Abstract

Memory for face–name associations is an important type of memory in our daily lives, and often deteriorates in older adults. Although difficulty retrieving face–name associations is often apparent in the elderly, there is little neuroscientific evidence of age-related decline in this memory. The current fMRI study investigated differences in brain activations between healthy young and older adults during the successful retrieval of people's names (N) and job titles (J) associated with faces. During encoding, participants viewed unfamiliar faces, each paired with a job title and name. During retrieval, each learned face was presented with two job titles or two names, and participants were required to choose the correct job title or name. Retrieval success activity (RSA) was identified by comparing retrieval-phase activity for hits versus misses in N and J, and the RSAs in each task were compared between young and older adults. The study yielded three main findings. First, the hippocampus showed significant RSA in both tasks of N and J, and the activity was greater for young compared to older subjects. Second, the left anterior temporal lobe (ATL) showed greater RSA in N than in J, but there was no age difference in the activity in this region. Third, functional connectivity between hippocampal and ATL activities in both retrieval tasks was higher for young than for older adults. Taken together, age-related differences in hippocampal activities and hippocampus–ATL connectivity could contribute to age-related decline in relational memory and to complaints of poor retrieval of people's names by older adults.

INTRODUCTION

Memory for face–name associations is an important type of memory in our daily lives, and often deteriorates in older adults. An age-related increase in problems with this type of memory has been reported in several psychological studies, in which retrieval performance was compared between young and older adults. For example, one study found a significant decline in the retrieval of face–name associations for newly learned people in older adults (Naveh-Benjamin, Guez, Kilb, & Reedy, 2004). Another study demonstrated that older adults were impaired in the retrieval of people's names associated with familiar faces, but preserved their ability to retrieve job titles associated with these faces (James, 2006). Although the importance of the hippocampus and anterior temporal lobe (ATL) regions in the retrieval of memory for people's names or other types of information associated with faces has been demonstrated in young adults by cognitive neuroscience studies (Tsukiura, Suzuki, Shigemune, & Mochizuki-Kawai, 2008; Tsukiura, Mochizuki-Kawai, & Fujii, 2006; Kirwan & Stark, 2004; Zeineh, Engel, Thompson, & Bookheimer, 2003; Tsukiura et al., 2002; Small et al., 2001; Damasio, Grabowski, Tranel, Hichwa, & Damasio, 1996), little is known about the neural mechanisms underlying age-related changes in this memory. The current fMRI study investigated an aging effect on hippocampal and ATL activations during the retrieval of memory for face–name associations.

The importance of the hippocampus in the retrieval of relational memories has been demonstrated by human cognitive neuroscience studies (for a review, see Diana, Yonelinas, & Ranganath, 2007). For example, functional neuroimaging studies of healthy young adults have linked hippocampal activity to the retrieval of associations between verbal and visual materials (Meltzer & Constable, 2005; Prince, Daselaar, & Cabeza, 2005; Bunge, Burrows, & Wagner, 2004; Giovanello, Schnyer, & Verfaellie, 2004), as well as face–name associations (Tsukiura et al., 2008; Kirwan & Stark, 2004; Zeineh et al., 2003; Small et al., 2001). Moreover, recent functional neuroimaging studies have shown an age-related decrease in hippocampal activity during the retrieval of relational memory (for a review, see Cabeza, 2006). For example, one fMRI study identified an aging effect on hippocampal activity in the recollection process, which is related to the recovery of specific contextual information associated with a study item, but not in the familiarity process, which is related to the feeling that an item is learned in the absence of contextual details (Daselaar, Fleck, Dobbins, Madden, & Cabeza, 2006). An aging effect on recollection-related hippocampal activity is supported by psychological findings, which have indicated that older adults tend to be impaired in terms of recollection, but not familiarity (Searcy, Bartlett, & Memon, 1999; Java, 1996; Jennings & Jacoby, 1993; Parkin & Walter, 1992). Age-related deficits in relational memory performance would be induced by an age-related decline in hippocampal activity.

Previous functional neuroimaging and neuropsychological studies have linked the left ATL region to the retrieval of memory for persons (for a review, see Olson, Plotzker, & Ezzyat, 2007). For example, there is functional neuroimaging evidence of greater activation in this region during the retrieval of people's names associated with faces than during the retrieval of job titles associated with faces (Tsukiura et al., 2002), and during the retrieval of people's names associated with faces encoded with person-related semantic cues such as job titles (Tsukiura et al., 2006). Left ATL activation was also identified in the retrieval of people's names from job titles (Tsukiura et al., 2008). Neuropsychological studies have consistently reported that patients with left ATL lesions or atrophy were impaired in the retrieval of unique names such as people's names (Tranel, 2006; Lah, Grayson, Lee, & Miller, 2004; Snowden, Thompson, & Neary, 2004; Glosser, Salvucci, & Chiaravalloti, 2003; Seidenberg et al., 2002; Tsukiura et al., 2002; Fukatsu, Fujii, Tsukiura, Yamadori, & Otsuki, 1999; Papagno & Capitani, 1998; Damasio et al., 1996). Also, previous psychological studies involving healthy young and older adults demonstrated that older adults show disproportionate deficits in naming people from familiar faces, but are preserved in the retrieval of job titles from faces (James, 2006), whereas there is little evidence of a disproportionate age-related impairment in naming people from newly learned faces (Rendell, Castel, & Craik, 2005). Thus, in the retrieval of memory for newly learned people, the left ATL could contribute more significantly to the retrieval of people's names than of job titles associated with faces, but show no difference in activity between young and older adults. However, no functional neuroimaging evidence is available regarding the effects of aging on left ATL activity during the retrieval of face–name associations. In addition, one fMRI study suggests that an interaction between the hippocampal and left ATL regions would be important in the retrieval of memory for newly learned persons (Tsukiura et al., 2008). However, there is no direct evidence concerning whether functional connectivity between these regions is modulated by the aging effect during the retrieval of this memory.

To investigate age-related differences in activity in the hippocampus and left ATL regions and their interaction during the retrieval of people's names or job titles associated with faces, we scanned healthy young (mean age = 21.0 years) and older adults (mean age = 68.6 years) using fMRI during the retrieval of face–name and face–job title associations. The design of this study is summarized in Figure 1. All fMRI experiments in this study were designed by the event-related fMRI method. Encoding and retrieval phases were alternated across 10 sessions, with each retrieval session testing memory for stimuli encoded in the previous encoding session (i.e., 5 encoding–retrieval blocks). During the encoding session of each block, 24 associations of face, job title, and name were presented one by one. Subjects were instructed to learn the associations by reading the job titles and people's names silently. During the retrieval session of each block, we prepared two tasks of retrieval, which were randomly presented. The first task (N task) was the retrieval of people's names, in which each of 24 learned faces was presented with two learned names, and participants were asked to press either the “left” or “right” button when they recognized the name correctly associated with the face. In the second task (J task) during the retrieval phase, each of 24 learned faces was presented with two learned job titles, and participants were asked to press either the “left” or “right” button when they recognized the job title correctly associated with the face. The presentation order of all experimental stimuli was randomized among subjects in both encoding and retrieval phases. The retrieval trials in individual subjects were divided by two factors of task (N and J) and retrieval accuracy (hit and miss), and retrieval success activity (RSA) was identified by comparing retrieval-phase activity for hits versus misses in each task. The RSAs in the N and J tasks were compared between the young and older subgroups using a two-way analysis of variance (ANOVA) with factors of age group (young vs. old) and task (N vs. J).

Figure 1. 

Task paradigm. During encoding, participants were required to learn associations of face, job title, and people's name. During retrieval, participants performed two tasks, which were randomly presented. The first task was the retrieval of people's names (N) associated with faces, and the second task was the retrieval of job titles (J) associated with faces. The retrieval trials for individual participants were divided into successful (hit) and missed (miss) retrieval in each task. Thus, we prepared four retrieval conditions of N–Hit, N–Miss, J–Hit, and J–Miss. RSA was identified by comparing retrieval phase activity for hits versus misses in each of the N and J tasks.

Figure 1. 

Task paradigm. During encoding, participants were required to learn associations of face, job title, and people's name. During retrieval, participants performed two tasks, which were randomly presented. The first task was the retrieval of people's names (N) associated with faces, and the second task was the retrieval of job titles (J) associated with faces. The retrieval trials for individual participants were divided into successful (hit) and missed (miss) retrieval in each task. Thus, we prepared four retrieval conditions of N–Hit, N–Miss, J–Hit, and J–Miss. RSA was identified by comparing retrieval phase activity for hits versus misses in each of the N and J tasks.

On the basis of the aforementioned research, we made three predictions. First, the hippocampus would show significant RSA in both N and J tasks (for a review, see Diana et al., 2007), and activity in this region would be greater in the young age group than in the older age group (main effect of age) (for a review, see Cabeza, 2006). Second, the left ATL region would show greater RSA during the retrieval of people's names than of job titles (Tsukiura et al., 2002), and there would be no age-related difference of activity in this region (main effect of task) because there was no age-related difference in the retrieval of people's names, compared to that of job titles (Rendell et al., 2005). Finally, given that both hippocampal and left ATL regions are important in the retrieval of face–name associations (Tsukiura et al., 2008), the subjective difficulty of retrieving people's names, which is one of the most common complaints made by older adults (Rendell et al., 2005), would be modulated by lower functional connectivity between these regions in older adults than in young adults. The findings of our study could contribute to our understanding of neural mechanisms underlying aging effects on relational memory processes as well as on specially organized memory processes, namely, face–name association processes.

METHODS

Participants

Twenty-two young adults (8 women and 14 men) and 22 older adults (11 women and 11 men) participated in this study. All participants were healthy, right-handed, native Japanese speakers, with no history of neurological or psychiatric disorders. All the young participants were recruited from the Tohoku University community, and all older participants were recruited from the local community. All subjects were paid for their participation in the study, and gave informed consent to a protocol approved by the Tohoku University Institutional Review Board. Two young adults were excluded from analyses because they felt sick in the scanner. In addition, we excluded two older adults from the analyses due to low scores on the Mini Mental State Examination (<24). Thus, the reported results are based on the data from 20 young [6 women and 14 men; mean age = 21.0 (SD = 3.4) years] and 20 older adults [10 women and 10 men; mean age = 68.6 (SD = 3.7) years]. In a separate session, all the older adults performed several neuropsychological tests, in which we assessed their general intelligence by means of the Mini Mental State Examination (Folstein, Folstein, & McHugh, 1975), frontal lobe function by the Frontal Assessment Battery (Dubois, Slachevsky, Litvan, & Pillon, 2000), long-term memory by several tests from the Wechsler Memory Scale—Revised (Wechsler, 1987), Rey Auditory Verbal Learning Test (Lezak, 1995), and Rey–Osterrieth Complex Figure Test (Lezak, 1995), processing speed by digit–symbol coding from the Wechsler Adult Intelligence Scale—III (Wechsler, 1997), and mental state of depression by the Geriatric Depression Scale (Neal & Baldwin, 1994). Results and participants' characteristics are reported in Table 1. These neuropsychological results confirmed that older adults in this study were not impaired in the general intelligence, frontal lobe functions, verbal and visual memory, processing speed, and geriatric mental state.

Table 1. 

Participant Characteristics

Measure
Young (n = 20)
Old (n = 20)
Age (years) 21.0 (3.4) 68.6 (3.7) 
Sex 6/20 females 10/20 females 
MMSE – 28.6 (1.5)/30 
FAB – 14.8 (2.2)/18 
WMS-R (visual paired associates: immediate) – 11.4 (4.2)/18 
WMS-R (visual paired associates: delayed) – 4.9 (1.6)/6 
WMS-R (verbal paired associates: immediate) – 17.3 (3.2)/24 
WMS-R (verbal paired associates: delayed) – 6.7 (1.2)/8 
RAVLT (delayed recall of list A) – 8.2 (2.5)/15 
RAVLT (recognition of list A) – 13.4 (1.4)/15 
RAVLT (false positive) – 0.35 (0.8)/15 
ROCF (recall) – 16.3 (7.0)/36 
WAIS-III (digit–symbol coding) – 65 (17.6)/133 
GDS – 3.4 (2.8)/15 
Measure
Young (n = 20)
Old (n = 20)
Age (years) 21.0 (3.4) 68.6 (3.7) 
Sex 6/20 females 10/20 females 
MMSE – 28.6 (1.5)/30 
FAB – 14.8 (2.2)/18 
WMS-R (visual paired associates: immediate) – 11.4 (4.2)/18 
WMS-R (visual paired associates: delayed) – 4.9 (1.6)/6 
WMS-R (verbal paired associates: immediate) – 17.3 (3.2)/24 
WMS-R (verbal paired associates: delayed) – 6.7 (1.2)/8 
RAVLT (delayed recall of list A) – 8.2 (2.5)/15 
RAVLT (recognition of list A) – 13.4 (1.4)/15 
RAVLT (false positive) – 0.35 (0.8)/15 
ROCF (recall) – 16.3 (7.0)/36 
WAIS-III (digit–symbol coding) – 65 (17.6)/133 
GDS – 3.4 (2.8)/15 

MMSE = Mini Mental State Examination; FAB = Frontal Assessment Battery; WMS-R = Wechsler Memory Scale—Revised; RAVLT = Rey Auditory Verbal Learning Test; ROCF = Rey–Osterrieth Complex Figure Test; WAIS-III = Wechsler Adult Intelligence Scale Third; GDS = Geriatric Depression Scale.

SD values are in parentheses.

Stimuli

We selected 120 Japanese faces, 60 male and 60 female (age range = 25–60 years), with neutral expressions from a face database, which was used with the permission of the Softpia Japan Foundation (www.softopia.or.jp/rd/facedb.html). It is strictly prohibited to copy or reuse this database, or to distribute the facial data, without permission. All stimuli were converted into grayscale images with dimensions of approximately 256 × 256 pixels on a black background. Additionally, 120 common Japanese family names and 120 common job titles were selected from an on-line name database (www2s.biglobe.ne.jp/∼suzakihp/index40.html) and job title database (www.stat.go.jp/index/seido/shokgyou/5naiyou.htm). Family names, rather than first names, are generally used when addressing colleagues, friends, and so forth in Japan. By combining faces, names, and job titles, we prepared 120 associations of face, name, and job title (Figure 1). These 120 associations were divided into five lists of 24 associations, which consisted of 12 male faces and 12 female faces.

Experimental Procedures

All fMRI experiments in this study were designed by the event-related fMRI method. Encoding and retrieval phases were alternated across 10 sessions, with each retrieval session testing memory for stimuli encoded in the previous encoding session (i.e., 5 encoding–retrieval blocks). Sessions were separated by intervals of approximately 1 min. Each stimulus was presented for 5500 msec in the encoding session. In the retrieval session, to avoid the potential artifacts by slower responses in older adults than in young adults, stimuli were presented for 3500 msec in young and for 5500 msec in older subjects. The duration of stimulus presentation was determined by the pilot study for other subjects. The stimuli were separated by fixation intervals of variable length (jittered from 500 msec to 6500 msec). The presentation order of the experimental stimuli was randomized among subjects. Figure 1 illustrates an example of the stimuli in the encoding and retrieval phases. During the encoding phase of each block, 24 associations of face, job title, and people's name were presented one by one. Subjects were instructed to learn the associations by reading the job titles and people's names silently, and to judge the sex of each face by pressing either the “left” (male) or “right” (female) button.

During the retrieval phase of each block, we prepared two tasks of retrieval, which were randomly presented. The first task (N task) was the retrieval of people's names, in which each of 24 learned faces was presented with two learned names, and participants were asked to press either the “left” or “right” button when they recognized the name correctly associated with the face. In the second task (J task) during the retrieval phase, each of 24 learned faces was presented with two learned job titles, and participants were asked to press either the “left” or “right” button when they recognized the job title correctly associated with the face. The presentation order of the all experimental stimuli during the retrieval phase of each block was randomized among subjects. The retrieval trials in individual subjects were divided by two factors of task (N and J) and retrieval accuracy (hit and miss). Thus, all retrieval trials were categorized into four conditions of N–Hit, N–Miss, J–Hit, and J–Miss in individual subjects.

fMRI Scanning and Data Analysis

All MRI data acquisition was conducted with a 3-T Philips Achieva scanner. Stimuli were visually presented through a projector and back-projected onto a screen. Participants viewed the stimuli via a mirror attached with the head coil of an MRI scanner. Behavioral responses were recorded using a two-button fiber-optic response box (Current Designs, Inc., Philadelphia, PA). Scanner noise was reduced with earplugs, and head motion was minimized using foam pads and a headband. Anatomical scans began by first acquiring a T1-weighted sagittal localizer series. Second, functional images were acquired utilizing echo-planar functional images (EPIs) sensitive to blood oxygenation level dependent contrast (64 × 64 matrix, TR = 2000 msec, TE = 30 msec, flip angle = 70°, FOV = 24 cm, 34 slices, 3.75 mm slice thickness). Finally, high-resolution T1-weighted structural images (MP-RAGE, 240 × 240 matrix, TR = 6.5 msec, TE = 3 msec, FOV = 24 cm, 162 slices, 1.0 mm slice thickness) were collected.

The preprocessing and statistical analyses for all images were performed using SPM5 (Wellcome Department of Cognitive Neurology, London, UK) implemented in MATLAB (www.mathworks.com). In the preprocessing analysis, images were corrected for slice-timing and motion, then spatially normalized into the MNI template and spatially smoothed using a Gaussian kernel of 8 mm FWHM.

The fMRI analyses focused on data from the retrieval phase. Encoding-related activity for young and older subjects will be reported elsewhere. Statistical fMRI analyses were performed first at the subject level and then at the group level. At the subject level, fixed effect analyses were performed. Stimulus onsets were modeled as delta functions convolved with a canonical hemodynamic response function in the context of the general linear model. Confounding factors (head motion, magnetic field drift) were also included in the model. Successful and missed retrieval activity for the retrieval task of N and J was identified in the retrieval-phase activity for the retrieval hits and misses, and RSA in the N and J tasks was identified by comparing retrieval-phase activity for hits versus misses in each task (N-RSA and J-RSA). All contrasts yielded a t statistic in each voxel.

At the group-level random effect analysis, by using contrast images from the subject-level fixed effect analyses, we conducted a model of a two-way ANOVA, in which two RSA contrasts (within-subject factor of task: N-RSA and J-RSA) were included in both age groups (between-subject factor of age group: young and old). At this analysis, we performed two patterns of statistical analysis. First, for assessing common areas of RSA across age groups, an effect (F-contrast) of all conditions (p < .005 with minimum cluster size of 5 voxels) was masked inclusively with two t-contrasts of RSA in young and RSA in old (p < .05). This procedure yielded an activation map containing voxels that showed significant RSAs for both age groups in both tasks. In addition, to identify greater RSAs in both N and J for young than old, an effect (F-contrast) of all conditions (p < .005 with minimum cluster size of 5 voxels) was masked inclusively with two t-contrasts of RSA-young versus RSA-old (p < .05) and RSA-young (p < .05). In this procedure, we found greater RSAs for young than for older adults in both tasks. Similarly, to identify greater RSAs in both N and J for old than young, an effect of all conditions (p < .005 with minimum cluster size of 5 voxels) was masked inclusively with two t-contrasts of RSA-old versus RSA-young (p < .05) and RSA-old (p < .05). This procedure showed us greater RSAs for older than for young adults in both tasks.

Second, to identify greater RSAs in N than J (task effect) in both age groups, a main effect (F-contrast) of task (p < .05 with minimum cluster size of 5 voxels) was masked inclusively with a t-contrast of N-RSA versus J-RSA (p < .05). This procedure yielded an activation map reflecting greater RSA for N than for J in both age groups. In addition, the aging effect on the activity of N-RSA versus J-RSA was identified in an F-contrast of task effect (p < .05 with minimum cluster size of 5 voxels) inclusively masked with two t-contrasts of RSA-young versus RSA-old (p < .05) and N-RSA versus J-RSA in young (p < .05). In this procedure, we found an activation map reflecting age-related decrease in the contrast of N-RSAs with J-RSAs. Similarly, the reverse effect of aging on the activity of N-RSA versus J-RSA was identified in an F-contrast of task effect (p < .05 with minimum cluster size of 5 voxels) inclusively masked with two t-contrasts of RSA-old versus RSA-young (p < .05) and N-RSA versus J-RSA in old (p < .05). This procedure provided us an activation map reflecting age-related increase in the contrast of N-RSAs with J-RSAs. All coordinates of activations were converted from MNI to Talairach space (Talairach & Tournoux, 1988).

To investigate the aging effect on functional connectivity between regions activated in the previous analysis, we conducted a three-step analysis on the basis of “individual trial activity” (Rissman, Gazzaley, & D'Esposito, 2004), using a procedure that was successfully applied in our previous study (Tsukiura & Cabeza, 2008). First, we created a general linear model, in which each individual trial was modeled by a separate covariate, yielding different parameter estimates for each individual trial and for each individual subject. Second, for each subject, activations in each individual trial were extracted from ROIs, which were each defined as a cluster activated in the previous analysis. Pearson correlations between activated regions were computed for individual trial activities during the retrieval of names and job titles from all subjects. Finally, these correlation coefficients (r) were converted to Z scores using Fisher's t-to-Z transformation, and then the differences in Z scores between young and older age groups were analyzed by the standard normal distribution (one-tailed).

RESULTS

Behavioral Results

Table 2 lists behavioral data for the young and older age groups. Young subjects retrieved both people's names and job titles more accurately than older subjects (71.8% in young and 57.8% in older adults). Additionally, retrieval accuracy in the J task (71.2%) was better than that in the N task (58.4%). A two-way ANOVA with factors of age (young vs. old) and task (N vs. J) showed significant main effects of age [F(1, 38) = 60.1, p < .001] and task [F(1, 38) = 84.7, p < .001], but no significant interaction between these factors [F(1, 38) = 2.2, ns]. The findings demonstrate that retrieval performance of relational memories was negatively affected by age, and retrieval performance of people's names was significantly worse than that of job titles, but no evidence was found for a disproportionate age-related impairment in the retrieval of people's names (Rendell et al., 2005). The pattern of retrieval accuracy is shown in Figure 2.

Table 2. 

Behavioral Results


Young (SD)
Old (SD)
Mean (SD)
Retrieval Accuracy (%) 
Overall 71.8 (10.6) 57.8 (8.7) 64.3 (11.8) 
N task 64.4 (8.6) 52.5 (5.9) 58.4 (9.4) 
J task 79.2 (6.2) 63.2 (7.8) 71.2 (10.7) 
 
Reaction Time (msec) 
Overall 1954.2 (295.6) 2990.4 (460.5) 2472.3 (647.2) 
Overall (N task) 1949.8 (270.3) 2860.7 (428.9) 2405.3 (580.5) 
N–Hit 1871.2 (246.6) 2835.8 (412.2) 2353.5 (592.4) 
N–Miss 2028.4 (276.0) 2885.7 (454.2) 2457.0 (571.0) 
Overall (J task) 1958.6 (322.3) 3120.0 (459.6) 2539.3 (705.0) 
J–Hit 1819.2 (256.5) 3011.8 (433.0) 2415.5 (698.6) 
J–Miss 2098.0 (326.3) 3228.2 (470.5) 2663.1 (698.1) 

Young (SD)
Old (SD)
Mean (SD)
Retrieval Accuracy (%) 
Overall 71.8 (10.6) 57.8 (8.7) 64.3 (11.8) 
N task 64.4 (8.6) 52.5 (5.9) 58.4 (9.4) 
J task 79.2 (6.2) 63.2 (7.8) 71.2 (10.7) 
 
Reaction Time (msec) 
Overall 1954.2 (295.6) 2990.4 (460.5) 2472.3 (647.2) 
Overall (N task) 1949.8 (270.3) 2860.7 (428.9) 2405.3 (580.5) 
N–Hit 1871.2 (246.6) 2835.8 (412.2) 2353.5 (592.4) 
N–Miss 2028.4 (276.0) 2885.7 (454.2) 2457.0 (571.0) 
Overall (J task) 1958.6 (322.3) 3120.0 (459.6) 2539.3 (705.0) 
J–Hit 1819.2 (256.5) 3011.8 (433.0) 2415.5 (698.6) 
J–Miss 2098.0 (326.3) 3228.2 (470.5) 2663.1 (698.1) 

N = retrieval of people's names; J = retrieval of job titles.

Figure 2. 

Retrieval accuracy in young and older adults. Hit rate [hits/(hits + misses)] was calculated for each participant. A two-way ANOVA for these data showed significant main effects of age (young vs. old) and task (N vs. J), but no interaction between these two factors.

Figure 2. 

Retrieval accuracy in young and older adults. Hit rate [hits/(hits + misses)] was calculated for each participant. A two-way ANOVA for these data showed significant main effects of age (young vs. old) and task (N vs. J), but no interaction between these two factors.

Regarding reaction time, young subjects showed significantly faster reaction times than older subjects in both retrieval tasks of people's names (young: 1949.8 msec; old: 2860.7 msec) and job titles (young: 1958.6 msec; old: 3120.0 msec). Additionally, reaction times during successful retrieval were faster than those during unsuccessful retrieval in both young (hit: 1845.2 msec; miss: 2063.2 msec) and older subjects (hit: 2923.8 msec; miss: 3056.9 msec). The difference in reaction times between hits and misses was identified in both tasks of N (hit: 2353.5 msec; miss: 2457.0 msec) and J (hit: 2415.5 msec; miss: 2663.1 msec). A three-way ANOVA with factors of age (young vs. old), task (N vs. J), and accuracy (hit vs. miss) showed significant main effects of age [F(1, 38) = 87.8, p < .001], task [F(1, 38) = 22.4, p < .001], and accuracy [F(1, 38) = 87.9, p < .001]. A significant interaction was identified between age and task [F(1, 38) = 19.5, p < .001], age and accuracy [F(1, 38) = 5.1, p < .05], and task and accuracy [F(1, 38) = 17.5, p < .001], but not between these three factors [F(1, 38) = 0.4, ns].

fMRI Results

Confirming our first prediction, significant RSA in the hippocampus during the retrieval of people's names and job titles was identified in both young and older adults, and the activity was greater for young than for older adults. However, there was no significant difference of hippocampal RSA between the N and J tasks (Figure 3). RSA during the retrieval of both people's names and job titles was identified in the right hippocampus, and the activity was significant in both young and older subjects. The same pattern of activations was found in the bilateral lateral prefrontal cortices, cerebellum, right superior temporal gyri (posterior portion), occipital regions, left parietal regions, and some subcortical areas such as the putamen or thalamus (Table 3). When we compared RSAs for both people's names and job titles between the two age groups, the bilateral hippocampi showed greater activations in young subjects than in older subjects (Figure 3). A two-way ANOVA with factors of age (young vs. old) and task (N vs. J) for the bilateral hippocampal activities showed a significant main effect of age [right: F(1, 38) = 5.7, p < .05; left: F(1, 38) = 7.2, p < .05], but not a main effect of task [right: F(1, 38) = 3.1, ns; left: F(1, 38) = 3.1, ns] or of their interaction [right: F(1, 38) = 0.2, ns; left: F(1, 38) = 0.8, ns]. Other regions showing an age-related decrease in RSA were identified in the bilateral inferior and medial parietal regions, right prefrontal cortex, left insular and cerebellar regions (Table 3). However, age-related increase in RSA was not identified in any region (Table 3).

Figure 3. 

Images, effect sizes, and time courses of the hippocampal activations. The bilateral hippocampi showed greater activity in young than in older adults, but there was no significant difference of activity in these regions between the N and J conditions. (A) Activation image and effect sizes in the right hippocampus. (B) Activation image and effect sizes in the left hippocampus. *p < .05.

Figure 3. 

Images, effect sizes, and time courses of the hippocampal activations. The bilateral hippocampi showed greater activity in young than in older adults, but there was no significant difference of activity in these regions between the N and J conditions. (A) Activation image and effect sizes in the right hippocampus. (B) Activation image and effect sizes in the left hippocampus. *p < .05.

Table 3. 

Retrieval Success Activity in Both People's Name and Job Title Retrieval Conditions

Regions
L/R
BA
Coordinates
F
x
y
z
Common to Both Young and Old Age Groups 
Hippocampus  26 −8 −22 18.44 
Superior frontal gyrus 10 −22 59 14 25.39 
Superior frontal gyrus −19 49 36 13.87 
Middle frontal gyrus 10 −41 41 15 25.63 
Middle frontal gyrus 26 35 40 13.75 
Inferior frontal gyrus 47 −48 25 −8 11.13 
Precentral gyrus −56 −13 32 9.29 
Superior temporal gyrus (posterior) 22/39 52 −54 20 25.20 
Superior temporal gyrus (posterior) 42 59 −36 16 11.72 
Fusiform gyrus 19 −30 −81 −21 21.51 
Supramarginal gyrus 40 −56 −57 27 35.42 
Postcentral gyrus 43 −52 −17 18 17.31 
Postcentral gyrus 52 −23 53 12.71 
Posterior cingulate gyrus LR 23 −50 16 22.29 
Lingual gyrus 18 −77 −6 10.29 
Cuneus 18 19 −90 18 11.11 
Putamen  −19 −10 11 18.29 
Thalamus  22 −18 11 11.94 
Cerebellar hemisphere  −15 −52 −10 20.46 
Cerebellar hemisphere  11 −45 −23 15.80 
Cerebellar hemisphere  −11 −37 −20 12.35 
 
Young Age Group > Old Age Group 
Hippocampus  22 −8 −22 15.16 
Hippocampus  −22 −33 −8 9.91 
Middle frontal gyrus 30 24 33 10.88 
Supramarginal gyrus 40 −48 −50 27 30.95 
Supramarginal gyrus 40 48 −52 48 11.47 
Posterior cingulate gyrus LR 23 −50 16 22.29 
Precuneus 31 −11 −49 34 14.42 
Insula  −33 10 17.99 
Cerebellar hemisphere  −30 −52 −29 18.97 
Cerebellar hemisphere  −19 −48 −13 12.45 
 
Old Age Group > Young Age Group 
No significant activation 
Regions
L/R
BA
Coordinates
F
x
y
z
Common to Both Young and Old Age Groups 
Hippocampus  26 −8 −22 18.44 
Superior frontal gyrus 10 −22 59 14 25.39 
Superior frontal gyrus −19 49 36 13.87 
Middle frontal gyrus 10 −41 41 15 25.63 
Middle frontal gyrus 26 35 40 13.75 
Inferior frontal gyrus 47 −48 25 −8 11.13 
Precentral gyrus −56 −13 32 9.29 
Superior temporal gyrus (posterior) 22/39 52 −54 20 25.20 
Superior temporal gyrus (posterior) 42 59 −36 16 11.72 
Fusiform gyrus 19 −30 −81 −21 21.51 
Supramarginal gyrus 40 −56 −57 27 35.42 
Postcentral gyrus 43 −52 −17 18 17.31 
Postcentral gyrus 52 −23 53 12.71 
Posterior cingulate gyrus LR 23 −50 16 22.29 
Lingual gyrus 18 −77 −6 10.29 
Cuneus 18 19 −90 18 11.11 
Putamen  −19 −10 11 18.29 
Thalamus  22 −18 11 11.94 
Cerebellar hemisphere  −15 −52 −10 20.46 
Cerebellar hemisphere  11 −45 −23 15.80 
Cerebellar hemisphere  −11 −37 −20 12.35 
 
Young Age Group > Old Age Group 
Hippocampus  22 −8 −22 15.16 
Hippocampus  −22 −33 −8 9.91 
Middle frontal gyrus 30 24 33 10.88 
Supramarginal gyrus 40 −48 −50 27 30.95 
Supramarginal gyrus 40 48 −52 48 11.47 
Posterior cingulate gyrus LR 23 −50 16 22.29 
Precuneus 31 −11 −49 34 14.42 
Insula  −33 10 17.99 
Cerebellar hemisphere  −30 −52 −29 18.97 
Cerebellar hemisphere  −19 −48 −13 12.45 
 
Old Age Group > Young Age Group 
No significant activation 

R = right; L = left; LR = interhemisphere; BA = Brodmann's area.

Confirming our second prediction, RSA in the left ATL (anterior part of the superior temporal gyrus) region during the retrieval of people's names was greater than that during the retrieval of job titles, but there was no difference in activity between the young and older subjects (Figure 4). Other regions showing greater RSA for people's names than for job titles were found in the left inferior frontal gyrus and the right caudate nucleus (Table 4). When we compared RSA in these regions between the two age groups, we found neither a significant aging nor reverse aging effect of activity in any region (Table 4). A two-way ANOVA with factors of age (young vs. old) and task (N vs. J) for the left ATL region showed a significant main effect of task [F(1, 38) = 4.6, p < .05], but not a main effect of age [F(1, 38) = 0.2, ns] or of their interaction [F(1, 38) = 0.9, ns].

Figure 4. 

Image, effect sizes, and time courses of the ATL activations. The left ATL region showed greater activity during the successful retrieval of people's names than during that of job titles associated with faces, but there was no significant difference of activity in this region between young and older adults. *p < .05.

Figure 4. 

Image, effect sizes, and time courses of the ATL activations. The left ATL region showed greater activity during the successful retrieval of people's names than during that of job titles associated with faces, but there was no significant difference of activity in this region between young and older adults. *p < .05.

Table 4. 

Regions Showing Greater Activity in the Successful Retrieval of People's Names than in That of Job Titles

Regions
L/R
BA
Coordinates
F
x
y
z
Common to Both Young and Old Age Groups 
Superior temporal gyrus (anterior) 38 −37 −22 6.11 
Inferior frontal gyrus 45 −41 26 16 6.70 
Caudate nucleus (tail) 26 −32 15 7.02 
 
Young Age Group > Old Age Group 
No significant activation 
 
Old Age Group > Young Age Group 
No significant activation 
Regions
L/R
BA
Coordinates
F
x
y
z
Common to Both Young and Old Age Groups 
Superior temporal gyrus (anterior) 38 −37 −22 6.11 
Inferior frontal gyrus 45 −41 26 16 6.70 
Caudate nucleus (tail) 26 −32 15 7.02 
 
Young Age Group > Old Age Group 
No significant activation 
 
Old Age Group > Young Age Group 
No significant activation 

R = right; L = left; BA = Brodmann's area.

Confirming our third prediction, functional connectivity between the hippocampal (left: x = −22, y = −33, z = −8; right: x = 22, y = −8, z = −22) and left ATL (x = −37, y = 6, z = −22) regions, which were identified in the prior analyses, was enhanced in the young adults, compared to the older adults (Table 5). We computed hippocampus–ATL correlations of individual trial activity during the retrieval of people's names and job titles in each of the young and older age groups (Figure 5), and compared correlation coefficients between these age groups. All positive correlations between the hippocampal and ATL regions were statistically significant (p < .001) for retrieval trials in the young group (left hippocampus–left ATL: r = .207; right hippocampus–left ATL: r = .110; data points: 4320) and older group (left hippocampus–left ATL: r = .138; right hippocampus–left ATL: r = .042; data points: 4665), and the difference between young and older subjects was significant for the left hippocampus–ATL correlation (p < .01) and the right hippocampus–ATL correlation (p < .01).

Table 5. 

Correlations between the Hippocampus (HIP) and the Anterior Temporal Lobe (ATL) in Young and Older Adults

Regions
Correlation Coefficient (r)
Z
Young (4320)
Old (4665)
L. HIP–L. ATL .207 .138 3.37* 
R. HIP–L. ATL .110 .042 3.24* 
Regions
Correlation Coefficient (r)
Z
Young (4320)
Old (4665)
L. HIP–L. ATL .207 .138 3.37* 
R. HIP–L. ATL .110 .042 3.24* 

L = left; R = right.

*p < .01.

Figure 5. 

Results of correlation analyses based on “individual trial activity” in young (circles and solid line) and older adults (crosses and dotted line). (A) Correlation between activities in the left hippocampus and the left ATL. (B) Correlation between activities in the right hippocampus and the left ATL.

Figure 5. 

Results of correlation analyses based on “individual trial activity” in young (circles and solid line) and older adults (crosses and dotted line). (A) Correlation between activities in the left hippocampus and the left ATL. (B) Correlation between activities in the right hippocampus and the left ATL.

DISCUSSION

Three main findings emerged from the present study. First, successful retrieval activity in the hippocampus was identified in the retrieval of both people's names and job titles associated with faces, and the activity was greater for young than for older subjects. Second, successful retrieval activity in the left ATL region was greater during the retrieval of face–name associations than of face–job title associations. However, there was no significant difference of activity between young and older adults in this region. Third, functional connectivity between the hippocampus and the left ATL was significantly higher in young than in older adults.

Before discussing each of these findings, we should comment a potential artifact by almost chance-level task performance for the people's name retrieval in older adults. In this study, older adults showed 52.5% accuracy in the retrieval of people's names. The lower performance in older adults implies that hippocampal and ATL activations identified in our study may be raised by the “lucky guesses” rather than the hit responses in older adults. However, we did not find a specific pattern of hippocampal and ATL activations in the retrieval of people's names by older adults, hence, the chance-level task performance for the people's name retrieval in older adults could not be directly reflected in the present findings of hippocampal and ATL activations, which showed no significant interaction between age and task factors. Thus, here we discuss these three main findings without considering the potential artifact.

Activity in the Hippocampus

The first main finding of our study was that the hippocampus was significantly activated during the retrieval of both people's names and job titles associated with faces, and the activity showed an age-related decrease in both tasks. These findings suggest that the hippocampus could contribute to the successful retrieval of relational memory, and the activity could be modulated by aging.

Activation of the hippocampus in the successful retrieval of memory for face–name and face–job title associations is consistent with functional neuroimaging evidence linking this region to the retrieval of relational memory within a visual or verbal modality (Meltzer & Constable, 2005; Prince et al., 2005; Bunge et al., 2004; Giovanello et al., 2004), as well as between different modalities such as face–name associations (Tsukiura et al., 2008; Kirwan & Stark, 2004; Zeineh et al., 2003; Small et al., 2001). This view of the hippocampal contribution to relational memory retrieval is supported by a substantial amount of neuropsychological evidence that hippocampal lesions produce greater deficits in relational memory but not in memory for a single item (Brown & Aggleton, 2001; Aggleton & Brown, 1999). Likewise, a recent neuropsychological study found that an amnesic patient with a medial temporal lobe lesion including the hippocampus was impaired in associative recognition but preserved in single-item recognition for remote autobiographical and public events (Tsukiura et al., 2003). The present result of hippocampal activations during the successful retrieval of relational memory for face–name and face–job title associations extends the previous findings by demonstrating hippocampal activations in both different word categories of people's names and job titles associated with faces.

Moreover, the present data show that hippocampal activity during the successful retrieval of memory for face–name and face–job title associations was greater in young adults than in older adults. The age-related decrease of hippocampal activity during the retrieval of relational memory is consistent with the results of previous neuroimaging studies (for a review, see Cabeza, 2006). For example, fMRI studies found that age-related decline of the recollection process, which is related to the recovery of specific contextual information associated with a study item, was caused by an age-related decrease of activity in the hippocampus (Daselaar et al., 2006; Cabeza et al., 2004). The aging effect on recollection-related hippocampal activity is supported by psychological findings, which have shown that older adults tend to be impaired in recollection but not in familiarity (Searcy et al., 1999; Java, 1996; Jennings & Jacoby, 1993; Parkin & Walter, 1992). In addition, a recent fMRI study demonstrated that older adults showed weaker activity in the hippocampus than young adults during the retrieval of true memory, whereas no age-related difference of hippocampal activity was identified during the retrieval of false memory (Dennis, Kim, & Cabeza, 2008). In the present study, compared to young adults, older adults showed weaker activity in the hippocampus and worse retrieval performance during the successful retrieval of relational memory for both face–name and face–job title associations, but there was no significant difference in hippocampal activity and retrieval performance between two retrieval tasks of people's names and job titles from faces. Therefore, hippocampal activity during the retrieval of relational memory could be negatively affected by age, and the age-related decrease of activity in this region could cause an age-related decline in the retrieval process of true relational memories.

Activity in the Left Anterior Temporal Lobe

The second main finding of our study was that the left ATL region showed greater activity during the successful retrieval of face–name associations than of face–job title associations, but there was no age-related difference of activity in this region. These findings suggest that the left ATL region could play a more important role in the successful retrieval of people's names than of job titles associated with faces, but the contribution of this region might not be affected by age.

Involvement of the left ATL region in the retrieval of people's names associated with faces is consistent with functional neuroimaging evidence showing the importance of this region in the retrieval of people's names from faces or semantic information about people such as their job titles (Tsukiura et al., 2002, 2006, 2008; Damasio et al., 1996). For example, one fMRI study found greater activations in the left ATL region during the retrieval of face–name associations encoded with job titles than without them (Tsukiura et al., 2008). In addition, involvement of the left ATL region in the retrieval of memory for persons has been reported in neuropsychological studies involving brain-damaged patients (Tranel, 2006; Lah et al., 2004; Snowden et al., 2004; Glosser et al., 2003; Seidenberg et al., 2002; Tsukiura et al., 2002; Fukatsu et al., 1999; Papagno & Capitani, 1998; Damasio et al., 1996). One case study of a patient who had undergone left temporal lobectomy found that the patient was impaired in the retrieval of people's names from faces or job titles, but was preserved in the retrieval of job titles from faces (Fukatsu et al., 1999). Another patient study reported that patients with left-dominant atrophy of the ATL region showed impairment in the retrieval of job titles from people's names but not from faces (Snowden et al., 2004). Thus, the left ATL activation in our study would reflect a binding process between person-related semantic information such as job titles and phonological information about people's names during the successful retrieval of face–name associations.

Moreover, the present finding of no significant difference in activity in the left ATL region between young and older adults could provide neuroimaging evidence for psychological studies, in which difficulty retrieving people's names associated with faces is common between young and older adults. For example, one psychological study examined the retrieval performance of people's names and job titles associated with newly learned faces in young and older adults, and found that aging affected retrieval performance of both people's names and job titles, whereas there was no disproportionate age-related impairment during the retrieval of people's names in older adults (Rendell et al., 2005). The behavioral data from our study also showed the same patterns of retrieval performance, wherein the retrieval of people's names was more difficult than that of job titles in both age groups, and compared to young adults, older adults showed worse performance during the retrieval of both people's names and job titles. However, there was no difference in the pattern of retrieval performance between young and older adults. In other words, the process of retrieving people's names from newly learned faces is more difficult than that of retrieving job titles from faces, whereas the degree of difficulty is not affected by age. The present finding could explain previous psychological findings of no disproportionate loss of the ability to retrieve people's names in older adults by demonstrating that there is no specific decrease in left ATL activity during the retrieval of people's names in older adults.

Functional Connectivity between the Hippocampus and the Left Anterior Temporal Lobe

The third main finding of our study was that functional connectivity between the activities of the hippocampus and the left ATL region was significant during the retrieval of people's names and job titles associated with faces, and that the connectivity was greater in young than in older adults. These findings suggest that functional connectivity between the hippocampus and the left ATL region modulates the retrieval of relational memory for persons, and that this connectivity is affected by age.

Significant connectivity between the hippocampus and the left ATL region during the retrieval of relational memory for persons is consistent with neuroimaging evidence that the hippocampus shows intrinsic functional connectivity with distinct regions in lateral temporal cortex extending into the temporal pole (Kahn, Andrews-Hanna, Vincent, Snyder, & Buckner, 2008). In addition, functional connectivity between these regions is supported by a previous neuropsychological study, which reported that 3/4 of patients with hippocampal sclerosis showed temporal pole signal abnormality on fluid-attenuated inversion-recovery MR imaging (Carrete et al., 2007). White matter connections between the hippocampus and the ATL region have also been demonstrated using diffusion tensor imaging in humans (Thivard et al., 2005). The present finding, in which correlations between the hippocampus and the left ATL region were significant during the retrieval of relational memories for face–name and face–job title associations, extends previous findings by demonstrating that functional connectivity between these regions was still significant in both age groups of young and older adults.

Moreover, the present data show that functional connectivity between the hippocampus and the left ATL region was significantly enhanced in young adults compared to older adults. An age-related difference in functional connectivity between these regions could be the cause of common complaints of poor retrieval of people's names associated with faces in older adults. In previous psychological studies, in which older adults reported memory complaints using the diary technique, adults of different ages recorded memory failure over several days or weeks (Burke, Mackay, Worthley, & Wade, 1991; Cohen & Faulkner, 1986). For example, one diary study found that a group of older adults subjectively reported more blocks when trying to retrieve people's names than either a young or a middle-aged group (Cohen & Faulkner, 1986). Another study also found that older adults reported a greater incidence of tip-of-tongue states than did their younger counterparts, and that the age difference was greatest for proper names (Burke et al., 1991). The behavioral data from our study demonstrate that older adults showed an age-related decline of relational memory in both retrieval tasks of people's names and job titles (main effect of age), and difficulty retrieving people's names, compared to job titles, was observed in both young and older adults (main effect of task). However, the deficit of people's name retrieval was not disproportionate in the older adults (no interaction between age and task). The fMRI data showed greater activity in the hippocampus during the successful retrieval of relational memories in young than in older adults, whereas there was no difference in hippocampal activity between the two retrieval tasks of names and job titles (main effect of age). Also, there was a greater increase in left ATL activity in the successful retrieval of people's names than of job titles, but there was no difference in activity between the young and older adults (main effect of task). In both regions, no significant interaction was found between the two factors of retrieval task and age. Thus, these activation patterns in the hippocampus and the left ATL region could explain the objective scores of behavioral data in our study. However, when we interviewed the older subjects who participated in our study, they also perceived themselves as having subjective difficulty retrieving people's names associated with faces, as found in previous psychological studies. Therefore, lower functional connectivity between the hippocampus and the left ATL region in older adults could lead to a subjective perception of difficulty retrieving people's names associated with faces.

Activity in Other Regions

As an age-related decrease of hippocampal RSA, our study demonstrated that activities in several regions were significantly decreased by the effect of aging. One important region showing the age-related decrease in activity was the right middle frontal gyrus. The age-related decrease in the right prefrontal activity is consistent with functional neuroimaging evidence showing greater activity of this region in young than in older adults during the retrieval of relational memories (for a review, see Cabeza, 2006). For example, fMRI studies have reported that activity in the right prefrontal cortices was smaller in older adults than in young adults during the retrieval of semantic relational memories (Cabeza et al., 1997) or of temporal-order relational ones (Cabeza, Anderson, Houle, Mangels, & Nyberg, 2000). The age-related decrease in the right prefrontal activity fits well with the concept of the “frontal lobe ageing hypothesis” (for a review, see West, 1996; Moscovitch & Winocur, 1995), in which age-related cognitive deficits are mainly caused by the prefrontal cortex dysfunction. However, previous functional neuroimaging studies for the retrieval process of relational memories have found an age-related increase of activity in left prefrontal cortex as well as an age-related decrease of activity in right prefrontal cortex (Cabeza et al., 1997, 2000). The left prefrontal activation in older adults is explained by some compensatory mechanism for the retrieval of relational memories. In the present study, older adults did not show greater activity in left prefrontal cortex than young adults. The present finding suggests that the compensatory mechanism in our paradigm could work less efficiently than that in previous fMRI studies.

Another region showing an age-related decrease of activity was identified in the bilateral supramarginal gyri. The activation pattern in our study was consistent with functional neuroimaging evidence showing reduced recollection-related activations of the parieto-temporal regions in older adults compared to young adults (Daselaar et al., 2006). The aging effect on this region could be explained by the anatomical connections of this region with the hippocampus (Daselaar et al., 2006). Previous studies for macaques have demonstrated that the location of region 7a, which corresponds to the recollection-related parieto-temporal areas in human, maintains the strong reciprocal connection to the hippocampus (Clower, West, Lynch, & Strick, 2001; Suzuki & Amaral, 1994). This anatomical connection suggests that the age-related decrease of supramarginal activities in our study could be associated with the age-related decrease in the hippocampal activity, which is associated with the age-related decline of relational memories. The similar interpretation is also available in the posterior cingulate activity, in which we found weaker activity in older adults than in young adults (Kobayashi & Amaral, 2003). The age-related decrease of the supramarginal and posterior cingulate activity could modulate the age-related decline of relational memory retrieval by interacting with hippocampal activity.

Conclusion

Using event-related fMRI, we investigated the effect of aging on the successful retrieval of people's names and job titles associated with faces. Consistent with past research, the hippocampus was significantly activated in the successful retrieval of relational memories for both people's names and job titles associated with faces, and the activity significantly decreased with age. The left ATL region showed greater activity during the successful retrieval of people's names than of job titles associated with faces, whereas there was no difference in the activity in this region between young and older adults. Additionally, as shown by single-trial correlation analysis, functional connectivity between the hippocampus and the left ATL region during retrieving people's names and job titles associated with faces was significantly enhanced in young adults compared to older adults. Taken together, the results suggest that aging could differentially affect hippocampal and left ATL activations during the retrieval of people's names and job titles associated with faces, and functional connectivity between these regions could modulate the effect of aging on this memory. An age-related difference in hippocampal activity and hippocampus–ATL connectivity could contribute to the age-related decline of relational memories and to complaints of poor retrieval of people's names in older adults.

Acknowledgments

This study was supported by Grant-in-Aid for Scientific Research on Innovative Areas, “Face Perception and Recognition,” by the Ministry of Education, Science, Sports and Culture, Japan (21119503). Part of this study was also supported by Cosmetology Research Foundation and JST/RISTEX, JST/CREST.

Reprint requests should be sent to Takashi Tsukiura, Department of Functional Brain Imaging, Institute of Development, Aging and Cancer (IDAC), Tohoku University, Seiryo-machi 4-1, Aoba-ku, Sendai 980-8575, Japan, or via e-mail: t-tsukiura@idac.tohoku.ac.jp.

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