets of analyses, the raw data were the mean amplitudes (with respect to the mean of the pre-stimulus baseline) of ERPs for the relevant latency regions. Group differences in the effects of interest (study material or old/new) were first assessed directly, using ANOVAs conducted on difference scores (words-pictures and hits-correct rejections, respectively). In the second stage, each group’s data were analysed separately. The latter analyses were carried out on the raw data, in order to characterise for each age group the effects of study material, or old/new effects, including main effects of these variables. Following the magnitude analyses, differences in the scalp topography of study material effects and old/new effects were assessed after the difference data for each had been rescaled to remove the confounding effect of inter-region and between-group differences in magnitude (McCarthy & Wood, 1985). These ANOVAs were also conducted in two stages. Analyses were carried out firstly of group differences in the scalp topography of these effects within and across latency regions where there were clear effects in both groups. Subsidiary analyses were also conducted of the temporal differences (across latency regions) in the topographic distribution of effects within each age group, including all latency regions where there was a clear effect in that group taken alone. Any interaction between group and electrode site would indicate a difference in the configuration of the generators of the relevant effect in the two age groups. Also of interest were interactions of scalp topography with latency region within a group, indicating a variation in the configuration of the generators over time for that group. Where group differences were found in scalp topography within any latency region, further analyses were carried out comparing groups across the different latency regions, and are reported only when they generate additional information about the

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points in time at which group differences in scalp generators occurred. Finally, planned analyses of both the ERP amplitude and rescaled data were conducted examining group differences in study material effects and old/new effects when the level of successful recognition was matched between the two age groups. This was done by including only data from the young subjects in the hard condition and the older subjects in the easy condition (see Section 1). Magnitude data were included from the electrode sites indicated in Fig. 1, while topographic analyses were conducted across all 29 scalp sites. The 18 sites were chosen to include the principal scalp locations of both study material and old/new effects. ANOVAs were factored according to hemisphere (left, right), anterior–posterior chain (frontal, anterior temporal/ central, posterior temporal/ parietal), and electrode site (inferior, middle, superior). Subsidiary ANOVAs were conducted on data from subsets of these sites or conditions as required to follow up significant findings. In all analyses, only effects involving the factor of age group or the relevant experimental factor/s are reported. Age differences in the magnitude of study material effects were further assessed by comparing the sites where these were largest in each of the two groups, to ascertain that apparent magnitude differences were not secondary to differences in the location of scalp maxima. The factor of task difficulty was principally of interest as a potential modulator of study material or old/new effects in the main analyses. Additional analyses were carried out to assess difficulty effects in each age group. However, to anticipate the findings, as there were no reliable group differences in the scalp distribution of these effects, and no group differences in their overall magnitude, only the presence or absence of main effects of difficulty in each group is reported. F ratios for factors with more than two levels are reported with degrees of freedom corrected for sphericity violation (Greenhouse & Geisser, 1959). 3. Results 3.1. Neuropsychological test findings Table 1 shows the results of the neuropsychological tests for the younger and older groups. The older group had a higher IQ as estimated by the NART, and better picture naming performance. Despite this, their long-term memory and fluid IQ scores were lower than those of the younger group. 3.2. Recognition memory performance Recognition memory performance for the two groups is summarised in Table 2. Memory accuracy was measured by the discrimination index Pr (Phit − Pfalse alarm ), and response

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Table 2 Percent correct in each age group and experimental condition, with associated reaction times (S.D.s in brackets) and memory accuracy and discrimination and response bias measures Pr and Br (see text) Easy

Hard

Word Old

Picture New

Younger subjects % corr. 88 (0.10) 93 (0.06) RT (ms) 892 (207) 979 (268) Pr 0.81 (0.11) Br 0.38 (0.29) Older subjects % corr. RT (ms) Pr Br

88 (0.07) 89 (0.14) 1055 (188) 1182 (181) 0.77 (0.13) 0.37 (0.35)

Old

Word

New

Old

Picture New

Old

New

85 (0.08) 94 (0.05) 986 (232) 1075 (224) 0.79 (0.09) 0.31 (0.23)

88 (0.08) 90 (0.08) 912 (183) 1028 (243) 0.78 (0.08) 0.46 (0.27)

86 (0.10) 89 (0.08) 985 (193) 1093 (230) 0.75 (0.11) 0.41 (0.27)

83 (0.08) 87 (0.10) 1164 (182) 1338 (216) 0.71 (0.12) 0.41 (0.23)

80 (0.16) 85 (0.15) 1151 (254) 1247 (162) 0.65 (0.15) 0.44 (0.31)

80 (0.11) 77 (0.14) 1161 (180) 1368 (221) 0.57 (0.15) 0.53 (0.22)

bias was estimated by the index Br (Pfalse alarm /1 − (Phit − Pfalse alarm )) (Snodgrass & Corwin, 1988). ANOVA of Pr revealed main effects of age (F(1, 30) = 15.45, P < 0.001), study material (F(1, 30) = 8.98, P < 0.005), and difficulty (F(1, 30) = 17.85, P < 0.001). There was also a significant interaction between age and difficulty (F(1, 30) = 5.54, P < 0.05). These effects reflected lower scores for older than younger subjects in all conditions, and an effect of difficulty that was reliable only in the older group (F(1, 15) = 14.32, P < 0.005 versus F(1, 15) = 3.59, n.s.). ANOVA of Br gave rise to a main effect of difficulty (F(1, 30) = 6.66, P < 0.05), reflecting a more conservative bias in the hard conditions in both age groups, but to no other effects. An ANOVA was also conducted on mean correct rejection RTs to parallel the ERP analyses of study material effects. This gave rise to a main effect of group, reflecting slower responses for older than for younger subjects (F(1, 30) = 13.24, P < 0.001). Responses across both subject groups were also slower in the hard than in the easy condition (main effect of difficulty: F(1, 30) = 7.16, P < 0.05), and when pictures had been studied compared with words (main effect of study material: F(1, 30) = 17.04, P < 0.001). There were no reliable interactions between any of these factors (maximum F = 2.73). Planned analyses were conducted to compare the performance of younger subjects in the hard condition with that of older subjects in the easy condition. For Pr, ANOVA gave rise to a reliable main effect of study material (F(1, 30) = 4.29, P < 0.05), but to no effects of group. For Br, there were no significant effects. ANOVA of correct rejection RTs revealed significant effects of group (F(1, 30) = 8.66, P < 0.01), and of study material (F(1, 30) = 9.98, P < 0.005). 3.3. ERP study material effects for new items Grand average ERPs elicited by correctly classified new items overlaid to identify the effects of study material are shown in Fig. 2, and the effects of task difficulty are illus-

trated in Fig. 4. Mean numbers of trials (range in brackets) comprising each subject’s waveforms were 27 (18–35) for the easy words condition, 26 (19–35) for easy pictures, 26 (16–33) for hard words, and 26 (17–31) for hard pictures for the young subjects, and 26 (19–33), 25 (16–33), 26 (17–33) and 23 (16–29), respectively, for the older subjects. An ANOVA with factors of group (young, older), study material (word, picture) and difficulty (easy, hard) confirmed that the groups did not differ reliably in this respect (maximum F = 2.63, n.s.). Fig. 3 illustrates the scalp distribution of study material effects for the latency regions 500–800 and 800–1100 ms post-stimulus. In the younger subjects, in both difficulty conditions, study material had a marked effect on ERPs elicited by new items, which are more positive-going when words were the study material. This differential activity is manifest from around 300 ms post-stimulus and is widespread across the scalp, with generally a right frontocentral maximum. In the older subjects, ERPs to new items also differ according to study material, but the effect appears less focal in its scalp distribution, and smaller in magnitude than in the young, with a left fronto-central maximum. It also appears to onset later, around 500 ms post-stimulus, and to decay more quickly, to be replaced by a negative-going effect. As evident in Fig. 4, in both groups the aforementioned effects of study material are accompanied by effects of difficulty. From around 300 ms post-stimulus, ERPs to items from the easy conditions demonstrate a positivity relative to those elicited in the hard conditions. 3.3.1. Magnitude analysis at 18 central sites For the between-group analyses (see Section 2), ANOVAs had factors of group (young, older), retrieval difficulty (easy, hard), and the electrode site factors of hemisphere (left, right), anterior–posterior chain (frontal, anterior temporal/central, posterior temporal/ parietal), and electrode site (inferior, middle, superior); see Fig. 1. Since the dependent variable was the ERP difference score for correctly clas-

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Fig. 2. Grandaverage ERP waveforms from 18 electrode sites (see Fig. 1), showing study material effects for A: younger and B: older subjects (N = 16 per group). Waveforms are shown for ERPs elicited by correctly classified new words following word and picture study tasks, collapsed across retrieval difficulty. The baseline timescales include major tick marks at 0 and 800 ms post-stimulus (as do the waveform timescales), and additional minor tick marks at 200, 400 and 600 ms.

sified new items (word-picture condition), any significant effect involving the group factor indicates a group difference in study material effects. For the within-group analyses, ANOVAs had factors of study material (word, picture), retrieval difficulty (easy, hard), hemisphere (left, right), anterior–posterior chain (frontal, anterior temporal/central, posterior temporal/parietal), and electrode site (inferior, middle, superior). Except where specified, the finding of a study material effect indicates that ERPs in the word con-

dition were more positive-going than those in the picture condition. 3.3.1.1. 300–500 ms. ANOVA revealed a reliable main effect of group (F(1, 30) = 9.68, P < 0.005) and a four-way interaction of group with difficulty, chain and site (F(2.6, 78.7) = 3.74, P < 0.05). An ANOVA in the young group demonstrated a reliable main effect of study material F(1, 15) = 14.35, P < 0.005, mean

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Fig. 3. Voltage maps showing the scalp distributions in the 500–800 and 800–1100 ms latency ranges of the study material effects (word minus picture) in the younger and older groups. Maps are normalized with respect to maxima and minima within each region.

1.2 ␮V, and no reliable interactions involving this factor. ANOVA in the older group demonstrated no main effect of study material (mean amplitude = 0.0 ␮V), but a reliable interaction of study material with difficulty and chain (F(1.2, 17.6) = 6.40, P < 0.05). However, subsidiary ANOVAs performed separately at anterior and posterior scalp locations at each level of task difficulty demonstrated no reliable main effects of study material. Main effects of difficulty were not reliable in either age group (for young, F(1, 15) = 3.54, 0.05 < P < 0.1; for older, F(1, 15) = 2.20, n.s.). These findings reflect study material effects that are robust in the young group, where they are largest over the frontal and right central scalp, and insensitive to task difficulty. In the older group, by contrast, study material effects are significantly smaller, reverse their anterior–posterior gradient in the two difficulty conditions, and are do not achieve significance when tested at the sites where they are maximal (see Fig. 3). 3.3.1.2. 500–800 ms. ANOVA across groups gave rise to a main effect of group, (F(1, 30) = 12.15, P < 0.005), and an interaction of group with hemisphere (F(1, 30) = 7.92, P < 0.01). An ANOVA in the young demonstrated a reliable main effect of study material (F(1, 15) = 45.72, P < 0.001), and an interaction of study material with hemi-

sphere (F(1, 15) = 5.00, P < 0.05). In the older group, the main effect of study material was also reliable (F(1, 15) = 16.46, P < 0.001), as was the interaction of this variable with hemisphere and chain (F(1.5, 22.8) = 7.14, P < 0.01). These group differences reflected the fact that in the young group the study material effect is most pronounced over the right hemisphere, whilst in the older group it is reliable but smaller than in the young, and appears focussed over the left anterior scalp (see Figs. 2 and 3). In this latency region there was also a clear main effect of difficulty in both groups, with ERPs more positive-going in the easy than in the hard condition (for young, F(1, 15) = 22.64, P < 0.001; for older, F(1, 15) = 7.05, P < 0.05). In the older group, the three-way interaction of study material with difficulty and chain was reliable (F(1.3, 19.5) = 4.20, P < 0.05). 3.3.1.3. 800–1100 ms. ANOVA showed no significant group differences in study material or difficulty effects. The former were numerically larger in the younger group, but reliable in both groups separately (means 1.6 and 0.9 ␮V for young and older; F(1, 15) = 21.20, P < 0.001, F(1, 15) = 7.06, P < 0.05, respectively). 3.3.1.4. 1100–1400 ms. In this latency region, ANOVA gave rise to reliable interactions of group with hemisphere

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Fig. 4. Grandaverage ERP waveforms from 18 electrode sites (see Fig. 1), showing retrieval difficulty effects (easy versus hard conditions), collapsed across study material, for A: younger and B: older subjects (N = 16 per group) (for timescale details see legend to Fig. 2).

and with chain (F(1.6, 49.2) = 5.98, P < 0.01), and with difficulty, chain and site (F(2.9, 87.6) = 3.46, P < 0.05). Subsidiary ANOVA in the young subjects demonstrated a reliable main effect of study material (F(1, 15) = 6.95, P < 0.05), and also an interaction of study material with difficulty, hemisphere and site (F(1.9, 29.2) = 4.90, P < 0.05). Further follow-up analyses in the young showed that in the easy condition the effects of study material were not reliable, but in the hard condition there was an interaction of study material with chain and site (F(2.1, 32.1) = 3.51, P < 0.05). There was also an interaction of study material with hemisphere and site (F(1.9, 28.7) = 5.37, P < 0.05). These effects reflected a right superior scalp focus of study material effects in the young, in the hard condition. In the

older group, however, ANOVA did not reveal any reliable effects of study material. In the young subjects, there remained a reliable main effect of difficulty in this latency region (F(1, 15) = 10.76, P < 0.005). In the older subjects, the main effect was marginal (F(1, 15) = 4.31, 0.05 < P < 0.1), but its magnitude did not differ reliably from that in the young (for interaction of group and difficulty in separate ANOVA, F < 1; means across 18 channels were 0.9 and 0.7 ␮V in young and older). 3.3.1.5. 1400–1700 ms. ANOVA revealed reliable 4-way interactions of age group with difficulty, hemisphere and site (F(1.7, 51.3) = 5.20, P < 0.05) and with difficulty, chain

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and site (F(3.0, 89.0) = 5.19, P < 0.005). In the young, as in the previous latency region, an ANOVA showed a reliable main effect of study material (F(1, 15) = 5.22, P < 0.05). There were also interactions of study material with difficulty, hemisphere and chain (F(1.5, 23.0) = 5.61, P < 0.05), with difficulty, hemisphere and site (F(1.9, 29.2) = 6.29, P < 0.01), and with difficulty, chain and site (F(2.8, 41.6) = 3.35, P < 0.05). Study material effects were again reliable only in the hard condition, where there was a main effect (F(1, 15) = 5.17, P < 0.05), and interactions of study material with hemisphere and chain (F(1.9, 28.3) = 4.02, P < 0.05) and hemisphere and site (F(1.9, 28.5) = 4.50, P < 0.05), which reflected maxima at anterior left and posterior superior right sided scalp locations. In the older subjects, there were no reliable effects of study material. Difficulty effects, however, remained significant in this latency region in both age groups (for main effect in young, F(1, 15) = 5.87, P < 0.05; in older, F(1, 15) = 5.00, P < 0.05) 3.3.2. Comparison of scalp maxima Inspection of the data indicated that the electrode sites employed in the foregoing analyses were closer to the scalp maximum of the study material effects in the younger than in the older group (see Fig. 3), and consequently the main analyses could have overestimated age differences in the magnitude of these effects. Separate between-groups analyses were therefore conducted for the latency regions 300–500 and 500–800 ms, using only data from the single electrode sites showing the largest study material effect in each group. The relevant electrode sites for the earlier interval were C4 for the young, and LF for the older subjects, and for the later interval, Fz and Fp1, for the younger and older subjects, respectively (see Figs. 1 and 3). For the 300–500 ms region, ANOVA on word-picture ERP differences revealed a reliable main effect of group (F(1, 30) = 4.50, P < 0.05), but no interaction of group with difficulty (F(1, 30) = 2.66, n.s.). On average, the study material effect magnitude was 1.9 ␮V in the younger and 0.6 ␮V in the older group; importantly, a subsidiary ANOVA on the raw ERP data indicated that the effect in the older group was not reliable (F(1, 15) = 2.80, n.s.). In the 500–800 ms latency range, there was again a reliable main effect of group, and no interaction with difficulty (F(1, 30) = 8.00, P < 0.01; F(1, 30) = 2.43, n.s., respectively; magnitudes 3.9 and 1.9 ␮V). In contrast to the earlier latency regions, the main effect of study material for the older group was reliable in this latency region (F(1, 15) = 42.59, P < 0.001). 3.3.3. Topographic analysis ANOVA of rescaled study material (word-picture) data was conducted across the two latency regions where both groups showed clear effects of study material, i.e. from 500 to 800 and 800 to 1100 ms. There were no reliable differences in the scalp topography of the effects between the two

groups or latency regions (maximum F = 1.92, n.s.). Separate ANOVAs of rescaled data were also conducted across all latency regions in the young, as well as the two regions specified above in the older group, to determine whether the scalp topography of study material effects changed over time post-stimulus. These generated no reliable effects. An additional rescaled analysis exploring group differences in the scalp topography of difficulty effects (easy–hard) also did not give rise to any significant findings (maximum F = 1.45, n.s.). 3.3.4. Magnitude analysis matched for difficulty In these analyses, details are given only of group differences, and subsidiary findings that may qualify the conclusions from the overall analyses reported above. For the 300–500 ms interval, ANOVA revealed a reliable interaction of group with chain (F(1.2, 35.9) = 4.74, P < 0.05). An ANOVA in the young group showed a reliable main effect of study material (F(1, 15) = 7.11, P < 0.05), along with an interaction with hemisphere and chain (F(1.5, 23.0) = 10.21, P < 0.001). In the older group, there were no reliable effects of study material. These findings reflect study material effects that in the young are robust and largest over right anterior scalp regions, whilst in the old they are small, variable in polarity across the scalp, and statistically nonsignificant. For the 500–800 ms interval, ANOVA gave rise to a reliable main effect of group and an interaction of group with hemisphere (F(1, 30) = 4.43 and 4.87, respectively, P < 0.05). Subsidiary ANOVAs supported the findings reported above of a study material effect that was largest on the right in the young, and on the left in the older group. ANOVA for the 800–1100 ms interval showed no reliable group differences in study material effects, although the effects were reliable in the young group but not in the old group taken alone (means 1.8 and 0.5 ␮V; F(1, 15) = 14.38, P < 0.005, F < 1, respectively). For 1100–1400 ms, ANOVA revealed only an interaction of group with study material, hemisphere and chain (F(1.6, 46.5) = 8.62, P < 0.005), reflecting, as described above, study material effects that were reliable only in the young, and were largest on the right at both anterior and posterior scalp locations. For the 1400–1700 ms latency region, ANOVA gave rise to a reliable interaction of group with study material (F(1, 30) = 12.14, P < 0.005), because the study material effect was positive in the young (for simple main effect, F(1, 15) = 5.17, P < 0.05), but negative in the older subjects (F(1, 15) = 7.06, P < 0.05). 3.3.5. Topographic analysis matched for difficulty For the rescaled data where difficulty was matched, ANOVA did not give rise to any reliable group differences in the scalp topography of the study material effect from 500 to 800 ms or from 800 to 1100 ms. 3.3.6. Summary of ERP study material effects Despite subtle effects involving the factors of site (not reflected in the topographical analyses where magnitude

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Fig. 5. Top: Mean amplitudes (and standard errors) of study material effects (word minus picture) for young and older subjects in the latency regions 300–500, 500–800, 800–1100, 1100–1400, and 1400–1700 ms, averaged across the 18 electrode sites analysed (see Fig. 1). Bottom: mean amplitudes (and standard errors) of difficulty effects (easy minus hard) for young and older subjects for the same latency regions and sites.

effects were eliminated by rescaling) and difficulty, these analyses demonstrate that material effects were slower to onset, and smaller in magnitude, in the older subjects regardless of difficulty. These effects can be well appreciated in Fig. 5, which illustrates the mean across-site magnitude of the effects, and those due to difficulty, according to latency region and group. 3.4. ERP old/new effects Grand average ERPs elicited by correctly classified old and new items are shown in Fig. 6. Mean numbers of trials comprising each subject’s waveforms for hits were as follows (range in brackets; for correct rejections, see above): 26 (16–33) for the easy words condition, 23 (16–32) for easy pictures, 25 (17–34) for hard words, and 25 (18–30) for hard pictures for the young subjects, and 25 (17–31), 24 (19–31), 23 (16–36) and 23 (16–30), respectively, for the older subjects. As for the new trials, an ANOVA with factors of group (young, older), study material (word, picture) and difficulty (easy, hard) was conducted on these data, and no reliable group differences were found (F < 1 for all). Fig. 7 illustrates the scalp distribution of old/new effects for the three latency regions analysed (see Section 2), with old/new effects in the first latency region subdivided according to task difficulty. In the younger subjects, ERPs to hits are generally more positive-going than those to correct rejections from around 300 ms post-stimulus. The waveforms clearly demonstrate two of the features reported in previous studies of recog-

nition memory. Notably, between approximately 500 and 800 ms post-stimulus, this positivity of ERPs to old versus new items (or old/new effect) has an left centroparietal maximum, and this then shifts to a more right frontal maximum from around 1100 to 1700 ms. Between 300 and 500 ms the picture is less clear cut, as the old-new difference is maximal over the left frontocentral scalp, but this lateralisation appears predominantly to reflect its distribution in the easy condition. In the older group, ERPs also show positive old/new effects from around 300 to 1700 ms post-stimulus, but the distribution of their maxima over the scalp is approximately right and frontocentral throughout the recording epoch. 3.4.1. Magnitude analysis at 18 central sites In parallel with the new item analyses (see Section 2), across-group ANOVAs had factors of group (young, older), study material (word, picture), retrieval difficulty (easy, hard), and the electrode site factors of hemisphere (left, right), anterior–posterior chain (frontal, anterior temporal/central, posterior temporal/parietal), and electrode site (inferior, middle, superior); see Fig. 1. As these were conducted on ERP difference scores (here, hits-correct rejections), any significant effect involving the factor group indicates a age-related difference in old/new effects. Within-group ANOVAs had factors of old/new, study material (word, picture), retrieval difficulty (easy, hard), hemisphere (left, right), anterior–posterior chain (frontal, anterior temporal/central, posterior temporal/ parietal), and electrode site (inferior, middle, superior). Unless otherwise

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Fig. 6. Grandaverage ERP waveforms from 18 electrode sites (see Fig. 1), showing old/new effects (hits vs. correct rejections), collapsed across study material and difficulty, for A: younger and B: older subjects (N = 16 per group) (for timescale details see legend to Fig. 2).

specified, the finding of an old/new effect indicates that ERPs for hits were more positive-going than those for correct rejections. 3.4.1.1. 300–500 ms. ANOVA gave rise to interactions of group with hemisphere (F(1, 15) = 4.95, P < 0.05) and of group with difficulty and hemisphere (F(1, 30) = 11.34, P < 0.005). There were no significant group differences involving the factor of study material, although there was an overall main effect of study material (F(1, 30) = 6.17, P < 0.05), reflecting old/new effects that are generally larger in the picture condition in both age groups.

In the young, ANOVA demonstrated reliable interactions of old/new with hemisphere (F(1, 15) = 8.11, P < 0.05), with site (F(1.2, 17.8) = 10.44, P < 0.005), and with chain and site (F(1.9, 29.9) = 5.72, P < 0.01), as well as a reliable interaction of old/new with difficulty and hemisphere (F(1, 15) = 5.43, P < 0.05). The latter effect reflected old/new effects in this group that have a left sided focus in the easy condition (subsidiary ANOVA demonstrating an interaction of old/new and hemisphere, F(1, 15) = 19.68, P < 0.001), but are relatively central in the hard condition. The other interactions reflect the fact that old/new effects were generally larger at superior, and anterior and posterior

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Fig. 7. Voltage maps showing the scalp distributions of the old/new effects (hits vs. correct rejections) in the 300–500, 500–800 and 1100 1700 ms latency ranges in the younger and older groups. In the first latency region, separate voltage maps are given for both groups according to task difficulty (see inset). Maps are normalized with respect to maxima and minima within each region.

(but not middle) scalp locations, and over the left hemisphere (see Figs. 6 and 7). In the older group, ANOVA revealed interactions of old/new with study material (F(1, 15) = 4.68, P < 0.05), and of both of these factors with hemisphere and chain (F(1.4, 20.6) = 4.62, P < 0.05). These findings reflected old/new effects that are larger in magnitude in the picture condition, over the right hemisphere, and at central scalp sites (see Fig. 7). 3.4.1.2. 500–800 ms. ANOVA revealed a main effect of study material (F(1, 30) = 7.07, P < 0.05), reflecting again the generally larger old/new effects in the picture condition (means = 1.2 versus 0.9 ␮V). There were also reliable interactions of group with hemisphere (F(1, 30) = 4.19, P < 0.05) and with difficulty and hemisphere (F(1, 30) = 8.56, P < 0.01), and of group with site (F(1.1, 33.1) = 8.10, P < 0.01). These reflected a more marked superior focus of old/new effects in the young than in the older group, and apparent differences in lateralisation of old/new effects in the older group according to difficulty (see below). The subsidiary ANOVA in the young demonstrated a significant main effect of old/new (F(1, 15) = 13.81, P < 0.005), and interactions of old/new with site (F(1.1, 16.2) = 33.76, P < 0.001) and with chain and site (F(1.7, 25.3) = 6.49, P < 0.01). As can be seen in Fig. 7, these findings reflect old/new effects with a narrowly superior scalp maximum at anterior sites, and a broader focus at the central and posterior sites.

In the older group, ANOVA revealed interactions of old/new with difficulty and hemisphere (F(1, 15) = 11.02, P < 0.005), and of old/new with site (F(1.1, 17.0) = 5.38, P < 0.05). Subsidiary analysis for the two difficulty conditions showed a reliable interaction of old/new with hemisphere for the easy condition only (F(1, 15) = 7.42, P < 0.05). In the older group, old/new effects are generally larger over superior scalp sites. In the easy condition they are right lateralised, but they are more bilateral in the hard condition. 3.4.1.3. 1100–1700 ms. ANOVA demonstrated reliable main effects of study material (F(1, 30) = 15.67, P < 0.001), of difficulty (F(1, 30) = 18.21, P < 0.001), and of hemisphere (F(1, 30) = 12.40, P < 0.001), and an interaction of group with difficulty and hemisphere (F(1, 30) = 5.15, P < 0.05). The latter interaction reflected a group difference in the lateralisation of old/new effects in the easy condition, but subsidiary analyses of old/new effects by group and hemisphere demonstrated that none of these were reliable. In the hard condition (and overall), old/new effects were larger on the right in both age groups. An ANOVA in the young showed significant interactions of old/new with study material (F(1, 15) = 10.29, P < 0.005), with difficulty (F(1, 15) = 13.49, P < 0.05), and with hemisphere (F(1, 15) = 5.19, P < 0.05). Interactions of old/new with chain and site (F(2.6, 39.0) = 11.76, P < 0.001), and with study material, difficulty, hemisphere and site (F(1.7, 24.9) = 3.85, P < 0.05) were also significant. The latter interaction mainly reflected the influence

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of old/new effects that were individually non-significant, and variable in polarity across the scalp, in the easy picture condition. However the findings in general reflect old/new effects in this group that are larger in the picture condition and in the hard condition, and are largest over the right hemisphere and at frontocentral sites. The ANOVA in the older group showed reliable interactions of old/new with study material (F(1, 15) = 5.40, P < 0.05), with difficulty (F(1, 15) = 5.73, P < 0.05), and with hemisphere (F(1, 15) = 8.27, P < 0.05), as in the younger group. There was also a significant interaction of old/new with difficulty and site (F(1.3, 19.8) = 8.49, P < 0.005). These findings reflect old/new effects that are (as in the young) larger in the picture condition, and overall are most marked on the right. These effects are also again larger in the hard condition, but particularly at central sites. 3.4.2. Topographic analysis ANOVA of rescaled data for the 300–500 ms latency region showed that the scalp distribution of old/new effects differed significantly according to age and difficulty (for interaction of group with difficulty and site, F(4.1, 121.8) = 2.52, P < 0.05). Within-group ANOVAs did not show reliable effects of difficulty on topography in either group, but comparisons by difficulty revealed a significant group difference only in the easy condition (F(3.5, 104.2) = 2.6, P < 0.05; for hard condition, F < 1). As seen in Fig. 7, in the easy condition old/new effects have two foci in the young, over the central and posterior scalp, and one over the left frontal scalp in the older group. Between 500 and 800 ms, there was a significant group difference in the topography of old/new effects irrespective of difficulty (for interaction of group with site, F(4.2, 126.6) = 2.73, P < 0.05), reflecting scalp maxima over the central/left parietal scalp in the young and the right frontocentral scalp in the older group. From 1100 to 1700 ms, there were no reliable group differences or effects of study material. Analysis for the young group alone did not reveal a reliable change in the effects of difficulty on the scalp topography of old/new effects over time, but did show a change in their overall topography between 500–800 and 1100–1700 ms post-stimulus (F(4.1, 61.9) = 11.79, P < 0.001). In the older group, there were no reliable changes in the scalp topography of old/new effects over peri-stimulus time. These findings reflected the shift of old/new effects from a left central to a right frontocentral focus in the young, whilst in the older group there was a right frontocentral focus throughout the recording epoch. 3.4.3. Magnitude analysis matched for difficulty For 300–500 ms, ANOVA revealed a reliable interaction of group with study material and chain (F(1.2, 35.1) = 5.12, P < 0.05). However, subsidiary ANOVAs did not demonstrate any significant interactions of old/new with study material for either group. The group difference appeared to reflect a tendency for the scalp maximum of old/new ef-

fects in the picture condition to be anterior in the young, and central/posterior in the older group. Between 500 and 800 ms, ANOVA gave rise to reliable interactions of group with hemisphere (F(1, 30) = 5.69, P < 0.05) and with site (F(1.1, 34.0) = 6.58, P < 0.05). Subsidiary ANOVA in the young demonstrated interactions of old/new with site (F(1.1, 16.2) = 18.90, P < 0.001), and in the older group, old/new interacted with hemisphere (F(1, 15) = 7.42, P < 0.05). Old/new effects in the young have a central scalp distribution, but in the older group they are predominantly right sided. 3.4.4. Topographic analysis matched for difficulty ANOVA of the rescaled data comparing the two age groups was also carried out with difficulty matched. This revealed reliable age differences in the scalp topography of old/new effects only for the latency region 500–800 ms (F(4.7, 139.7) = 2.91, P < 0.05), as has been described above. 3.5. Summary of ERP old/new effects These analyses confirm the presence of clear old/new effects in both age groups. They also support the observation that age differences in these effects occur relatively early in the recording epoch, most notably between 500 and 800 ms, where a left centroparietal old/new effect is present only in the young group. Both groups show a robust old/new effect with a right frontocentral maximum towards the end of the recording epoch. The topography of these old/new effects and the group differences in their magnitude were not modulated by study material or by difficulty, although old/new effects were generally larger in the study-picture condition, and in the hard condition, particularly in the latter part of the recording epoch. In addition, in both groups there are small old/new effects between 300 and 500 ms post-stimulus which are modulated by task difficulty, and which show group differences in their scalp distribution in the easy condition only, being largest at left anterior and posterior sites in the young, and at right middle sites in the older group.

4. Discussion This study explored whether the neural correlates of the differential processing of retrieval cues vary with age. In the younger subjects, the effects of study material on ERPs elicited by test items replicated previous findings (Herron & Rugg, 2003; Robb & Rugg, 2002), although the difficulty effects elicited in this study differed from those previously reported by Robb and Rugg (2002). The effects of study material in the older subjects onset later and offset sooner than those in the younger group, and were smaller in magnitude. These inter-group differences remained when recognition accuracy was matched. Old/new effects also showed age-related differences, consistent with the presence of a left

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parietal old/new effect in the young group only. In both age groups, old/new effects were larger in the picture condition and in the hard condition, but these factors did not interact with age. The implications of these findings for accounts of age-related decline in episodic memory are considered below, following a discussion of the behavioral data. 4.1. Behavioural findings The neuropsychological test scores revealed the typical pattern of age-related reduction on tests of long-term memory and fluid intelligence (Light, 1991). In addition, recognition accuracy on the experimental task was lower, and responses slower, in the older group. These subjects were also more sensitive to the difficulty manipulation than were the younger subjects. As in the study of Robb and Rugg (2002), recognition memory was more accurate, and response time to new items faster, when words rather than pictures had been studied. These findings are consistent with Robb and Rugg’s observation that the influence of study item-retrieval cue compatibility on recognition memory performance outweighed any tendency towards superior memory for pictures (see also Herron & Rugg, 2003). This behavioural pattern did not vary according to age, in keeping with the usual finding that encoding specificity effects are preserved in older adults (see Light, 1996). This finding supports the interpretation of the age-related differences in ERP findings (see below) in terms of a reduction in the specificity of retrieval cue processing, rather than the engagement of qualitatively different encoding strategies in the two age groups. Unlike in Robb and Rugg’s (2002) study, in the present experiment response criterion was influenced by the difficulty manipulation, with subjects adopting a stricter criterion in the hard than in the easy condition. Since this effect did not differ with age or study material, it does not confound the ERP comparisons between age groups or study materials, although it may have influenced the ERP correlates of task difficulty (see below). 4.2. ERP findings 4.2.1. Study material effects In both groups, ERPs elicited by new items showed a sustained positive shift when words were the study items rather than pictures. In the younger subjects, this effect was strikingly similar in both time course and scalp distribution to that reported by Robb and Rugg (2002), onsetting around 300 ms post-stimulus and lasting throughout most of the recording epoch. It had a central/right scalp maximum, compared with the central maximum described by Robb and Rugg (2002). As in the previous study, the topography of the effect did not change over time, suggesting that a single set of neural generators was responsible. In the older subjects, the study material effect was smaller, onset later, and was less sustained, reversing in polarity after around 1400 ms.

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Its scalp topography also did not change reliably over time, and was indistinguishable from that found in the young, implicating the same neural generators in differential cue processing in older and younger subjects. In the magnitude analysis, although there appeared to be some modulation of the scalp distribution of study material effects according to task difficulty early in the recording epoch, this was eliminated by rescaling and is therefore likely to be secondary to the differences in the magnitude of the effect across the scalp (McCarthy & Wood, 1985). In addition, although difficulty appeared to modulate study material effects in the older group in the 300–500 ms latency region, the effects varied in polarity and were not reliable at the sites analysed. These age-related differences in the ERP correlates of retrieval orientation are not explicable in terms of simple behavioural differences. Crucially, the group differences were essentially unchanged when recognition accuracy was equated by comparing ERPs for the hard condition in the younger with those for the easy condition in the older subjects. This suggests that the age-related differences in the study material effect do not simply reflect differences in the neural correlates of cue processing associated with relatively good versus relatively poor performance. One caveat to this conclusion comes from the finding that while recognition accuracy could be matched between the groups, RTs to new items remained slower in the older group. Another potential caveat is that if there were greater variability in the older than the younger subjects in the timing of the differential ERP responses to retrieval cues, and hence greater across-trial jitter in study material effects, these effects would appear to be smaller in the older group. Such a mechanism would, however, result in effects that were more, rather than less, extended in time than those in the young subjects. Regarding the apparent reversal of direction of the study material effect at the end of the recording epoch in the older group, we note that this was reliable only in the easy condition taken alone (in the difficulty matched analysis), whilst in the overall analysis there was neither a main effect of study material nor an interaction with difficulty in this group. Thus, the ‘reversed’ effect appears not to be robust, and indeed it has not been observed in previous studies of retrieval cue effects in the young (Herron & Rugg, 2003; Hornberger, Morcom, & Rugg, in press; Robb & Rugg, 2002). 4.2.2. Difficulty effects The effects of task difficulty on ERPs elicited by retrieval cues in this study were different from those of Robb and Rugg (2002). In the latter study, difficulty effects were not only additive with those of study material, but they were separable in time, being reliable only for the first 300 ms post-stimulus. In the present study, however, difficulty effects were sustained throughout much of the recording epoch. What might be the explanation for this discrepancy? The picture study task used here was only subtly different from

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that employed by Robb and Rugg (2002), and the word study task was identical. Moreover, the difficulty manipulations in the previous and present studies were also identical. Thus, the disparate difficulty effects in the previous and present studies seem unlikely to be due to procedural differences. One possibility is that the present effects are a correlate of the shift in response criterion that occurred between the two difficulty conditions, a shift that was not found in Robb and Rugg (2002); c.f. Windmann, Urbach, and Kutas (2002). Regardless of the reasons for the different effects of difficulty between the present and previous study, it is important to note that, unlike the effects of study material, neither the timing nor the magnitude of the difficulty effects varied with age (see Figs. 4 and 5). Thus, the age-related differences evident in the study material effects do not merely reflect a general insensitivity of older individuals’ ERPs to changes in task demands. 4.2.3. Old/new effects Old/new effects and their scalp generators differed according to age in the first latency region, and this difference was modulated by task difficulty. Old/new effects between around 300–500 ms post-stimulus have previously been associated with familiarity processing in recognition memory tasks (e.g. Curran, 2000; Rugg et al., 1998), although these effects typically have a frontocentral distribution. To our knowledge, age-related differences in these early effects have not previously been reported, and there is substantial evidence to suggest a relative preservation of familiarity with age in recognition memory (Yonelinas, 2001). Evidently, more is reflected by old/new effects in this latency range than an undifferentiated sense of familiarity (see also Rugg et al., 1998; Tsivilis et al., 2001); however the functional significance of the present findings remains obscure. From 500 to 800 ms post-stimulus, old/new effects in the young group showed the typical central/left posterior focus consistent with the posterior or ‘left parietal’ old/new effect reported in numerous previous studies of recognition memory (see Friedman, 2000; Rugg et al., 2002 for review). This effect was essentially absent in the older group. The late right frontocentral old/new effect, on the other hand, was common to the two age groups. Despite appearing to be less focused over the right frontal scalp in the older group, its scalp distribution, and hence the disposition of its generators, did not differ significantly according to age. In the context of previous functional descriptions of right frontal old/new effects (e.g. Rugg & Wilding, 2000), and given the timecourse of this effect, it likely represents processes that operate on the products of retrieval. It has been argued previously that such processes are relatively unaffected by age (Li, Morcom, & Rugg, in press; Mark & Rugg, 1998; but see Trott et al., 1997; Wegesin et al., 2002). As might be expected, these processes (Rugg et al., 2002) appear to be modulated by difficulty, in that the ERP effects are larger both for the hard conditions, and for picture rather than word retrieval.

4.3. General discussion The present findings suggest that whereas healthy older adults process retrieval cues differentially, this differential processing is applied less consistently, or to a lesser degree, than is the case in younger individuals. Given the preservation of this age-related difference when level of recognition accuracy was matched between the two groups, the difference is unlikely merely to reflect a disparity in recognition performance. As noted above, RT was slower in the older group even when accuracy was matched, and the later onset of the study material effect in these subjects might therefore be a reflection of age-related cognitive slowing (Salthouse, 1996), rather than of a specific impairment of retrieval cue processing (see Mark & Rugg, 1998, for an example of such a finding). Cognitive slowing cannot, however, easily account for the earlier offset and the smaller magnitude of the effect. There are a number of possible reasons why retrieval cues might be processed in a less differentiated way by older than younger adults. Firstly, the memory representations laid down by older subjects may be less specific than those laid down by the young. This would be consistent with the wealth of data suggesting age-related impairments in episodic memory encoding, and particularly with evidence that older adults do not process to-be-remembered material as elaboratively as younger adults (see Craik, 2000; Light, 1996 for review). Although such age-related encoding difficulties are minimised by the use of specific, semantically-oriented, study tasks, as here, they are probably not eliminated entirely, and encoding may still be less distinctive (cf. Morcom et al., 2003). However, as mentioned earlier, it is unlikely that encoding difficulties are sufficient in themselves to explain age-related changes in episodic memory, and many encoding manipulations benefit older and younger adults’ memory to an equivalent extent (Craik, 2000; Light, 1996). Furthermore, had the older subjects in the present study encoded the pictures and words less distinctively than the young group, this should have been reflected in a smaller ‘encoding specificity effect’ (Morris, Bransford, & Franks, 1977; Tulving & Thomson, 1973), that is, in a smaller disparity in recognition performance for pictures versus words. The disparity did not, however, differ according to age, supporting previous findings (see Light, 1996 for review). It seems likely, therefore, that the age-related ERP effect observed here does not result entirely from age differences in encoding operations. What might the effect signify in terms of age effects on retrieval processing? One possibility is that it is secondary to the predominance in older adults of familiarity-based responding, as opposed to recollection, in recognition memory tests (Yonelinas, 2001). On presentation of a retrieval cue, older adults may fail to engage search processes because these are unlikely to yield successful recollection. There may therefore be strategic reasons, secondary to a recollective impairment, for the reduction in the differential processing of cues according to the way that

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information was encoded. Data supporting such an interpretation would be informative about the characteristics of recollection and familiarity, but would not explain older adults’ recollective impairment. Perhaps a more interesting account of the present findings is the converse possibility, referred to earlier, that older adults have impaired recollection because they do not process retrieval cues effectively, and that their greater reliance on familiarity is a consequence rather than a cause of this. The present data cannot speak to this distinction, and the pattern of group differences in old/new effects, and specifically the absence of a left parietal effect in the older group, is consistent with both possibilities. An important direction for future work will be to determine whether the ERP correlates of retrieval cue processing are influenced by experimental manipulations which vary the relative probabilities of familiarity- and recollection-based recognition. More generally, the present data are consistent with the possibility that it is not the amount of ‘support’ provided by retrieval cues that is the main determinant of age-related differences in memory performance (Craik, 1983, 2000), but rather the requirement to implement a controlled memory search (see Light, 1996). An age-related impairment in controlling search might perhaps reflect a more general impairment in cognitive control (Moscovitch & Winocur, 1995; West, 1996). It is also consistent with the view that episodic retrieval involves an active specification of ‘search parameters’ (Burgess & Shallice, 1996), and one consequence of ageing may be to compromise the ability to achieve such a specification.

5. Conclusions This study provides evidence that the neural correlates of retrieval cue processing differ according to age. Although older adults are able to process retrieval cues differentially according to the nature of the material to be retrieved, the present ERP data show that this differential processing is attenuated compared with that engaged by younger adults, although there is no evidence that cue processing recruits different neural generators in the two age groups. Further work is required in both younger and older adults to determine which aspects of differential cue processing are associated with the ERP retrieval orientation effect and its modulation by age, and to ascertain their impact on age-related episodic memory impairment.

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