The influence of directed attention at encoding on source memory retrieval in the young and old: An ERP study

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1 brain research 1500 (2013) Available online at Research Report The influence of directed attention at encoding on source memory retrieval in the young and old: An ERP study Michael R. Dulas n, Audrey Duarte School of Psychology, Georgia Institute of Technology, 654 Cherry Street, Atlanta, GA , USA article info abstract Article history: Accepted 11 January 2013 Available online 21 January 2013 Keywords: Aging Monitoring Source memory ERP Retrieval Neuroimaging evidence suggests that older adults exhibit deficits in frontally-mediated strategic retrieval processes, such as post-retrieval monitoring. Behavioral research suggests that explicitly directing attention toward source features during encoding may improve source memory for both young and older adults and alleviate age-related source memory impairments, in part, by reducing demands on post-retrieval monitoring. We investigated this hypothesis in the present event-related potential (ERP) study. Young and older adults attended to either objects and their presented color (source) or to the object alone during study and made color source memory decisions at test. We attempted to match performance between groups by halving the memory load for older adults. Behavioral results showed that, while direction of attention to object and color improved source memory for both groups, older adults benefited less than the young. ERPs revealed that demands on late right frontal effects, indicative of post-retrieval monitoring, were similarly reduced by directed attention at encoding for both groups. However, older adults showed reduced ERP correlates of recollection (parietal old new effect), as well as a sustained widespread negativity, potentially indicative of memory searches for perceptual details in the face of impaired recollection. These results suggest that older adults, like the young, can engage in post-retrieval monitoring when source details are difficult to recover. However, impaired recollection may underlie persistent age-related source memory deficits, even when encoding is supported via directed attention. & 2013 Elsevier B.V. All rights reserved. 1. Introduction A great deal of evidence suggests that healthy aging, even in the absence of neurodegenerative pathology, is associated with disproportionate declines in source memory (i.e. memory for experimentally manipulated episodic features) relative to item memory (see Mitchell and Johnson, 2009; Spencer and Raz, 1995 for reviews). It has been proposed that source memory judgments may rely on executive processes to a greater extent than item memory judgments. These processes may include elaboration and organization of episodic information during initial encoding, as well as monitoring and evaluation processes during attempts to retrieve sourcespecifying information at test (see Blumenfeld and Ranganath, 2007; Mitchell and Johnson, 2009 for reviews). Evidence suggests that these and other executive processes may be particularly disrupted by normal aging (Hasher and Zacks, 1979; Johnson et al., 1993). It is possible that memory n Corresponding author. Fax: þ addresses: mrdulas@gatech.edu (M.R. Dulas), audrey.duarte@psych.gatech.edu (A. Duarte) /$ - see front matter & 2013 Elsevier B.V. All rights reserved.

2 56 brain research 1500 (2013) tasks placing high demands on these processes may result in substantial age-group differences. Thus, age-related deficits in performance may be particularly evident on a source memory task, where experimentally-manipulated source details must be integrated during encoding and subsequently retrieved in the face of competing alternatives. An interesting question that has not been fully addressed is whether there are conditions under which age-related impairments in source memory accuracy may be reduced. Behavioral evidence from the attention literature suggests that attention impacts both the strength and content of memory (Chun and Turk-Browne, 2007). Consistent with the attentional account, behavioral evidence shows that both young and older adults source memory accuracy improves if participants are directed to specifically attend to the relationship between an item and its experimentallymanipulated source association during study (e.g. How well does this chair (item) fit the room (source)? ) (Glisky et al., 2001; Glisky and Kong, 2008; Hashtroudi et al., 1994; Naveh- Benjamin et al., 2007). This manipulation can sometimes even restore older adults performance to the level of the young (e.g. Glisky et al., 2001). These findings suggest that directing attention toward associations between items and source features facilitates source memory accuracy for these attended features in both young and older adults. However, the mechanisms supporting this effect are not entirely clear. One possibility is that directed attention may improve source memory accuracy, in part, by affecting processing at retrieval. Specifically, it has been suggested that post-retrieval monitoring demands increase as memories become impoverished with respect to the retrieval decision (e.g. Did I see this chair presented in this room or the other? ) (Henson et al., 2000). It follows that, if directed attention during encoding increases the strength of item source associations, the demands on strategic retrieval processes like monitoring may be reduced. Given that impaired or inefficient strategic retrieval processes contribute to older adults source memory impairments (Cohn et al., 2008; Naveh-Benjamin et al., 2009), age-related deficits in source memory accuracy may be attenuated if post-retrieval monitoring demands are reduced. Event-related potentials (ERPs) may be useful for investigating the time course of neural activity and demands on retrieval and post-retrieval processes contributing to the recovery of item source associations. Several ERP old new effects have been identified in recognition memory studies, including source recognition studies. Typically, more positivegoing deflections in the waveforms are observed for recognized studied items (i.e. hits) compared to correctly rejected new items. An early frontal-maximal negative-going old new effect, occurring between 300 and 500 ms, the FN400, has often been linked to familiarity-based processes (Curran, 2000; Duarte et al., 2006; see Friedman and Johnson, 2000; Rugg and Curran, 2007 for reviews; Wolk et al., 2009). A later occurring ( ms) parietal-maximal parietal old new effect is thought to be indicative of recollection (see Friedman and Johnson, 2000; Johnson, 1995; Rugg, 1995 for reviews) as it is largest for items that elicit correct source (Ranganath and Paller, 2000; Trott et al., 1997; Wilding and Rugg, 1996, 1997) or remember judgments (Duarte et al., 2004; Duzel et al., 1997; Smith, 1993; Trott et al., 1999). Finally, a late-onsetting (700 ms), often right-lateralized ERP that is typically sustained for several hundred milliseconds, the late frontal old new effect, is observed when participants must evaluate retrieved episodic information, as in a source memory test. This effect is often largest for unsuccessful source trials and more prominent when source details are difficult to recover. Further, given the time course of this ERP effect, it has been posited as an index of post-retrieval monitoring (Cruse and Wilding, 2009; Friedman and Johnson, 2000; Kuo and Van Petten, 2006, 2008; Senkfor and Van Petten, 1998; Wilding and Rugg, 1996). Although the neural generators of the right frontal old new effect have not been established, fmri evidence suggests post-retrieval monitoring may be mediated, at least in part, by the right dorsolateral prefrontal cortex (DLPFC) (Henson et al., 1999; Rugg et al., 2003). Although there are discrepancies across previous studies with regard to the effects of aging on specific ERP old new effects, evidence suggests that age-related attenuations and onset delays are often observed during source retrieval (Duarte et al., 2006; Dulas et al., 2011; Mark and Rugg, 1998; Swick et al., 2006; Trott et al., 1997, 1999; Wegesin et al., 2002). Of primary interest for the current study, the late-frontal old new effect is often attenuated during source retrieval in older adults, even when earlier old new effects (i.e. FN400, parietal old new) are robust (see Friedman, 2000 for review; Gutchess et al., 2007; Trott et al., 1997; Wegesin et al., 2002). Thus, even when recollection and familiarity processes appear to be intact, memory impairments may be explained by dysfunction in post-retrieval monitoring processes. This prediction is consistent with the idea that age-related difficulties in engaging post-retrieval monitoring operations likely contribute to older adults source memory impairments (Cohn et al., 2008; Naveh-Benjamin et al., 2009). fmri evidence has also suggested older adults show dysfunction in executive processes mediated by the DLPFC during shortterm memory tasks (Mitchell et al., 2006), episodic encoding (Grady et al., 1999), and contextual memory retrieval (McDonough et al., 2012; see Rajah and D Esposito, 2005 for review; Rajah et al., 2009). Pertinent to the current study are findings from an interesting ERP study in young adults (Kuo and Van Petten, 2006). In this study, participants received encoding instructions that explicitly directed attention toward the conjunction of items and their source features (i.e. Is this a plausible color for the object? ). This direction of attention improved source memory accuracy for color and attenuated late-frontal old new ERP effects at test, as compared to instructions that were object oriented only (size judgment). Moreover, no similar alterations were observed for earlier onsetting ERP effects, such as the FN400 and parietal old new effects. This suggests the amount of information retrieved may be similar between conditions, though participants may recollect more noncriterial details for the object-oriented condition (Yonelinas and Jacoby, 1996). These results suggest that when an item and its associated contextual details are more tightly bound during encoding via directed attention, successful recovery of source may occur without the need of post-retrieval monitoring. As discussed earlier, this type of supportive encoding has been shown to reduce age-related deficits in source memory

3 brain research 1500 (2013) accuracy (Glisky et al., 2001; Glisky and Kong, 2008; Hashtroudi et al., 1994; Naveh-Benjamin et al., 2007). No studies, to our knowledge, have assessed the effects of aging on post-retrieval monitoring activity when attentional demands at encoding are manipulated. If post-retrieval monitoring demands are reduced when sought-after source details are strongly bound to items, and older adults are less able or unable to recruit these strategic retrieval mechanisms (Gutchess et al., 2007; Trott et al., 1997; Wegesin et al., 2002), age-related differences in the late frontal old new ERPs may be minimal after directed attention. The present study sought to investigate the effect of directed attention toward item feature conjunctions on source memory accuracy, as well as its effect on age-related changes in source memory accuracy and related ERPs. During study, participants viewed pictures of colored objects presented either in an encoding condition which specifically required the participant to attend to the conjunction of each object and its color (object color), or in an encoding task that directed attention toward the object with no explicit direction regarding the color (object-only). During test, participants first judged whether they had previously studied the object, regardless of its color. Then they decided if items endorsed as old were presented in the same color in which they were presented during encoding. Importantly, a response option was included that allowed participants to indicate that they did not know which color was associated with the recognized object, as has been implemented in prior studies (Duarte et al., 2008, 2009, 2011; Dulas and Duarte, 2011a, 2011b; Gottlieb et al., 2010; Morcom et al., 2007; Smith et al., 2004). This procedure minimizes the possible dilution by guesses on estimates of source memory accuracy and associated neural activity. Furthermore, the memory load was halved for older adults in an attempt to more closely equate levels of performance between age groups. It has been suggested that large group differences in performance may compromise the interpretation of age-related differences in neural activity, such that performance differences are confounded with differences related to aging, per se (reviewed in Rugg and Morcom, 2005). We predicted that source memory accuracy would be greater following directed attention toward object color conjunctions (object color trials) for both young and older adults. Consistent with previous findings (Kuo and Van Petten, 2006), we predicted that, while there would be no differences between conditions in early ERP effects (FN400, parietal old new), late frontal old new ERP effects would be reduced for retrieval of object color compared to object-only trials in the young. If, as suggested by some previous behavioral (Cohn et al., 2008; Naveh-Benjamin et al., 2007) and ERP studies (see Friedman, 2000 for review; Gutchess et al., 2007; Trott et al., 1997; Wegesin et al., 2002) older adults are less able or unable to recruit post-retrieval monitoring mechanisms, older adults may show attenuated late-frontal old new effects in general compared to the young. However, if older adults are able to recruit these mechanisms when required by the demands of the task and when performance is similar between age groups (Li et al., 2004), we predict that older adults, like the young, will show reduced post-retrieval monitoring effects for object color compared to object-only Table 1 Group characteristics. Measure Young (n¼18) Old (n¼18) Age (4.66) (4.61) Gender 10/18 female 8/18 female Education (2.49) (2.42) Letter fluency (14.73) (18.79) List recall (immediate) (1.13) (1.45) List recall (immediate, cued) (1.03) (1.46) List recall (delayed) (0.70) (1.16) List recall (delayed, cued) (0.85) (1.29) List recognition (0.32) (0.24) MAS digit span forward 6.94 (1.16) 6.89 (1.37) MAS digit span backward 5.50 (1.20) 4.72 (1.18) Trails A (in seconds) (6.37) (9.20) Trails B (in seconds) (9.07) (15.79) Visual recognition (1.28) (1.92) Delayed visual recognition (0.79) (2.09) Visual reproduction 9.33 (1.19) 5.56 (2.53) WCST (# of errors) (5.78) (8.78) Note: Standard deviations in parentheses. All neuropsychological test scores are reported as raw scores. n Marginally different from Young (po0.1). nn Significantly different from Young (po0.05). trials. Regardless, we predict age-related differences in late frontal old new ERPs should be minimal for object color compared to object-only trials. 2. Results 2.1. Neuropsychological assessment results Group characteristics and results for neuropsychological tests are shown in Table 1. All participants scored within 1 standard deviation of age-adjusted normative averages for all neuropsychological tests. Older adults exhibited significantly poorer performance than young adults on several tests including Trails A and B, Visual Recognition, Delayed Visual Recognition, and Visual Reproduction [t(34) s43.59, p so0.002] and marginally poorer on Wisconsin Card Sorting and Verbal Span Backwards [t(34) s41.96, p so0.06]. There were no other significant group differences [t(34) so1.41, p s40.17] Behavioral results The mean proportions of correct, incorrect and don t know source judgments and new responses made to studied items (misses) are presented in Table 2, along with the proportions of correctly rejected (CR) new items. Item recognition accuracy was estimated by the Pr measure of discriminability (Snodgrass and Corwin, 1988), i.e. p(hits) p(false alarms) for object color and object-only encoding conditions. Source accuracy was also estimated by Pr, excluding don t knows, i.e. Pr¼p(correct) p(incorrect). 1 These item and 1 Analyses, were also conducted when source accuracy was estimated by Psr, derived from a single high threshold model (Snodgrass and Corwin, 1988), as used in previous source

4 58 brain research 1500 (2013) Table 2 Response proportions, performances indices, and response times to studied and unstudied items at test. Young adults Older adults Object color Object-only Object color Object-only Response proportions Studied objects Correct 0.73 (0.12) 0.51 (0.11) 0.65 (0.10) 0.50 (0.12) Incorrect 0.12 (0.07) 0.26 (0.07) 0.19 (0.07) 0.26 (0.07) Don t know 0.05 (0.04) 0.12 (0.11) 0.03 (0.04) 0.07 (0.09) Miss 0.10 (0.07) 0.11 (0.08) 0.13 (0.08) 0.17 (0.11) Unstudied objects Correct rejections (CR) 0.91 (0.10) 0.92 (0.05) Performance Indices Item recognition (Pr-item) 0.81 (0.13) 0.81 (0.14) 0.79 (0.10) 0.74 (0.12) Corrected source (Pr-source) 0.68 (0.23) 0.30 (0.18) 0.54 (0.17) 0.31 (0.17) Response times Studied objects Correct 1243 (135) 1235 (155) 1548 (218) 1542 (215) Incorrect 1315 (189) 1246 (162) 1576 (222) 1596 (248) Don t know 1491 (401) 1374 (209) 1806 (497) 1779 (468) Miss 1789 (488) 1726 (339) 2035 (286) 1933 (380) Unstudied objects Correct rejections (CR) 1369 (196) 1624 (288) Note: Standard deviations in parentheses. For Performance Indices, Chance¼0. source accuracy estimates for young and older adults are shown in Table 2. To assess the effects of explicit direction of attention at encoding on item memory and source memory accuracy, we conducted a Memory (Item, Source) Encoding Condition (object color, object-only) Group (Young, Old) ANOVA on the Pr measures. The ANOVA revealed significant main effects of Memory [F(1,34)¼207.1, po0.001], Condition [F(1,34)¼189.9, po0.001], as well as significant interactions of Memory Condition [F(1,34)¼107.8, po0.001], Condition Group [F(1,34)¼5.76, p¼0.02] and Memory Condition Group [F(1,34)¼13.57, p¼0.001]. Separate subsidiary ANOVAs for item and source memory estimates revealed reliable main effects of Condition [F(1,34) s411.50, p so0.002], both of which were modified by interactions with Group [F(1, 34) s47.69, p so0.01]. For item memory, follow-up contrasts suggest that the interaction reflected greater item memory estimates for object color than object-only trials in older adults [t(17)¼3.93, p¼0.001] but not young adults [t(17)o1]. However, there were no significant group differences for item memory estimates within either Condition [t(34) so1]. Subsidiary analyses for source memory revealed that both groups benefitted from explicit direction of attention to object color conjunctions at encoding [t(17) s47.13, p so0.001]. Young adults source memory estimates were greater than those of the old for the object color [t(34)¼2.82, p¼0.01] but not the (footnote continued) memory studies (e.g. Dulas and Duarte, 2011a; Duverne et al., 2008). Psr¼(p(correct) 0.5(1 p(don t know)))/(1 (0.5(1 p(don t know)))). Analyses using Psr showed the exact same pattern of results as Pr. Psr provides an index of a participant s accuracy for choosing the source when the contribution of lucky guessing is removed, while Pr provides an estimate of accuracy for source out of all source attempts. object-only condition [to1]. Thus, as can be seen in Table 2, our performance matching manipulation successfully matched the groups for item memory performance for both conditions, as well as for source memory performance for the object-only condition. Although both groups received a source memory benefit from the directed attention manipulation, older adults did not receive the same magnitude of benefit as young adults. Mean reaction times (RTs) for memory judgments are shown in Table 2. For consistency with the ERP analyses (i.e. comparison of source correct and correct rejections), these RTs were subjected to a Response (object color source correct, object-only source correct, CR) Group (young, old) ANOVA, revealing main effects of Response [F(2,68)¼13.66, po0.001], and Group [F(1,34)¼20.62, po0.001], with no significant interaction between these factors [Fo1]. As shown in the table, the main effect of Group indicates that young adults were faster to respond to test items than older participants while the effect of Response reflects the fact that RTs were faster for correct source responses than CR judgments [t(17) s42.14, p so0.05]. Correct source RTs did not differ between object color and object-only correct source judgments for either group [t(17) so1] ERP results ERPs to objects studied in the object color and object-only encoding conditions and associated with correct source judgments and ERPs for correctly rejected new objects are shown for selected electrode sites for the young in Fig. 2 and the older adults in Fig. 3. For both groups, old new effects similar to those reported in previous studies (see Section 1) were observed with correct source ERPs for each condition eliciting more positive-going activity than correct rejection

5 brain research 1500 (2013) Fig. 1 Experimental design. Example trials from both study (left) and test (right). ERPs beginning at roughly 300 ms post-stimulus onset. Visual inspection of the waveforms revealed that older adults showed a sustained negative-going effect beginning 500 ms, similar to the pattern seen in Li et al. (2004). Li and colleagues suggested that the negativity obscured early old new effects (i.e. FN400, parietal old new) potentially confounding the interpretation of age group differences for these effects. To address this potential issue, we applied a polynomial detrend (1st order) temporal filter to remove the sustained components from the ERPs for both age groups. Results for the early time windows ( , ms) are reported for this detrended data, while results for the late time windows ( , ms) are reported for the non-detrended data, as the detrending attenuates all sustained components, including the late frontal old new effects of interest in this study. Results for ANOVAs for each time window [see Section 4.6] are shown for young adults in Table 3 and for older adults in Table Old new effects: magnitude and topographical analyses ms. Young adults: The ANOVAs for the ms time window revealed significant object color and object-only old new effects. Follow-up analyses for the object color condition revealed reliable old new effects at the frontal chain and at parietal and parietal occipital electrode locations. Follow-up analyses for the object-only condition showed these effects were reliable at all electrodes except lateral parietal and occipital electrodes. As can be seen in Fig. 4, these results were indicative of widespread frontocentral maximal old new effects for both conditions. No differences between object color and object-only trials were observed. In order to determine if there were any topographical differences between object color and object-only old new effects, the vector-length rescaled difference scores [see Section 4.6] were subjected to an Encoding Condition (object color, object-only) Chain Location Hemisphere ANOVA. Results showed no reliable effects involving the factor of Condition [F so1.8, p s40.16], reflecting that object color and object-only old new effects had similar topographies, as can be seen in Fig. 4. Older adults: The ANOVAs for this time window revealed that object color old new effects were reliable at frontal sites only. The ANOVA comparing object-only and CR trials showed that this old new effect was not reliable at either chain. The comparison of object-only and object color trials showed that object color ERPs were greater than object-only ERPs in the right hemisphere [F(1,17)¼5.17, p¼0.04], but not the left [F so1.9, p s40.16], as can be seen in Fig. 5. As there were no reliable object-only old new effects, vectorlength rescaled analyses were not performed. Between groups analyses: For time windows where young and older adults both showed significant effects, the raw difference scores for each encoding condition were compared in order to assess age group differences in the magnitude of old new effect. Further, the vector-length rescaled difference scores were also compared in order to assess age group differences in topography and possible neural generators.

6 60 brain research 1500 (2013) Fig. 2 Young participants. Grand average ERPs for objects recognized and associated with source correct (SC) judgments for object color and object-only encoding conditions and unstudied objects correctly rejected as new. ERPs are presented for six of the ten electrode locations analyzed. Left and right columns correspond to left and right scalp locations, respectively. On the scalp map, circles represent electrode locations as viewed from above; filled circles represent plotted electrodes. Fig. 3 Older participants. Grand average ERPs for objects recognized and associated with source correct (SC) judgments for object color and object-only encoding conditions and unstudied objects correctly rejected as new. ERPs are presented for six of the ten electrode locations analyzed. Left and right columns correspond to left and right scalp locations, respectively. On the scalp map, circles represent electrode locations as viewed from above; filled circles represent plotted electrodes.

7 brain research 1500 (2013) Table 3 ANOVA results for each ERP time window for young adults ms ms ms ms Omnibus C (2,34) 4.89, p¼ , p¼ , p¼0.03 C CH (2,34) 10.04, po0.001 C H (2,34) 5.80, p¼ , p¼0.01 C L (8,136) C CH H (2,34) C CH L (8,136) 2.75, p¼ , po0.001 C H L (8,136) 4-way (8,136) Obj-col SC vs. CR C (1,17) 4.84, p¼ , p¼ , p¼0.08 C CH (1,17) 16.79, p¼0.001 C H (1,17) 8.14, p¼ , p¼0.01 C L (4,68) 2.04, p¼0.01 C CH H (1,17) 6.46, p¼0.02 C CH L (4,68) 3.29, p¼0.03 C H L (4,68) 4-way (4,68) Obj-only SC vs. CR C (1,17) 13.68, p¼ , po , p¼ , p¼0.05 C CH (1,17) 12.46, p¼0.003 C H (1,17) 5.31, p¼ , p¼0.01 C L (4,68) C CH H (1,17) C CH L (4,68) 3.44, p¼ , p¼0.003 C H L (4,68) 4-way (4,68) Obj-col SC vs. Obj-only SC C (1,17) C CH (1,17) 6.97, p¼0.02 C H (1,17) C L (4,68) C CH H (1,17) C CH L (4,68) C H L (4,68) 4-way (4,68) Note: C¼condition (old new, or obj-color vs. obj-only); CH¼chain (frontal, posterior); H¼hemisphere (left, right); L¼electrode location. ¼No significant effect (a40.05) In this time window, older adults showed reliable effects for the object color condition only. The raw difference score ANOVA comparing the age groups for this condition showed marginal Chain Group interaction [F(1,34)¼3.26, p¼0.08]. However, follow-up analyses showed these differences were not reliable at either chain. The vector-length rescaled ANOVA for the object color condition showed a significant Chain Group interaction [F(1,34)¼4.26, p¼0.047], reflecting that young adults showed effects that extended more posteriorly than older adults. Summary: Both young and older adults showed reliable object color old new effects at frontocentral electrodes, though these effects were more widespread for young adults. Only young adults showed evidence of object-only old new effects ms. Young adults: The ANOVAs for the ms time window revealed that object color and object-only old new effects were reliable at all posterior electrodes and left frontocentral channels. The betweenencoding condition ANOVA revealed no significant effects involving Encoding Condition. ANOVAs of the vector-length rescaled difference scores showed no significant differences between conditions [F so1.8, p s40.19], suggesting the two conditions had similar topographies. Older adults: The ANOVAs for this time window showed that object color old new effects were reliable at all electrodes except for the right parietal electrode location, and objectonly effects were reliable at right anterior frontal, frontocentral and posterior scalp sites. There was no reliable difference in magnitude between object-only and object color trials. Vector-length rescaled analyses revealed no significant effects involving condition [F so1.8, p s40.15], suggesting the effects for these two old new effects were not topographically distinct in this time window. Between group analyses: The raw difference wave ANOVAs for object color and object-only old new effects revealed

8 62 brain research 1500 (2013) Table 4 ANOVA results for each ERP time window for older adults ms ms ms ms Omnibus C (2,34) 6.35, p¼ , p¼0.04 C CH (2,34) 4.62, p¼0.03 C H (2,34) C L (8,136) C CH H (2,34) C CH L (8,136) 2.54, p¼0.01 C H L (8,136) 4.20, p¼ way (8,136) 1.94, p¼0.08 Obj-col SC vs. CR C (1,17) 5.20, p¼ , p¼ , p¼0.06 C CH (1,17) 6.73, p¼ , p¼0.06 C H (1,17) 3.17, p¼0.09 C L (4,68) C CH H (1,17) C CH L (4,68) 3.80, p¼0.01 C H L (4,68) 8.24, p¼ way (4,68) 2.40, p¼0.06 Obj-only SC vs. CR C (1,17) 4.59, p¼0.047 C CH (1,17) 4.60, p¼0.047 C H (1,17) 3.23, p¼0.09 C L (4,68) C CH H (1,17) 4.54, p¼0.048 C CH L (4,68) 2.76, p¼0.04 C H L (4,68) 4-way (4,68) 2.95, p¼0.04 Obj-col SC vs. Obj-only SC C (1,17) 6.21, p¼0.02 C CH (1,17) C H (1,17) 4.16, p¼0.06 C L (4,68) C CH H (1,17) 3.12, p¼0.09 C CH L (4,68) C H L (4,68) 2.30, p¼ way (4,68) Note: C¼condition (old new, or obj-color vs. obj-only); CH¼chain (frontal, posterior); H¼hemisphere (left, right); L¼electrode location. ¼No significant effect (a40.05). significant Chain Group [F(1,34) s49.22, p so0.01] and Hemisphere Group [F(1,34) s43.33, p so0.08] interactions. Follow-up analyses revealed reliable differences in the posterior chain, particularly on the left. The vector-length rescaled ANOVAs also showed Chain Group [F(1,34) s43.75, p so0.06] and Chain Hemisphere Group interactions [F(1,34) so3.33, p s40.08]. As can be seen in Figs. 4 and 5, these results reflect the stronger, bilateral parietal old new effects seen in young adults for both conditions, as well as the older adults showing more right frontal distribution of the effects. Summary: Both groups showed evidence of parietal old new effects in this time window. In the young, these effects were mostly confined to parietal electrodes for both conditions. Older adults showed overall weaker parietal old new effects compared to the young, but showed effects that spread into right frontal electrodes ms. Young adults: The ANOVAs for this time window revealed that object color old new effects were reliable at frontocentral and parietal locations. Object-only old new effects showed a widespread topography. The between-encoding condition ANOVA revealed no significant differences between the object color and object-only trials. Vector-length rescaled analyses revealed no reliable differences [F so2.9, p s40.10]. Older adults: The omnibus ANOVA for this time window revealed no significant effects involving Condition. Between groups analyses: As there were no significant old new effects in the older adults, no between groups analyses were performed. Summary: Frontocentral maximal old new effects were reliable for both conditions in the young only. No effects were reliable for older adults in this time window ms. Young adults: Analyses in this time window showed object color old new effects were not reliable at any location. Object-only old new effects were reliable in the right frontal chain. The between encoding condition

9 brain research 1500 (2013) Fig. 4 Young participants. Scalp topography of old new effects within each window (source correct correctly rejected new) for object color and object-only encoding conditions. Exemplar electrodes are presented next to each corresponding scalp topography. Time windows and ms depict polynomial detrended data, while and ms depict non-detrended data. n.s. ¼not significant. ANOVA revealed that object-only trials were greater in magnitude than the object color trials at frontal locations. As there were no reliable object color old new effects, vector-length rescaled analyses were not performed. Older adults: For this time window, the object color old new ANOVA revealed new4old effects that were significant bilaterally in the frontal chain and at the left-lateralized central parietal electrode location. For the object-only old new effects, analyses showed reliable new4old effects at the left-lateralized frontocentral electrode location. The between-encoding condition ANOVA showed object-only old new effects were significantly greater (less negative) than object color at right frontal electrodes, and marginally so at all left-lateralized electrode locations for both the frontal and posterior chains. Vector-length rescaled analyses revealed no significant effects [F so1.9, p s40.15]. Between groups analyses: As can be seen in Figs. 4 and 5, old new effects were markedly different between age groups, with negative-going effects in the old only. However, the difference between object-only and object color trials was similar for young and older adults (object-only4object color). Given our particular interest in late frontal effects and the influence of directed attention at encoding on these effects, we compared difference scores between object-only and object color trials between groups. The ANOVA comparing these difference scores showed no significant effects involving Group [F so1.9, p s40.17]. As can be seen in Fig. 6, both young and older adults showed greater activity for objectonly than object color trials at right frontal channels. Summary: Right frontal old new effects were observed for the object-only condition only in the young. By contrast, older adults showed a widespread negativity across the scalp that was more pronounced for the object color condition. However, comparing object-only to object color ERPs suggested that older adults may show evidence of right frontal old new effects, just these may be swamped by the late negativity. 3. Discussion In the current study we investigated the effect of directed attention toward object source feature associations during encoding on age-related impairments in source memory, as well as age group differences in ERP correlates of postretrieval monitoring. Consistent with our predictions, directed attention improved source memory accuracy in both young and older adults. Interestingly however, older adults did not receive the same level of source memory benefit from this manipulation as did the young. ERP results showed that directed attention resulted in attenuated late right frontal post-retrieval monitoring effects in both young and older

10 64 brain research 1500 (2013) Fig. 5 Older participants. Scalp topography of old new effects within each window (source correct correctly rejected new) for object color and object-only encoding conditions. Exemplar electrodes are presented next to each corresponding scalp topography. Time windows and ms depict polynomial detrended data, while ms depicts nondetrended data ms is not depicted, as there were no significant effects in this window. n.s. ¼not significant. Fig. 6 Late frontal effects. Scalp topographies of object-only minus object color source correct trials for the ms time window. Exemplar electrodes are presented next to each corresponding scalp topography. adults. This suggests that older adults can recruit these frontally mediated processes, depending on the manner in which the episodes were encoded. Older adults, however, exhibited weaker parietal old new effects compared to the young. Further, older adults displayed a sustained latenegativity that was more pronounced for the object color condition. Lastly, FN400 effects were larger for object color than object-only trials in the old only. These results and their implications are discussed further below Behavioral results As predicted, explicit direction of attention toward item source associations at encoding did improve source memory accuracy for young and older adults, replicating previous findings suggesting encoding support may effectively improve performance in young (Kuo and Van Petten, 2006) and older adults (Glisky et al., 2001; Glisky and Kong, 2008; Hashtroudi et al., 1994; Naveh-Benjamin et al., 2007). Interestingly, while this direction of attention did not influence item memory accuracy in the young, consistent with the results of Kuo and Van Petten, there was a slight benefit for older adults. Nevertheless, the benefit to source memory accuracy far exceeded that to item memory accuracy in both groups. These results were consistent with our hypothesis that the explicit direction of attention at encoding would reduce demands on strategic retrieval processes, which are especially critical for source compared to item recognition (Hasher and Zacks, 1979; Troyer et al., 1999). Interestingly, while older adults did display a source memory accuracy benefit from the attention manipulation, the magnitude of this benefit was less than for young adults. This was evident despite the fact that our performance matching manipulation generally equated performance for

11 brain research 1500 (2013) the object-only condition between groups. 2 These results suggest that directing attention toward item source conjunctions alone is insufficient to raise older adults source accuracy to the level of the young. Although some previous studies (Glisky et al., 2001; Glisky and Kong, 2008) have found that similar encoding manipulations can ameliorate older adults memory impairments, the memory loads for these studies were much smaller compared to our own (o20 vs. 180). Thus, at higher memory loads, the direction of attention may be less advantageous for the old than for the young. We have previously shown that elaborative encoding manipulations like self-referential processing also enhance source memory accuracy in the young and old, but agerelated deficits persist (Dulas et al., 2011). It may be the case that while encoding support may benefit older adults, it is not sufficient to boost their source memory accuracy to the level of the young. In support of this idea, previous work has shown that only when older adults are given support at both encoding and retrieval do they perform as well as young adults on associative memory tests (Naveh-Benjamin et al., 2007). In that study, participants were asked to generate a sentence with a meaningful link between two words at encoding. At retrieval, they were asked to reflect back on the sentences they generated during encoding before making their memory decision. This finding is consistent with the idea that age-related episodic memory deficits may have several underlying causes, including inefficient or nonspontaneous encoding (Craik and Byrd, 1982; Dunlosky and Hertzog, 1998; Glisky et al., 2001), associative binding deficits (Old and Naveh-Benjamin, 2008), and declines in executive processes related to strategic memory retrieval, including monitoring (Cohn et al., 2008; Gallo et al., 2006; Hasher and Zacks, 1979; Johnson et al., 1993). Further research is necessary to determine if other forms of encoding support besides directed attention, or combinations of encoding and retrieval support, are sufficient to overcome age-related source memory deficits ERP results Parietal old new effects As predicted, the explicit direction of attention during encoding had no effect on the magnitude of the parietal old new effect in either age group. The parietal old new effect has typically been associated with recollection (Allan et al., 1998; Curran, 2000; see Friedman, 2000; Johnson et al., 2008; Rugg and Curran, 2007 for review; Tendolkar and Rugg, 1998; Wilding and Rugg, 1996). Given that the magnitude of this effect is believed to be proportional to the amount of information recollected (Vilberg et al., 2006), this finding 2 In order to assess whether our matching manipulation may have contributed to the residual source memory impairment in the old, we tested a second group of young adults who also performed the experiment with the halved memory load, like the old. Results showed that although young adults source memory estimates were greater than those of the old for both conditions, young adults still obtained a larger benefit than the old from directed attention. Thus, it is unlikely that our memory load manipulation accounts for residual source memory impairment in the old. suggests that the amount of information recollected may have been equivalent for object color and object-only conditions. This may seem at odds with the fact that source accuracy was substantially greater for object color than object-only trials for both groups. However, it is possible that a similar amount of contextual information was recollected for both conditions, but that some of this information was non-criterial (i.e. not color) (Dodson and Johnson, 1996; Mollison and Curran, 2012; Yonelinas and Jacoby, 1996). For example, participants may recollect the encoding task, which would not necessarily inform their source memory decision. Studies using measures of recollection, such as ROC curves, would be necessary to interrogate this idea further. Interestingly, older adults showed reduced parietal old new effects compared to young adults for both conditions. Age-related reductions in parietal old new effects have been observed in previous studies, including those assessing recollection directly (Ally et al., 2008; Wegesin et al., 2002). In the present data, this was true even when source memory performance was matched with that of the young, i.e. the object-only condition. This suggests that age-related alterations in the neural correlates of recollection are not simply related to performance differences. That is, as performance declines (i.e. with age), it is possible that the number of lucky guesses will increase, diluting the neural correlates of recollection (Li et al., 2004; Rugg and Morcom, 2005). Given that the parietal old new effect was reduced in the old regardless of whether source accuracy estimates were reduced relative to those of the young, it is unlikely that this pattern is simply a performance-related effect. Instead, the overall reduction in the magnitude of the parietal old new effect likely reflects an age-related alteration in recollective processing. Further, explicit direction of attention at encoding may be insufficient to attenuate age-related source memory impairments in the face of impaired recollection FN400 The earliest evidence of the influence of directed attention during encoding on retrieval processing was in the FN400 in older adults. While older adults showed no significant objectonly old new effects, their FN400 for object color trials was of an equal magnitude as that of young adults. The FN400 has generally been tied to familiarity-based recognition (Curran, 2000; Duarte et al., 2006; Wolk et al., 2009), or more recently, conceptual priming (e.g. Paller et al., 2007; Voss and Paller, 2006). Further, behavioral and ERP evidence has shown that estimates of familiarity and the FN400 may be attenuated in older adults (Duarte et al., 2006; Dulas et al., 2011; Wolk et al., 2009). Previous behavioral work using ROC curves has suggested that, when items and their features are highly unitized (e.g. via object color integration), familiarity may support source memory decisions (Diana et al., 2008). Interestingly, ERP evidence suggests that the FN400 is enhanced for accurate retrieval of highly unitized item source (Diana et al., 2011; Mollison and Curran, 2012) or intra-item (Jager et al., 2006) associations. Collectively, these results suggest that unitization may enhance familiarity-based recognition of item source associations for both young and older adults. Future studies implementing direct measures of familiarity

12 66 brain research 1500 (2013) and recollection processes will be necessary to better understand age-related differences in unitization Late old new effects As predicted, explicit direction of attention at encoding to the conjunction of item and source features attenuated the late right frontal maximal old new effects seen between 1000 and 1400 ms in the young. The late right frontal old new effect is commonly observed in source memory studies (Allan et al., 1998; Donaldson and Rugg, 1998; Wilding and Rugg, 1997; Wilding, 1999). Given its time course, onsetting after initial memory recovery (e.g. FN400, parietal old new), it has been suggested to reflect post-retrieval monitoring processes, such as evaluating the products of retrieval, resolution of interference, and confidence monitoring (Cruse and Wilding, 2009; Donaldson and Rugg, 1998; Kuo and Van Petten, 2006, 2008; see Mitchell and Johnson, 2009 for review; Wilding, 1999). Further, work has shown this right-lateralized late frontal effect is not dependent on recollection success (Senkfor and Van Petten, 1998), nor task difficulty (Van Petten and Senkfor, 1996), and is not even specific to episodic memory (Hayama et al., 2008). Collectively, these studies suggest that the right frontal old new effect is most pronounced when the sought after information, episodic or not, is difficult to recover and the participant is close to his/her decision criterion (i.e. is this object the same color?). Our finding of an attenuated right frontal old new effect for object color trials, for which item source associations were tightly bound, is consistent with this theory. Although recollection likely supported correct source memory judgments regardless of prior encoding history, as evidenced by the similar magnitude of parietal old new effects for both object color and object-only conditions in both age groups, additional monitoring operations may have been engaged when the sought after color information was difficult to recover or resolve. Interestingly, despite the late widespread negativity seen in older adults only, which partly swamped the old4new effects (discussed below), results showed evidence that directed attention at encoding attenuated late frontal effects in older adults as well. That is, the same pattern of objectonly4object color ERPs was present in both young and older adults, despite the pronounced negativity. Indeed, there was no significant difference in the magnitude of this effect between the groups. This suggests that older adults may also engage frontally mediated post-retrieval monitoring processes, and that the need for these processes may be attenuated when item source associations are tightly bound in older adults as well. These results are in line with previous evidence suggesting that, when performance is matched, older adults are able to recruit frontally-mediated postretrieval processes to a similar degree as young adults (Li et al., 2004). Studies which show age-related attenuation of late frontal effects (see Friedman, 2000 for review; Gutchess et al., 2007; Trott et al., 1997; Wegesin et al., 2002) have not always matched for performance between groups. Further, it is possible that the late negativity, seen in the present study, may have been present to some degree in these studies, swamping the late frontal effect. However, we believe it is likely that the demands in the present study simply may have encouraged participants to initiate postretrieval monitoring. It should be noted, however, that the sustained, widespread negativity seen in older adults may mask some age-related differences in the late right frontal effect. Further, it is impossible to discern if the neural generators of the late right frontal effect are in fact the same for both groups. That is, while the attenuation of this effect by directed attention at encoding may be similar in magnitude between groups, it is unclear if both groups are engaging in the same frontally mediated monitoring processes. Future work using other imaging techniques may be better able to address these issues. As stated previously, older adults showed a widespread late negative old new effect particularly for the object color condition, which pervaded most electrodes. Previous evidence in young adults suggests this late negativity may reflect activity related to additional searches for visual information that may support source recognition decisions (Cycowicz et al., 2001; Friedman et al., 2005; see Johansson and Mecklinger, 2003 for review; Mecklinger et al., 2007), which in the current study could be color. As this effect also occurs after the onset of the parietal old new effect, it seems likely that this late negativity reflects another form of postretrieval monitoring (Johnson et al., 2008). That is, while the late frontal effect may reflect manipulation and/or judgments concerning the products of retrieval, the late negativity may reflect controlled searches for perceptual source-specifying details. Two previous studies have shown evidence of a stronger late negative effect for older than young adults (Cansino et al., 2012; Li et al., 2004). Li et al. (2004) proposed that this might suggest that young and older adults are relying on different kinds of information; namely young adults may be relying on abstract/conceptual information, while older adults may be attempting to retrieve the specific visual information about the prior episode. The authors suggest their results may underlie differences in retrieval orientation and/or age-related impairments in the encoding of abstract details. Given that older adults in the current study showed reduced parietal old new effects, it is possible that, due to poorer recollection, older adults were more likely to engage in additional searches for visual details. Further, as older adults also showed a stronger FN400 for object color trials, this may suggest that older adults particularly engaged in this search when they had a strong feeling of familiarity. Lastly, evidence has suggested older adults may recruit additional processes relative to the young, perhaps in a compensatory manner (Park and Reuter-Lorenz, 2009). In the present study, this compensation may be sufficient to raise performance to the level of the young under some conditions (e.g. object-only condition) but not others (e.g. object color condition). With regard to the particular prefrontal cortical (PFC) regions that might support the ERP effects shown here, lesion (Burgess and Shallice, 1996; Duarte et al., 2006; Janowsky et al., 1989) and fmri studies (Cabeza et al., 1997; Henson et al., 2000; Rugg and Henson, 2003) suggest that the lateral PFC, particularly the dorsolateral PFC (DLPFC) (see Mitchell and Johnson, 2009 for review), may support strategic retrieval processes. Interestingly, corresponding event-related fmri research from our own lab (Dulas and Duarte, 2011a) and