Neuroscience 261 (2014) 95–106

AGE-RELATED EFFECTS ON PERCEPTUAL AND SEMANTIC ENCODING IN MEMORY M. C. C. KUO, a,c K. P. Y. LIU, a,b* K. H. TING a AND C. C. H. CHAN a*

INTRODUCTION The cognitive decline that accompanies aging includes domains such as working and episodic memory (e.g., Buckner, 2004; Luo and Craik, 2008; Lim et al., 2012). These memory deficits observed in older people are characterized as either encoding or retrieval specific. The decline in memory encoding abilities might be more difficult to detect than the decline in retrieval (Friedman et al., 2007). Nevertheless, neuroimaging studies have suggested that older adults might experience significant deficits in encoding (e.g., Morcom et al., 2003; Gutchess et al., 2005). A full understanding of memory function in older adults therefore requires investigation of their encoding deficits. Subsequent memory effect (SME) is a common eventrelated potentials (ERPs) index that reflects processes during encoding (Wagner et al., 1999). It is defined as the differences in amplitude between the ERPs elicited during encoding (approximately 400–700 ms post stimulus, corresponding to P550, and 700–1000 ms or later as the late positive component [LPC] for subsequently successfully retrieved trials versus missed trials (e.g., Cansino and Trejo-Morales, 2008; Cansino et al., 2010; Kuo et al., 2012). SMEs reflect the processes of encoding, such as elaborative processing and maintenance of representation for further incorporation (Wagner et al., 1999; Cansino et al., 2010). Early SMEs near the 150–250-ms (P2) and 250– 400-ms (N3) time windows have also been found to reflect attention, working memory, and access to semantic memory (Tellez-Alanis and Cansino, 2004; Kutas and Federmeier, 2011; Kuo et al., 2012). Subsequently correctly identified trials typically elicit more positive-going ERPs. These differences in ERPs (i.e., SME) are attributable to the processes that are associated with successful encoding for subsequent memory retrieval tests. Five ERP studies investigated differences in encoding, using SMEs as indices, between younger and older adults using perceptual and/or semantic encoding tasks (Friedman et al., 1996; Friedman and Trott, 2000; Tellez-Alanis and Cansino, 2004; Gutchess et al., 2007; Cansino et al., 2010). Only Tellez-Alanis and Cansino (2004) found early SMEs in the P2 and N3 time windows in younger and older adults. Of the four studies that utilized tasks prompting semantic encoding (natural/ artificial judgments in Friedman et al., 1996; Cansino et al., 2010, and Tellez-Alanis and Cansino, 2004; participant’s own strategy in Friedman and Trott, 2000),

a

Applied Cognitive Neuroscience Laboratory, Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hong Kong, China b University of Western Sydney (School of Science and Health), Australia c Department of Applied Science, Hong Kong Institute of Vocational Education, Hong Kong, China

Abstract—This study examined the age-related subsequent memory effect (SME) in perceptual and semantic encoding using event-related potentials (ERPs). Seventeen younger adults and 17 older adults studied a series of Chinese characters either perceptually (by inspecting orthographic components) or semantically (by determining whether the depicted object makes sounds). The two tasks had similar levels of difficulty. The participants made studied or unstudied judgments during the recognition phase. Younger adults performed better in both conditions, with significant SMEs detected in the time windows of P2, N3, P550, and late positive component (LPC). In the older group, SMEs were observed in the P2 and N3 latencies in both conditions but were only detected in the P550 in the semantic condition. Between-group analyses showed larger frontal and central SMEs in the younger sample in the LPC latency regardless of encoding type. Aging effect appears to be stronger on influencing perceptual than semantic encoding processes. The effects seem to be associated with a decline in updating and maintaining representations during perceptual encoding. The age-related decline in the encoding function may be due in part to changes in frontal lobe function. Ó 2013 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: event-related potentials, subsequent memory effect, aging, perceptual encoding processing, semantic processing.

*Corresponding authors. Address: University of Western Sydney, School of Science and Health, Locked Bag 1797, Penrith, NSW 2751, Australia. Tel: +61-2-4620-3432; fax: +61-2-4620-3792 (K. P. Y. Liu). Address: Applied Cognitive Neuroscience Laboratory, Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China. Tel: +8522766-6727 (C. C. H. Chan). E-mail addresses: [email protected] (K. P. Y. Liu), Chetwyn. [email protected] (C. C. H. Chan). Abbreviations: A/C/P, anterior, central, posterior; ANCOVA, analysis of covariance; EEGs, Electroencephalograms; EOGs, electrooculograms; ERPs, event-related potentials; LPC, late positive component; RTs, reaction times; SME, subsequent memory effect.

0306-4522/13 $36.00 Ó 2013 IBRO. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neuroscience.2013.12.036 95

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three reported significant SMEs at the P550 and LPC latencies in both groups (Friedman and Trott, 2000; Tellez-Alanis and Cansino, 2004; Cansino et al., 2010). Two studies have included a perceptual task; Gutchess et al. (2007) used scenic pictures as stimuli (determining if water is present in the picture), whereas Friedman et al. (1996) used words (determining if first and last letters were in exact ascending alphabetic sequence). Gutchess et al. (2007) showed significant SMEs in both younger and older adults groups; however, Friedman et al. (1996) showed that the effect was only significant in the younger group. The inconsistent findings across these two studies could be partly due to differences in the designs both across (e.g., stimulus material pictures vs. words) and within (e.g., number and location of analyzed electrode sites) the experiments. Among all of these studies, only the one conducted by Friedman et al. (1996) included both perceptual and semantic tasks. However, the complexity level of their tasks was not equalized, which makes the comparison and interpretation of the results difficult. Any comparisons between tasks could be confounded by task difficulty. This also seems to be a common shortcoming in other studies of younger adults that include both tasks (Weyerts et al., 1997; Otten and Rugg, 2001). The results typically suggest that SMEs elicited from perceptual encoding are unreliable or smaller in magnitude than those from semantic encoding (Paller et al., 1987; Weyerts et al., 1997). The findings of these studies indicate that meaningful comparisons of SMEs elicited through perceptual and semantic encoding tasks would need consistent and stringent controls of encoding processes stipulated by the tasks. The contrasts among SMEs elicited across age groups shed light on the age-related effects of encoding. Significant differences in SME amplitude and topography were revealed in a LPC latency that was beyond 600 ms post-stimulus (Friedman and Trott, 2000; Gutchess et al., 2007; Cansino et al., 2010). Other results revealed non-significant amplitude differences at LPC in the ERPs elicited by remember and know (or with higher or lower confidence judgments) judgments that were subsequently correctly identified among older adult subjects (Friedman and Trott, 2000; Gutchess et al., 2007). It was therefore proposed that older adults might tend to encode information uniformly without much elaboration. This seems to be true in both perceptual (Gutchess et al., 2007) and semantic encoding (Friedman and Trott, 2000), which indicates that encoding may be affected by aging indiscriminately across tasks. All of these studies drew conclusions based on results generated from independent perceptual and semantic encoding tasks. The extent to which the differences in the task designs and contents would have confounded the results had not been properly addressed. The aim of this study was to readdress the age-related effects on perceptual and semantic encoding. To address the weaknesses in the design of the tasks used in previous studies, perceptual and semantic tasks

employed in this study used comparable visual stimuli, i.e., single Chinese characters of objects, for producing the perceptual and semantic encoding processes. The difficulty levels of the tasks were similar, to minimize any possible confound on the SME amplitude. A previous study using the same task with a group of young adults revealed SMEs at the P2 and N3 latencies (Kuo et al., 2012). In the literature, age differences are most consistently found at approximately 600 ms post stimulus. Therefore, it is hypothesized that, similar to young adults, older adults would manifest SMEs at the P2 and N3 latencies in both semantic and perception conditions with little or no difference across groups in both conditions. This indicates that older adults would have intact perceptual analysis and access of semantic memory. In contrast, between-group differences would be found in the SMEs at the P550 and/or LPC latencies. This would indicate that older adults have deficits in early elaborative processing and maintaining representation for further processing across conditions.

EXPERIMENTAL PROCEDURES Participants Seventeen healthy young adults (six male, 11 female) were recruited for the study using the following selection criteria: (1) between 18 and 28 years of age, (2) righthanded, (3) native Chinese speaker, (4) able to read a local Chinese newspaper to ascertain Chinese literacy level to ensure recognition of all of the stimuli used in the study, (5) normal or corrected-to-normal vision, and (6) no history of neurological or memory diseases. The subjects were recruited through advertisements posted on the university campus or through personal referrals. Among them, 14 were university students, and three were university graduates. A total of 17 healthy older participants (10 male, seven female) were also recruited through advertisements using the same selection criteria as for the younger participants, except for the age requirement; these subjects were required to be older than 60 years of age. The ethics committee of the Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, approved this study. Informed consent was obtained from all participants. The younger and older adults received a reimbursement of HKD $250 (around USD $32) and HKD $300 (around USD $38), respectively, for travel expenses. Materials A total of 402 common Chinese characters (frequency >10 occurrences/million), which represent objects, were extracted from a dictionary called Xian Dai Han Yu Zi Pin Tong Ji Biao (現代漢語字頻統計表) (State Language and Letters Committee, 1992). Chinese characters are mostly composed of strokes organized into an orthographic square. The selected characters were divided into four 40-item encoding lists and eight 40-item recognition lists according to the following method. Characters were randomly selected from the

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402-character pool to each of the four encoding lists. Characters with an extreme number of strokes were identified and swapped across the four encoding lists or the eight recognition lists to ensure that the mean number of stroke characters remained balanced across the lists. Among the four encoding lists, two were used for perceptual encoding training and the other two were used for semantic training. The complexity of the characters across the four encoding lists ranged from 10.4 to 10.6 strokes, and with no between-list differences (F(3,159) = 0.016, p = 0.997). The characters grouped under the eight recognition lists followed a different method. Among the 40 characters, 20 came from random selection among those grouped under the encoding lists while the other 20 came from the pool of the unused characters. The complexity of the studied (from encoding lists) and unused characters were not statistically differed (t(318) = 0.886, p = 0.38). The character stimuli were prepared in black against a white background using Chinese font DFKai-SB (標楷 體) with a font size of 140 using the STIM2 software (Compumedics Neuroscan, Charlotte, North Carolina, USA) on a 17-inch cathode ray tube monitor, subtending maximum visual angles of 3.4° (vertical) and 4° (horizontal). Task design and procedure The paradigm used in this study was modeled on Tellez-Alanis and Cansino (2004) and was adapted from Kuo et al. (2012). There were two conditions: perceptual and semantic. In each condition, there were two phases: study and recognition. The rules and task processes stipulated in the perceptual and semantic trials made reference to those employed in previous studies (e.g., Smith, 1993; Ranganath and Paller, 1999; Rugg et al., 2000; Wilding, 2000; Otten and Rugg, 2001; Yonelinas, 2002; Duarte et al., 2004; Liu et al., 2006; Woodruff et al., 2006; Cansino and Trejo-Morales, 2008; Hayama et al., 2008; Johnson et al., 2008). The difficulty levels of the final perceptual and semantic task processes were evaluated as comparable by a panel composed of 22 professionals (with occupational therapy or psychology backgrounds). The participants received training on the task taking processes prior to beginning of the experiment. The sequence of conditions was randomized across the participants. Perceptual condition (study and recognition phases). In the study phase, a perceptual trial involved the participant to view the character presented and judge whether the character was composed of a top and bottom component. The participant indicated with pressing the left button on a keyboard with the left thumb to indicate a ‘‘Yes response while the right button with the right thumb to indicate a ‘‘No response. The participant completed two blocks (or lists) of characters in the study phase (a total of 80 trials). The order of the two blocks was randomized across the participants. The rest period was 1 min between the two blocks. After completing the study phase, the participants entered

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into the recognition phase. A recognition trial required the participant to view the character presented and judge whether the character had been previous studied in the study phase. The ‘‘Yes and ‘‘No responses were made the same way as those for the study trials. There were four recognition blocks (or lists) giving a total of 160 recognition trials. The order of the four blocks was randomized across the participants. The rest period was 1 min between every two blocks. The key allocation for the ‘‘Yes and ‘‘No responses in the study and recognition blocks was counterbalanced between participants. These responses were captured using STIM2 software (Compumedics Neuroscan, Charlotte, NC, USA) and transferred to Microsoft Excel for further processing. The participants were reminded to avoid excessive eye blinking and movements of their body to minimize movement-related artifacts throughout the experiment. Semantic condition (study and recognition phases). The sequence of the study and recognition phases in semantic condition was the same as those in the perceptual condition. A semantic study trial required the participant to view the character presented and judge whether the object referred by the character can produce a sound. The method of making the responses, and the number of blocks and trials completed by the participants were the same as those in the perceptual condition. The arrangements for the recognition phase for semantic condition were also similar to those for the perceptual condition. Timing of trials. The design of a trial was the same across all blocks (Fig. 1). For the younger group, a trial began with a fixation cross presented in the center of the screen for 500 ms. This was followed by presentation of a character for 400 ms. In a study trial, a blank screen lasted for 3100 ms (a total of 3500 ms for response) before the trial ended. In a recognition trial, the presentation of a character lasted for 300 ms and the blank screen for 2200 ms (a total of 2500 ms for response) within which the participant was to make a response. The total time for a younger participant to complete one block was 13 min and 20 s. For the older group, the timing of a trial was similar to that for the younger group, but with two exceptions. First, the exposure of the fixation cross was 1000 instead of 500 ms. Second, the blank screen followed a character presentation lasted for 3200 instead of 2200 ms. Longer time was allocated to the trials for participants in the older group due to compensation for the age-related slowness and allowing sufficient time for making responses. Similar adjustments in the timing of trials were employed by Guillaume et al. (2009) for accommodating the between younger-older group differences. The average time accommodation given to the older participants was approximately 16 min. The typical resting time between blocks was 1 min. Between the study and recognition phases, the resting time was 2 min, and between the conditions, the resting time was 10 min.

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Fig. 1. Schematic diagrams of trials in the study and recognition blocks: (A) Two trials in study blocks and (B) two trials in recognition blocks. (A) Note: 弓 (pinyin: gong, means bow); 斧 (pinyin: fu, means axe). (B) Note: 弓 (pinyin: gong, means bow); 貓 (pinyin: mao, means cat).

EEG data acquisition Electroencephalograms (EEGs) were recorded from 128 scalp sites using a SynAmps2 amplifier, a Quikcap system, and Acquire 4.3 software (Compumedics Neuroscan, Charlotte, NC, USA), with the impedance maintained below 10 kX at all locations. All channels were referenced to the left mastoid. The ground electrode was positioned on the forehead. Vertical electrooculograms (EOGs) were recorded using electrodes located above and below the director eye, and horizontal EOGs were recorded from electrodes at the outer canthus of each eye. The EEGs and EOGs were sampled at 1024 Hz with a low pass 200-Hz filter. Offline data were pre-processed using Edit 4.3 software (Compumedics Neuroscan, Charlotte, NC, USA). The signals were re-referenced off-line to link the left and right mastoids. Digital band-pass filtering with zero-phase shift from 0.1 Hz to 30 Hz (24 dB/oct) was applied, and ocular artifacts in EEGs were corrected using an algorithm suggested by Semlitsch et al. (1986). Continuous EEG signals were segmented into epochs from 200 ms before to 1200 ms after stimulus onset and then baseline corrected to the pre-stimulus interval. Epochs with amplitude ±75 lV in any of the 128 channels were excluded from averaging. The averaged ERPs were computed per participant by classifying epochs that were subsequently correctly identified or missed during the recognition phase. Data analysis The Statistical Package for the Social Sciences 17 software package (IBM, Chicago, IL, USA) was used to analyze the behavioral and ERP data. The behavioral data include the reaction times (RTs) and accuracies of responses obtained from the study and recognition trials. The responses from the recognition trials are categorized: ‘correctly identified’, ‘missed’ (i.e., studied item not identified as studied), ‘false alarm’ (i.e., unstudied item incorrectly identified as studied) and

‘correctly rejected’. Only trials of responses indicating correctly identified and missed were selected in the behavioral and ERP analyses. In this study, participants’ performances on the recognition trials were estimated with the d-prime (d0 ) measure (Neath and Surprenant, 2003). The d0 measure provides an accurate index of how well participants discriminated between studied and distractor items. It was calculated as Z-score of the correctly identified rate (the number of items identified correctly divided by the total number of studied items) minus Z-score of the false alarm rate (the number of items not studied but incorrectly identified as studied divided by the total number of unstudied items). To compare between-group differences, a two-way analysis of covariance (ANCOVA) was conducted for testing the Group (older, younger) and Condition (perceptual, semantic) effects on the RTs and accuracies of the study trials and d0 measures of the recognition trials. As significant difference was revealed in the years of education received by the participants between the two groups, year of education was put as the covariate in the analysis. A three-way ANCOVA was conducted for testing the Group (older, younger), Condition (perceptual, semantic), and Item (correctly identified, missed) effects for the RTs of the recognition trials. Any significant results were followed by post-hoc tests using univariate analysis with years of education as the covariate for between-group comparisons or paired-t tests for within-group comparisons. For the ERP data, the time windows of P2, N3, P550 and LPC were determined based on visual inspection and results reported in previous studies (Cansino and Trejo-Morales, 2008; Yick and Wilding, 2008; Kuo et al., 2012). Average peak latencies of P2, N3, and P550 were computed based on the correctly identified or missed recognition trials for each of the younger and older groups. Within each time window, analysis was conducted to compare peak latencies of ERP elicited from correctly identified and missed trials of the two age groups using one-way ANOVAs. Comparisons of the

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average peak latencies indicated no significant differences in the P2, N3 and P550 between the younger and older groups (all p’s > 0.063). The same time windows were used in both groups: P2 – 120 to 240 ms (peaks at approximately 174 ms post stimulus), N3 – 240 to 360 ms (peaks at approximately 292 ms post stimulus), P550 – 360 to 700 ms (peaks at approximately 552 ms post stimulus), and LPC – 700 to 1000 ms. ANCOVAs were conducted on a total of 15 electrode sites in the ERP data for P2, N3, P550 and LPC in each age group and condition, years of education as the covariates. These analyses included the factors response (correctly identified, missed)  Anterior– Central–Posterior A/C/P (anterior, central, posterior)  Right-to-Left (right inferior, right superior, midline, left superior, left inferior). The 15 electrode sites were made reference to those used in Kuo et al. (2012) with support from previous ERP studies on SME (e.g., Otten and Rugg, 2001; Tellez-Alanis and Cansino, 2004; Cansino and Trejo-Morales, 2008; Cansino et al., 2010). They were left anterior inferior F7, left anterior superior F3, midline anterior Fz, right anterior superior F4, right anterior inferior F8, left central inferior T7, left central superior C3, midline central Cz, right central superior C4, right central inferior T8, left posterior inferior P7, left posterior superior P3, midline posterior Pz, right posterior superior P4, and right posterior inferior P8. Post-hoc analyses were conducted on the significant interaction effects revealed. The Greenhouse-Geisser correction was applied to results that did not meet sphericity requirements. Bonferroni corrections were applied to the p levels of all post-hoc analyses, i.e., p 6 0.05/n (number of comparisons). Between-group analyses were performed on the subtracted waveform (ERPs of the correctly identified trials minus ERPs of the missed trials) of the same 15 sites. An ANCOVA was conducted with group (old, young)  condition (perceptual, semantic)  A/C/P (anterior, central, posterior)  right-to-left (right inferior, right superior, midline, left superior, left inferior), years of education as the covariates. Post-hoc analyses were conducted for all significant interaction effects. The between-group topographic differences were also investigated based on the subtracted waveforms. Rescaling procedure described in McCarthy and Wood (1985) was performed for removing globe amplitude differences across the subtracted waveforms. The rescaled waveforms were then tested using a three-way repeated measures ANCOVA [Group  Condition  Site (15 levels; all sites)]. The analysis was conducted to each of the P2, N3, P550 and LPC time windows. Correlation analyses were conducted to further understand the aging effect on the encoding processes. First, Pearson’s correlation was used to reveal the relationships between participants’ average SME amplitudes measured at each of the 15 sites and performances on the recognition trials (i.e., d0 measure). This procedure was implemented to the P2, N3, P550 and LPC time windows of the two conditions and two age groups. Second, to increase the power, the

analyses were conducted to correlate SME amplitudes at each of the 15 sites with d0 measure by pooling participants in the older and younger groups. Partial correlation (controlling for age as it may affect the amplitudes of the ERP components and the behavioral performance) was used in this second part of the analyses.

RESULTS Six younger subjects and five older subjects were excluded from the behavioral and ERP analyses secondary to low missed trial counts (less than 8) in either or both conditions. The remaining younger participants had a mean age of 21.8 ± 2.8 (18–28) years and an average education level of 14.8 ± 1.3 years (n = 11). The mean age of the older participants was 65.1 ± 5.2 (60–76) years with an average of 9.1 ± 4.6 years of education (n = 12). The years of education between the two groups were significantly differed (t(21) = 4.015, p = 0.001). The proportion of gender was tested using Chi-squared analysis, which showed non-significant differences between the two groups (v2 = 0.434, p = 0.510). As the sample sizes of both groups entered into analyses were relatively small, the power of the analyses (Cohen’s d or partial eta squared (gq2)) are reported together with results. Behavioral results The results of the study and recognition trials were analyzed separately. No significant Group or Condition effects were revealed on the accuracies (Group: F(1,20) = 1.866, p = 0.187, gq2 = 0.085; Condition: F(1,20) = 1.203, p = 0.286, gq2 = 0.057) and RTs of the study trials (Group: F(1,20) = 0.075, p = 0.787, gq2 = 0.004; Condition: F(1,20) = 2.02, p = 0.171, gq2 = 0.092). All the interaction effects (F’s(1,20) 0.603, gq2 < 0.014) were also not statistically significant. The Condition effect was not statistically significant on the d0 measures obtained from the recognition trials (F(1,20) = 2.624, p = 0.121, gq2 = 0.116). The Group effect however was statistically significant (F(1, 20) = 14.908, p = 0.001, gq2 = 0.427) on the d0 measure. Post-hoc tests indicated that the older group had significantly smaller d0 measures than the younger group in both the perceptual (F(1,20) = 13.782, p = 0.01, gq2 = 0.408) and semantic conditions (F(1,20) = 6.703, p = 0.018, gq2 = 0.251). The Group  Condition interaction effects (F(1,20) = 0.062, p = 0.806, gq2 = 0.003) and the covariate (F(1,20) = 0.071, p = 0.793, gq2 = 0.004) were not significant. Tests on the recognition RTs showed significant results in Item (F(1,20) = 7.953, p = 0.011, gq2 = 0.285). Post-hoc paired-t tests indicated that the mean RTs for the missed trials were significantly longer than that for the correctly identified trials in the younger group (t(21) = 4.631, p < 0.001, d = 1.302) and in the older group (t(23) = 2.502, p = 0.02, d = 0.55). All other effects, such as

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between-group (F(1,20) = 0.167, p = 0.687, gq2 = 0.008), within-group (F’s(1,20) < 4.304), p’s > 0.051, gq2 = 0.177), or covariate (F(1,20) = 0.006, p = 0.94, gq2 < 0.001) effects, were not significant (Table 1). ERP results All the 11 younger participants entered into the analyses had at least 14 correctly identified or missed trials (Duarte et al., 2004). The mean numbers of epochs for the correctly identified trials epochs for the perceptual and semantic conditions were 51.5 (SD = 8.5) and 51.3 (SD = 13.2) respectively, while those for the missed trials were 22.1 (SD = 7.0) and 22.4 (SD = 7.8). For the 12 older participants included in the analyses, the mean number of epochs for the correctly identified trials was 40.8 (SD = 13.5) and 54.8 (SD = 12.1) for the perceptual and semantic conditions, respectively, while those for the missed trials were 33.1 (SD = 13.8) and 20.3 (SD = 11.0). Between-group comparisons. Significant Group effects were revealed in the SME amplitudes over the N3 (F(1,20) = 4.349, p = 0.05, gq2 = 0.179), P550 (F(1,20) = 7.033, p = 0.015, gq22 = 0.026) and LPC latencies (F(1,20) = 5.119, p = 0.035, gq2 = 0.204). The Condition, A/C/P and Right-to-Left effects were all statistically not significant. For the Group effect, the younger group showed overall larger SME amplitudes than the older group. The Group  A/C/P interactions were statistically significant at the LPC latency (F(2,40) = 6.302, p = 0.004, gq2 = 0.24). All other interaction effects (including those related to Condition) and covariate were not statistically significant. Post-hoc analyses suggested that the younger group participants showed larger SME amplitudes only in the frontal (F(1,227) = 25.527, p < 0.001, gq2 = 0.101) and central sites (F(1,227) = 16.66, p < 0.001, gq2 = 0.068) than the older group. Within-group comparisons. Perceptual condition. In the younger group, significant SMEs were observed in all four windows (Fig. 2). The main effects of Response on the SMEs at the P2 (F(1,10) = 9.903, p = 0.01, gq2 = 0.498), P550 (F(1,10) = 10.43,

p = 0.009, gq2 = 0.511) and LPC (F(1,10) = 13.01, p = 0.005, gq2 = 0.565) latencies were all statistically significant. Among all, only the Response  Right-to-Left interactions were statistically significant over at the N3 latency (F(1,10) = 13.337, p = 0.004, gq22 = 0.571). Post-hoc comparisons showed that the correct identified trials elicited more positive SMEs at the N3 latency than missed trials at all (t’s(32)P3.756, p’s 6 0.001, d0 s > 0.598) except the right inferior sites (t(32) = 2.192, p = 0.036, d = 0.389). The interaction effects for the P2, P550 and LPC windows were not statistically significant. In the older group, significant SMEs were observed in the P2 (F(1,11) = 6.587, p = 0.026, gq2 = 0.375) and N3 windows (F(1,11) = 11.506, p = 0.006, gq2 = 0.511) (Fig. 3). Among all the interaction effects, Response  A/C/P  Right-to-Left was statistically significant at the LPC latency (F(8,88) = 2.224, p = 0.033, gq2 = 0.168). Post-hoc comparisons did not reveal significant contrasts (All p’s > 0.025). Semantic condition. For the younger group, significant SMEs were not as widely distributed as in the perceptual condition. Similar to the perceptual condition, significantly more positive SME were elicited in the correctly identified trials than in missed trials in all four windows. At the P2 latency, only a significant main effect of Response was found (F(1,10) = 6.282, p = 0.031, gq2 = 0.386). At the N3 latency, there was a significant Response  A/C/P site interaction (F(2,20) = 5.356, p= 0.014, gq2 = 0.349) and a Response  Right-to-Left interaction (F(4,40) = 3.099, p = 0.026, gq2 = 0.237). Post-hoc testing indicated that more positive SMEs were elicited at frontal (t(54) = 4.492, p < 0.001, d = 0.694) and central sites (t(54) = 2.584, p = 0.013, d = 0.41), as well as at sites in the right hemisphere (right superior t(32) = 2.742, p = 0.01, d = 0.5 and right inferior sites t(32) = 3.27, p = 0.003, d = 0.584). At the P550 latency, only a significant main effect of Response was identified (F(1,10) = 5.537, p = 0.04, gq2 = 0.356). At the LPC, a Response  A/C/P sites interaction was detected (F(1.21,20) = 5.006, p = 0.039, e = 0.605, gq2 = 0.334), indicating significant SMEs in the frontal sites (t(54) = 4.109, p < 0.001, d = 0.447). Similarly, in the older group, more positive waveforms were elicited for correctly identified trials versus missed

Table 1. Mean accuracies and RTs of older and younger participants. Standard deviations are shown in parentheses Younger group

Older group

Perceptual

Semantic

Perceptual

Semantic

Study Correct (%) Correct RT (ms)

90.46 (3.28) 661.23 (125.22)

87.17 (5.46) 750.37 (131.09)

84.9 (5.9) 652.69(145.96)

80.21 (6.1) 732.17 (179.99)

Recognition Correct (%) False alarm (%) d-prime Correct RT (ms) Missed RT (ms)

70.49 (11.29) 13.21 (11.56) 1.79 (0.60) 714.22 (120.13) 845.53 (217.81)

74.43 (14.34) 13.98 (10.72) 1.94 (0.57) 721.79 (137.60) 843.40 (219.46)

53.44 (16.23) 31.54 (13.4) 0.63 (0.40) 669.10 (161.03) 809.33 (336.04)

71.98 (15.74) 33.58 (19.88) 1.17 (0.73) 666.64 (161.74) 836.79 (278.20)

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Fig. 2. Grand average of the event-related potentials elicited by correctly identified and missed trials for (A) perceptual condition and (B) semantic condition of the younger group. A selection of 12 electrode locations from left (F3, C3, P3, F7, T7, P7) and right (F4, C4, P4, F8, T8, P8) hemispheres are shown.

trials. At the P2 latency, the Response and Right-to-Left interaction (F(2.158,23.735) = 8.181, p = 0.05, e = 0.539, gq2 = 0.233), which was confirmed in the post-hoc tests, showed that the effect was present in both the left superior (t(35) = 2.919, p = 0.006, d = 0.218) and midline sites (t(35) = 2.735, p = 0.01, d = 0.415). The main Response effect was also significant at N3 (F(1,11) = 5.7, p = 0.036, gq2 = 0.341) and at P550 latencies (F(1,11) = 5.255, p = 0.043, gq2 = 0.323). A significant Response and A/C/P site interaction was observed at the LPC latency

(F(2,22) = 4.719, p = 0.02, gq2 = 0.3). However, posthoc tests did not confirm this effect (All p’s > 0.037). Topography analyses. The between-group topographic differences were also investigated based on the subtracted waveforms. Rescaling procedure described in McCarthy and Wood (1985) was performed for removing globe amplitude differences across the subtracted waveforms. The amplitudes of the rescaled waveforms were then tested using a three-way repeated measures ANCOVA. The model was

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Fig. 3. Grand average of the event-related potentials elicited by correctly identified and missed trials for (A) perceptual condition and (B) semantic condition of the older group. A selection of 12 electrode locations from the left (F3, C3, P3, F7, T7, P7) and right (F4, C6, P4, F8, T8, P8) hemispheres are shown.

Group  Condition  Site (15 levels; all sites). The analysis was conducted to each of the P2, N3, P550 and LPC time windows. Topographies of the younger and older groups are shown in Fig. 4. The scalp analysis of topographic shapes did not reveal significant site differences between the groups in the four windows analyzed. However, the main effects of the Group were significant in N3 (F(1,20) = 4.54, p = 0.046, gq2 = 0.185), P550 (F(1,20) = 5.160, p = 0.034, gq2 = 0.205) and LPC (F(1,20) = 4.538, p = 0.046, gq2 = 0.185). All covariates were not significant statistically.

Correlation analysis. Significant correlation was found for the P2 window of the older group in the semantic condition only (r = 0.584, p = 0.046). No other significant correlation was found between the average SME amplitudes and d0 measures in other time windows of the two conditions and the two groups although the results showed a trend toward positive correlations in most windows and conditions analyzed. By pooling participants in the older and younger groups, partial correlation analyses showed that, once the effects of age were taken into account, significant relationships emerged between the amplitude of the LPC window and

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Fig. 4. Topographic representations of the scalp distributions showing the differences between activities elicited by correctly identified trials and missed trials for the 120–240-ms, 240–360-ms, 360–700-ms and 700–1000-ms intervals in (A) perceptual condition and (B) semantic condition of both groups.

the d0 measure in the perceptual condition (r = 0.588, p = 0.004).

DISCUSSION The aim of this study was to investigate age-related differences in perceptual and semantic encoding using SMEs. We used visual stimuli that were comparable between the two encoding tasks. Attempts were made to adjust difficulty level and behavioral performance between the two conditions, though RTs during the study phase were longer in the semantic condition than in the perceptual condition. Between-group differences in behavioral performance were revealed in the recognition but not the study phase. Participants in the younger group showed significantly larger d0 scores than those in the older group in the semantic and perceptual task conditions. ERP results indicated different waveform patterns across the two groups. The younger

group showed significant SMEs in all four time-windows in both conditions. In contrast, the older group exhibited significant SMEs at the P2 and N3 latencies in the perceptual condition and at the P2, N3, and P550 latencies in the semantic condition. Between-age-group differences were observed in the latter three time windows, especially in the LPC. These results suggest that the older group’s processes of visual analysis and accessing semantic memory may be preserved fairly well but that elaborative processes may be adversely affected. In addition, perceptual encoding processes seemed to be more affected by aging. Study phase performance was not significantly different between the older and younger groups, suggesting that the perceptual and semantic encoding of the Chinese characters used in this study did not seem to be biased against the older participants. The older participants performed more poorly during the character recognition phase than their younger

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counterparts, regardless of the encoding method. Other studies have also indicated that younger adults perform better than older adults in either perceptual or semantic tasks (Friedman et al., 1996; Tellez-Alanis and Cansino, 2004; Cansino et al., 2010). This indicates that both perceptual and semantic encoding are affected in aging, even though our behavioral data for encoding were equal. Within each group, significant SMEs were found in multiple windows. In the younger group, significant SMEs at the P2 latency were found at widespread scalp sites during both conditions. The SMEs at the N3 latency were found over the frontal areas and in the left hemisphere during perceptual encoding and in the right hemisphere during semantic encoding. The older sample deviated from these patterns. These deviations were not statistically significant at the P2 latency. At the N3 latency, the younger participants showed overall larger SME amplitudes than the older participants but without clear patterns of topographic distribution. These results are similar to those revealed by Tellez-Alanis and Cansino (2004), who examined semantic encoding of Spanish words in intentional and incidental contexts. These authors observed that in both young and older adults, significant SMEs were observed at P2 and N3 latencies, with a widespread distribution over the scalp. The P2 and N3 potentials were reported to associate with perceptual analysis of the orthographic forms (Liu et al., 2003) and implicit binding processes that create meaningful mental representations of stimuli through accessing the semantic memory (Kutas and Federmeier, 2011). The insignificant between-group differences observed in this study indicate that the older and younger participants might undergo similar visual analysis. However, the older adults’ implicit binding processes may be less efficient than those of the younger participants. The significant SMEs at these latencies further suggest that early visual analysis and access to semantic memory would be common and necessary for encoding Chinese characters, regardless of perceptual and semantic methods or age groups. In the older group, there were discrepancies in the generation of SMEs at the P550 and LPC latencies across the two encoding conditions, which was not the case in the younger group. The SMEs at the P550 and LPC latencies of older participants during perceptual encoding of the Chinese characters were not significant. In contrast, the SMEs elicited in the semantic encoding condition at the P550 latency were significant. In the younger group, significant SMEs were found at P550 and LPC in both conditions, and the amplitudes were comparable (Kuo et al., 2012). Our findings on the older group are consistent with Friedman et al. (1996) but are somewhat inconsistent with one previous study related to perceptual encoding. Gutchess et al. (2007) observed that perceptual encoding of scenic pictures resulted in significant fronto-central distributed SMEs at both the P550 and LPC latencies among older subjects. The fronto-central distribution identified by Gutchess et al. (2007) was very commonly associated with the processing of semantic information (Mangels et al., 2001; Cansino et al., 2010). In line with this, other

studies have suggested that pictures could be processed more spontaneously using semantically rather than perceptually based strategies (Paivio, 1971; Levie, 1987; Mintzer and Snodgrass, 1999). Therefore, results in Gutchess et al. (2007) may only be applied to pictures as encoding material. Our findings are consistent with the idea that even though Chinese characters retain some salient pictographic qualities, perceptual encoding of these characters yielded significantly lower recognition performances than semantic encoding among the older participants. The non-significant P550 and LPC SMEs should further account for the reduced performance at recalling the Chinese characters. The functions of the SMEs at the P550 and LPC latencies are early elaborative processing and maintenance of representation for further processing. The challenges to the older participants might be in updating the perceptual representation of the characters, as reflected in the nonsignificant P550 SME, which would subsequently affect maintaining the representation in the working memory and incorporating the learned characters into long-term memory for retrieval in the recognition phase of the task. Overall, the ERP results seemed to indicate that perceptual encoding is more affected by aging than is semantic encoding. Widespread SMEs were present at the P550 but not at the LPC latency when Chinese characters were semantically encoded in the older participants. Four previous studies examined SMEs in semantic encoding in older adults (Friedman et al., 1996; Friedman and Trott, 2000; Tellez-Alanis and Cansino, 2004; Cansino et al., 2010). Two studies reported significant SMEs, which lasted up to 1000 ms post stimulus and involved both P550 and LPC latencies (Friedman and Trott, 2000; Cansino et al., 2010). The third study only observed significant SMEs at the P550 latency, as analyses were conducted up to 800 ms post stimulus (Tellez-Alanis and Cansino, 2004). These three studies showed that the effect at the P550 latency was characterized by a widespread distribution that is similar to the present study. A reason for the non-significant SME at the LPC latency in the older group could be due to the more varied onset and duration of encoding processes in older adults (Friedman et al., 1996). Although the selection of windows for analysis in this study considered this variability, it was still possible that these processes might be smeared or somewhat lost due to latency jitters. In addition, encoding processes responsible for SMEs at the P550 latency may be inefficient, as evidenced by overall smaller SME amplitudes in the older sample during this latency. This could subsequently affect the encoding processes at LPC latency. One important finding from between-group contrasts is that SMEs were significantly smaller in the frontal and central regions of the older participants during the LPC window. Interaction effect for the contrast at this window was significant only between group and A/C/P sites but not in group and conditions. Therefore, it appeared such reduction in SMEs in the frontal and central sites is

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generic regardless of conditions. Within-group comparisons seemed also to concur with this postulation, such that SMEs was not significant during LPC in the older group but significant in the younger group. As noted earlier, the functions of the LPC potentials are maintenance of representation for further processing (Mangels et al., 2001; Cansino et al., 2010). Significant LPC SME differences (smaller than younger group in this case) seem to suggest that older participants might find maintaining the Chinese characters for further elaboration in working memory more challenging than do their younger counterparts. This result regarding frontal SME changes is consistent with those reported in two similar studies. First, Cansino et al. (2010) revealed that at the 800–1200-ms timewindow (an LPC latency), the SME amplitudes were smaller in the older group in the frontal region. Second, Friedman and Trott (2000) observed laterality differences among the younger participants in the 810– 1000-ms window (left > right at the frontal sites), but not among their older participants. The SME activities elicited from the frontal region have been suggested to be associated with integration and coordination of the processed information, which are functions of the frontal lobes (Cansino et al., 2010; Kuo et al., 2012). The older participants’ difficulty with maintaining information might therefore be due in part to changes in frontal lobe function. The results of partial correlation analyses indicated that, independently of age, significant relationships emerged between the amplitude of the LPC window and the d0 measure in the perceptual condition. Intervals that showed significant SMEs indicated that ERP amplitudes and performance were associated. This correlation result showed that SME amplitudes and d0 measure in the LPC window of the perceptual condition behaved in a more predictable way than other intervals. In other words, SME amplitudes in the LPC could be considered as a predictor for memory performance in the perceptual condition, and vice versa, even when the samples sizes were relatively small. The present study might be limited by the significantly lower educational level of the older group compared with the younger group, although the Chinese literacy level of both groups was comparable. The behavioral and ERP analyses were adjusted for this difference using education as a covariate. Although some effort was made to ensure that the data were comparable between groups, it would have been better if the groups were fully matched. Future research will need to take this limitation into consideration. This study investigated age-related differences in perceptual and semantic encoding tasks of similar difficulty. We observed that younger adults performed better than the older group in both tasks. Significant SMEs were observed in P2 and N3 time windows in both conditions and in the P550 time window in the semantic condition in the older participants. Group differences in SME amplitude were shown from 240 to 1000 ms post stimulus. Older participants might have a similarly strong visual analysis but less efficient access

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to semantic memory than younger participants. Perceptual encoding seemed to be more affected by aging as shown by non-significant SMEs at P550 and LPC latencies, even when recognition performance was equal between the conditions. SMEs were significantly smaller in the frontal regions of the older participants during the LPC window. As the SME activities elicited from these regions have been suggested to be associated with functions of the frontal lobes, agingrelated encoding changes may be due in part to changes in frontal lobe function. Acknowledgements—The work was supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. PolyU 5620/07M) awarded to K.P.Y. Liu. It was partially supported by an internal research grant from The Hong Kong Polytechnic University and the Health and Medical Research Fund from the Food and Health Bureau of the Hong Kong SAR Government (C.C.H. Chan as principal investigator).

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(Accepted 16 December 2013) (Available online 25 December 2013)