Material-speci c neural correlates of memory retrieval

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1 BRAIN IMAGING Material-speci c neural correlates of memory retrieval Yee Y. Yick and Edward L. Wilding Cardi University Brain Research Imaging Centre, School of Psychology, Cardi University, Cardi, Wales, UK Correspondence toyeey.yick, School of Psychology, Cardi University, Cardi CF10 3AT, Wales, UK Tel: ; fax: ; Received 26 June 2008; accepted1july 2008 DOI: /WNR.0b013e32830ef76f It is well established that the neural activity engaged during memory retrieval varies with the kinds of information that are recovered. Less well established is whether this activity re ects online recovery of information, or processes operating downstream of successful recovery. We used event-related potentials (ERPs) to adjudicate between these alternatives, emphasizing that an online recovery account would be supported if material-speci c indices of successful retrieval occurred no later than a material-independent index of recollection, the left-parietal ERP old/new e ect. A contrast between ERP correlates of successful memory retrieval for words and for faces revealed material-speci c neural activity that onset as early as the left-parietal old/new e ect. These ndings suggest that the material-speci c neural activity indexes the online recovery of encoded information. NeuroReport 19 :1463^1467 c 2008 Wolters Kluwer Health Lippincott Williams & Wilkins. Keywords: event-related potentials, material speci city, old/new e ects, recognition memory, recollection, retrieval Introduction A widely held view is that recovery of information from episodic memory involves recapitulation of activity in neocortical regions engaged during the encoding of that information [1 3]. Data from functional magnetic resonance imaging (fmri) studies support this account, because recovery of different kinds of information has been associated with distinct neural activity [4 6]. A critical interpretive limitation for the fmri findings, however, has been emphasized recently. Johnson et al. [7] noted that the sluggish nature of the haemodynamic response means that fmri data cannot separate interpretations casting distinct activations as either (i) processes engaged as a consequence of retrieval or (ii) processes that reflect directly the retrieval of different information. This separation can be achieved in studies using eventrelated potentials (ERPs), because (i) ERPs index neural activity in real time and (ii) ERPs acquired during retrieval provide a material-independent and content-independent index of recollection. This index is the left-parietal ERP old/new effect, comprising a greater relative positivity for old than for new items attracting correct memory judgments [8 13]. The effect is prominent from 500 to 800 ms poststimulus, and largest over left-parietal scalp. The link between this old/new effect and recollection is strong (e.g. [8,10]), and the critical predictions here are that materialspecific indices of retrieval, which are temporally coincident with the left-parietal effect are candidates for processes that reflect directly the retrieval of study information, whereas operations that are contingent upon successful retrieval would occur later than the parietal effect [7]. To investigate these possibilities, ERPs were acquired in a memory task, where stimuli were faces and words. To our knowledge, there are no published direct contrasts of ERP indices of successful retrieval for these stimulus types, but separate reports suggest that faces and words are associated with distinct patterns of memory-related neural activity in the same time period in which the left-parietal ERP old/new effect occurs [8,11 14]. A formal contrast between face and word memory effects thus offers a means of using the time course of ERP effects to distinguish between competing accounts of material-specific neural activity. Methods Thirty-five participants were Caucasian right-handed English speakers with normal or corrected-to-normal vision (18 25 years, five males). All were paid d7.50/h and gave informed consent. The experiment was approved by the Cardiff University Psychology Ethics Committee. Data from 11 participants (four males) were discarded because of insufficient trials in critical categories (see below). Stimuli were 200 faces and 200 words. Faces were an equal number of young-to-middle age Caucasian males and females. All were standardized black and white images ( pixels) with head and shoulder information and minimal background [face stimuli are available from Y.Y.Y. on request Words were concrete nouns (frequency range¼1 10/million), and were presented in black. All stimuli were shown on a white background on a monitor 1 m from the participants. Maximum visual angles c Wolters Kluwer Health Lippincott Williams & Wilkins Vol 19 No 15 8 October

2 YICK AND WILDING for words were 0.41 (vertical) and 2.21 (horizontal). Visual angles for faces were 3.71 and Ten study-test blocks were constructed. Half contained faces and the rest words. Study phases had 16 targets and 8 distracters. Test phases had the 16 studied targets and 16 new items. Study and test trials started with an asterisk shown centrally (1000 ms), followed by a blank screen (100 ms). Words and faces were then presented for 300 ms. Targets were presented centrally. Equal numbers of distracters (four per study block) were shown 5.21 of visual angle to left/right of fixation. All stimuli were followed by a blank screen lasting the participant response time and 1500 ms before the presentation of the asterisk signalling onset of the next trial. Study instructions were to respond with left/right index fingers to stimuli on the left/right of fixation, and with one thumb for those presented centrally. Test trials required an old/new judgment. The thumb used for the centre judgments, and hands used for the old/new judgments, were balanced across participants. Study-test blocks alternated between faces and words. Half of the participants started with faces. Item presentation order in study/test phases was determined randomly for each participant. Event-related potential recordings The electroencephalogram (EEG) was recorded from 25 silver/silver chloride electrodes in an elastic cap and from electrodes on the mastoids. Electrode sites included midline, left and right hemisphere locations (based on the 10/20 system [15]). Eye movements were recorded from above and below the right eye [vertical electrooculogram (EOG)] and the outer canthi (horizontal EOG). The influence of eye blinks was eliminated via a correction procedure based on a linear regression estimate. Before this, trials containing other EOG movement artefact were rejected, as were trials with A/D saturation or baseline drift (difference between first and last data point 4780 mv). EEG was recorded at 200 Hz referenced to Fz, and rereferenced off-line to the average signal at the mastoids into 1280 ms epochs, with a 100 ms prestimulus baseline against which all amplitude measures were taken. Data from Fz were reclaimed. EEG and EOG recording bandwidth was Hz ( 3 db down). Participants were excluded if contributing less than 16 trials to four categories: correct Faces responses to old and new faces and words. Averaged ERPs underwent a 7-point (21 Hz) binomially weighted smoothing filter before analysis. Results Behavioural data Mean probabilities of correct responses to old stimuli (hits) were 0.67 (faces) and 0.76 (words). Probabilities of incorrect responses to new items (false alarms) were 0.30 and Discrimination measures [P(hit) P(false alarm)] were above chance level (zero) for faces [t(23)¼12.24, Po0.001] and words [t(23)¼16.36, Po0.001]. Discrimination was superior for words [t(23)¼7.59, Po0.001]. A two-way analysis of variance (ANOVA) (factors of stimulus and old/new status) revealed only that reaction times were faster for words than faces [864 vs. 989 ms: F(1,23)¼8.20, Po0.001]. Event-related potential data Face and word old/new effects were first analysed separately to determine when reliable old/new effects were evident. Mean trial numbers per participant for hit and correct rejection ERPs for faces were 26 [standard deviation (SD)¼9] and 27 (SD¼11). For words, numbers were 31 (SD¼13) and 32 (SD¼14). Initial contrasts were conducted with Greenhouse Geisser corrected repeated measures ANOVAs. On the basis of earlier reports of ERP old/new effects for faces and words, analyses encompassed 16 electrodes at anterior and posterior sites (left anterior: FP1, F7, F5, F3; right anterior: FP2, F8, F6, F4; left posterior: O1, T5, P5, P3; right posterior: O2, T6, P6, P4). The analyses included factors of response category (two levels), anterior/ posterior dimension (two), hemisphere (two) and site (four). Figure 1 shows grand-averaged ERP old/new effects for faces and words. In line with earlier approaches (e.g. [8]), ERPs were analysed for three epochs ( , , ms) capturing the effects shown in Fig. 1. Outcomes of the separate ERP old/new effect analyses for faces and words are detailed in Table 1. The description of these outcomes below is restricted to reliable effects unmoderated by higher-order interactions. Face old/new effects Table 1 shows that positive-going ERP old/new effects for faces were reliable from 300 to 800 ms. See Fig. 2 for the Words F5 Fz F6 F5 Fz F6 C5 Cz C6 C5 Cz C6 P5 Pz P6 P5 Pz P ms ms ms ms ms ms + Hits Correct Rejections 10µV Fig. 1 Grand averaged event-related potentials elicited by hits and correct rejections for faces and for words. Data are shown for nine electrode locations at midline, left and right hemisphere sites over anterior (F5, Fz, F6), central (C5, Cz, C6) and posterior scalp (P5, Pz, P6) Vol 19 No 15 8 October 2008

3 MATERIAL-SPECIFIC ERP SIGNATURES Table 1 Outcomes of separate analyses of face and word event-related potential old/new e ects for the 300^500, 500^800 and 800^1100 ms epochs 300^500ms 500^800ms 800^1100ms Faces Words Faces Words Faces Words RC (1,23) 17.63*** 30.12*** 34.39*** 13.60*** 3.76 a 8.96** RC AP (1,23) RC HM (1,23) a 3.56 a 3.09 a 0.68 RC ST (3,69) 7.47** (0.61) 15.10*** (0.50) 15.40*** (0.63) 7.78** (0.49) 1.19 (2.11) 2.82* (0.73) RC AP HM (1,23) ** 3.26 a RC AP ST (3,69) 0.40 (0.63) 3.75* (0.71) 0.86 (0.64) 12.98*** (0.70) 0.81 (0.59) 11.97*** (0.73) RC HM ST (3,69) 0.36 (0.76) 1.52 (0.76) 1.11 (0.78) 0.06 (0.77) 1.65 (0.82) 0.49 (0.81) RC AP HM ST (3,69) 0.40 (0.75) 0.99 (0.93) 1.17 (0.71) 2.20 (0.92) 0.88 (0.66) 0.82 (0.95) AP, anterior/posterior; HM, hemisphere; RC, response category; ST, site. All main e ects and interactions involving RC are shown.full degrees of freedom are shown on the left. Epsilon values (the correction used in analyses when there is a violation of sphericity) are shown where appropriate in bold after each relevant interaction term. a Po0.1; ***Po0.001; **Po0.01; *Po ms ms Faces Words Fig. 2 Topographic maps showing the scalp distributions of the di erences between activities evoked by correctly recognized old items and correctly identi ed new items for faces and for words for 300^500 and 500^800 ms time windows. The front of the head is at the top of each map. Each dot denotes a recording electrode location. The mean voltage maxima and minima for each map can be understood via reference to the centrally located colour bar. distributions of these effects. The category site interactions in the and ms epochs reflect the fact that the old/new effects are largest at sites closest to the midline. The three-way interaction in the ms epoch reflects the left-sided posterior old/new effect alongside less lateralisation at anterior sites. Word old/new effects Positive-going word old/new effects were reliable from 300 to 1100 ms. Interactions between category, the anterior/ posterior dimension and site were reliable in each epoch. From 300 to 800 ms these reflect the superior and midlateral posterior maximum of the word old/new effects, although the effect is also somewhat larger at frontopolar than at occipital sites. The three-way interaction in the ms epoch reflects the anterior superior maximum of the effect. Contrasts between the scalp distributions of the face and word old/new effects The contrasts were conducted separately for the epochs ( and ms) where reliable old/new effects for faces and words were obtained. All location factors were as described above, and the contrasts were conducted on difference scores for faces and words obtained by subtracting mean amplitudes for ERPs associated with correct rejections from those associated with hits. These difference scores were also rescaled to remove overall amplitude differences between the face and word old/new effects. Rescaling ensures that reliable interactions involving scalp locations in the subsequent analysis suggest differences in the brain regions engaged in the two cases, rather than simply differences in the sizes of the face and word effects [16]. These ANOVAs also had a group factor (two levels), which was included in light of the superior discrimination for words. The similar group consisted of the 12 participants for whom old/new discrimination was most similar for faces and words. Discrimination scores were 0.43 (faces) and 0.54 (words) for this group. The dissimilar group contained participants for whom discrimination was most different. Their discrimination scores were 0.33 (faces) and 0.68 (words). Although discrimination was superior for words in both groups [similar: t(11)¼4.98, Po0.01; dissimilar: t(11)¼12.89, Po0.01], the discrimination advantage for words was greater in the dissimilar than in the similar group [0.35 vs. 0.11: t(22)¼6.85, Po0.01]. Assuming that neural activity which is sensitive to task difficulty changes with the degree of difficulty, then interactions involving group would suggest that relative difficulty contributes to differences between the face and word old/new effects (for conceptual points and the same logic applied to other ERP data, see ref. [17 19]). For the ms epoch, stimulus type (faces/words) interacted with the anterior/posterior dimension as well as with site [F(2.2, 49.9)¼3.26, Po0.05]. Figure 2 shows that the reason for this interaction is that the distribution of the face old/new effect extends more anteriorly than the word effect, particularly at sites closest to the midline. As stated above, reliable interactions between stimulus type and scalp location in analyses of rescaled data comprise evidence for differences in the brain regions engaged in the two cases [16]. Vol 19 No 15 8 October

4 YICK AND WILDING Critically, no reliable effects involving group were obtained in the analyses for either epoch, suggesting that differences in relative difficulty do not contribute to these outcomes. The possible influence of task difficulty was also tested in a second analysis, which was an assessment of whether the anterior element of the old/new effect for faces is related to the greater relative difficulty across participants of the face task. In this contrast, old/new discrimination scores for faces for each participant were correlated with the average magnitude of face ERP old/new effects at sites F3, Fz and F4. These are the sites at which the differences between the old/new effects for words and faces are prominent. A negative correlation between discrimination accuracy and the magnitude of the face old/new effect at these locations would implicate difficulty in the differences across stimulus type. This view is based on the assumption that, as difficulty increases (as indexed by lower discrimination scores), the degree to which difficulty-sensitive neural processes are engaged also increases. No support for a difficulty account was observed, as a weak positive and nonsignificant correlation was obtained (r¼0.23, P¼0.28). Discussion ERP indices of successful retrieval for faces and words differed reliably from ms. The effects extended over frontal and frontocentral scalp to a greater degree for faces than for words. These findings indicate that not entirely the same brain regions were associated with memory for faces and words, and suggest that ERPs index material-specific retrieval processing. The findings complement earlier reports of content-independent ERP memory indices, where old/new effects varied according to the kinds of encoding to which words were subjected [7]. The strong similarities between the left parietal maxima of the face and word old/new effects in the ms epoch (Fig. 2) suggest a common left posterior old/new effect for faces and words. This view is also supported by the morphological and temporal similarities between the effects here and those in other studies [8,10]. If this account is correct, then the differences between the face and word old/ new effects arise because the parietal old/new effect for faces overlaps in time with a second effect that has a more anterior distribution (for similar face effects, see ref. [11 13]). Figure 2 suggests that this anterior effect onsets in the ms epoch, and statistical support for this claim comprises two outcomes. First, analyses of the face old/ new effect in the ms epoch did not indicate that the effect was larger at either posterior or anterior locations (Table 1). Second, analyses of the word old/new effect revealed an interaction including the anterior/posterior dimension, because word old/new effects were largest at superior and midlateral posterior sites. This anteriorly distributed face effect can be interpreted as evidence for material-specific retrieval processes. The claim requires scrutiny, however, because response accuracy was superior for words. Thus, differences ascribed to material type might reduce to the greater relative difficulty of the face task. Two tests of this possibility were conducted. First, for the direct face/word contrasts, participants were split into groups according to the degree to which the face memory task was more difficult than the word task. No reliable effects involving group were observed. Second, the size of the face-specific frontal element of the old/new effect was correlated with memory accuracy for faces. No reliable correlation was obtained. These outcomes at group and individual levels suggest that differences between the face and word ERP old/new effects are not because of the greater relative difficulty of the face task. The absence of evidence for a difficulty account is also consistent with earlier indications that distributions of ERP old/new effects do not vary with differences in response accuracy (e.g. [18,20]). The common posterior positivity shared by the face and word old/new effects has been identified as a generic signature of recollection [8,21] and it has been argued that content-specific as well as material-specific effects sharing the time course of this generic effect reflect processes involved in the online recollection of different material [7]. According to this account, the material-specific anteriorly distributed old/new effect in the ms epoch indexes processes involved in the online recovery of specific contents. An alternative, however, is that the anteriorly distributed effect indexes material-specific processes operating on the products of retrieval. By this view, the posterior and anterior elements of the effects from 500 to 800 ms are linked via an iterative relationship: post-retrieval processing operations indexed by the anterior element come online as recovered information (indexed by the posterior element) becomes available (for similar arguments, see ref. [8]). At least two challenges to this account exist. First, Fig. 2 suggests that the anterior modulation specific to faces onsets before 500 ms, and as noted above there is statistical support for this claim. Second, material-specific old/new effects were restricted to the time period when the generic ERP index of recollection is evident; there were no reliable face old/new effects after 800 ms. Although processes operating on the products of retrieval may work iteratively with material-independent processes, it is reasonable to assume that the time course of the former should extend beyond that of the latter. In light of this, the data presented here implicate the material-specific anterior old/new effect with processes that reflect direct recovery of information that is associated with faces to a greater degree than with words. This does not imply, however, that the anterior effect is specific to faces. One possibility is that it indexes recovery of configural or spatial information that is a feature of faces but also of stimuli such as scenes and objects. It will be important subsequently to delineate the functional significance of the anterior old/new effect described here by investigating how it changes with manipulations of material type. Another manipulation will be an explicit measure of recollection rather than the recognition memory judgments required here. Conclusion These ERP data suggest strongly that material-specific correlates of successful retrieval index processes that form part of the online representation of information as it is recovered from long-term memory. References 1. Mesulam MM. From sensation to cognition. Brain 1998; 121: Damasio AR. The brain binds entities and events by multiregional activation from convergence zones. Neural Comput 1989; 1: Vol 19 No 15 8 October 2008

5 MATERIAL-SPECIFIC ERP SIGNATURES 3. Allan K, Robb WGK, Rugg MD. The effect of encoding manipulations on neural correlates of episodic retrieval. Neuropsychologia 2000; 38: Woodruff CC, Johnson JD, Uncapher MR, Rugg MD. Content-specificity of the neural correlates of recollection. Neuropsychologia 2005; 43: Johnson JD, Rugg MD. Recollection and the reinstatement of encodingrelated cortical activity. Cereb Cortex 2007; 17: Wheeler ME, Petersen SE, Buckner RL. Memory s echo: vivid remembering reactivates sensory-specific cortex. Proc Natl Acad Sci USA 2000; 97: Johnson JD, Minton BR, Rugg MD. Content dependence of the electrophysiological correlates of recollection. Neuroimage 2008; 39: Wilding EL, Rugg MD. An event-related potential study of recognition memory with and without retrieval of source. Brain 1996; 119: Curran T. Brain potentials of recollection and familiarity. Mem Cognit 2000; 28: Vilberg KL, Rugg MD. Dissociation of the neural correlates of recognition memory according to familiarity, recollection, and amount of recollected information. Neuropsychologia 2007; 45: Yovel G, Paller KA. The neural basis of the butcher-on-the-bus phenomenon: when a face seems familiar but is not remembered. Neuroimage 2004; 21: Curran T, Hancock J. The FN400 indexes familiarity-based recognition of faces. Neuroimage 2007; 36: MacKenzie G, Donaldson D. Dissociating recollection from familiarity: electrophysiological evidence that familiarity for faces is associated with a posterior old/new effect. Neuroimage 2007; 36: Paller KA, Kutas M. Brain potentials during memory retrieval provide neurophysiological support for the distinction between conscious recollection and priming. J Cogn Neurosci 1992; 4: Jasper HA. The ten twenty system of the international federation. Electroencephalogr Clin Neurophysiol 1958; 10: McCarthy G, Wood CC. Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. Electroencephalogr Clin Neurophysiol 1985; 62: Rugg MD, Allan K, Birch CS. Electrophysiological evidence for the modulation of retrieval orientation by depth of study processing. J Cogn Neurosci 2000; 12: Rugg MD, Wilding EL. Retrieval processing and episodic memory. Trends Cogn Sci 2000; 4: Dzulkifli MA, Sharpe HL, Wilding EL. Separating item-related electrophysiological indices of retrieval effort and retrieval orientation. Brain Cogn 2004; 55: Wilding EL, Rugg MD. An event-related potential study of memory words spoken aloud or heard. Neuropsychologia 1997; 35: Friedman D, Johnson R. Event-related potential (ERP) studies of memory encoding and retrieval: a selective review. Microsc Res Tech 2000; 51:6 28. Vol 19 No 15 8 October

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