Experimental Aging Research, 32: 61–77, 2006

Copyright # Taylor & Francis Inc.

ISSN: 0361-073X print/1096-4657 online
DOI: 10.1080/03610730500326291

THE EFFECTS OF AGING ON THE RECOGNITION OF

DIFFERENT TYPES OF ASSOCIATIONS

Christine Bastin

Cognitive Psychopathology Unit, University of Liège, Liège, Belgium

Martial Van der Linden

Cognitive Psychopathology Unit, University of Liège, Liège, Belgium, and

Cognitive Psychopathology Unit, University of Geneva, Geneva, Switzerland

The present study examined how aging influences item and associative
recognition memory, and compared memory for two types of associations:
associations between the same kinds of information and associations
between different kinds of information. A group of young adults and a
group of older adults performed a forced-choice face recognition task
and two multitrial forced-choice associative recognition tasks, assessing
memory for face-face and face-spatial location associations. The results
showed disproportionate age-related decline of associative recognition
compared to intact item recognition. Moreover, aging affected both types
of associative tasks in the same way. The findings support an associative
deficit hypothesis (Naveh-Benjamin, Journal of Experimental Psycho-
logy: Learning, Memory and Cognition, 26, 1170–1187, 2000), which
attributes a substantial part of the age effect on episodic memory tasks
to difficulty with binding individual components into a cohesive memory
trace. This associative deficit seems to affect same-information associa-
tions, as well as different-information associations.

Received 28 December 2004; accepted 5 April 2005.

Christine Bastin is a postdoctoral scientific collaborator of the Belgium National Fund for
Research (F.N.R.S.).
Address correspondence to Christine Bastin, Cognitive Psychopathology Unit, University
of Liège, Boulevard du Rectorat, B33, B-4000 Liège (Sart-Tilman), Belgium. E-mail: Christine.
Bastin@ulg.ac.be
62 C. Bastin and M. Van der Linden

Changes in episodic memory are part of normal aging. However, it is

now well established that the age-related differences are not uniform
across all types of episodic memory tasks. Indeed, recognition mem-
ory is less affected by aging than recall (Craik & McDowd, 1987;
Nyberg et al., 2003; Whiting & Smith, 1997). Moreover, older adults
show better memory for items (e.g., words, pictures, unfamiliar faces)
than for contextual information, such as the modality of presen-
tation, the spatial location, the temporal context, or the source of
the information (Spencer & Raz, 1995). There is also evidence of
age-related differences in paired-associate learning tasks. For
example, compared to young adults, older participants recall less
associated words when cued with the first word of a pair and learned
the new associations more slowly than young participants. Moreover,
this difficulty is observed even when older participants learned the
individual components of the pairs prior to the paired-associate task
and were as good as young adults at free-recalling them (see Kausler,
1994, for a review).
In an effort to explain the effect of aging on episodic memory
tasks, some authors have suggested that this effect could partly result
from a difficulty to create and retrieve the associations between indi-
vidual pieces of information, such as two items or an item and its
context (Chalfonte & Johnson, 1996; Naveh-Benjamin, 2000). This
hypothesis, referred to as the associative deficit hypothesis (ADH;
Naveh-Benjamin, 2000), has been supported by several studies which
compared item and associative memory using recognition paradigms.
For example, in Chalfonte and Johnson’s (1996) study, young and
older adults were shown colored objects located within an array.
Older adults were as good as young adults at recognizing the objects,
but poorer at recognizing object-location and object-color associa-
tions. In addition, there was an effect of age on memory for the loca-
tions themselves, but not on memory for color information. Several
recent studies (Naveh-Benjamin, 2000; Naveh-Benjamin, Hussain,
Guez, & Bar-On, 2003; Naveh-Benjamin, Guez, Kilb, & Reedy,
2004; Castel & Craik, 2003) also demonstrated poorer associative
recognition memory compared to item recognition memory in aging.
Indeed, older participants showed greater difficulty recognizing asso-
ciations between items of the same type (e.g., words pairs, pairs of
pictures) than the items themselves (words and pictures). The same
pattern was found when comparing memory for intraitem asso-
ciations (the associations between words and the font in which
they are written) and memory for individual items (words and
fonts; Naveh-Benjamin, 2000, Experiment 3). Moreover, when older
participants could rely on preexisting associations (e.g., pairs of
Aging and Associative Memory 63

semantically related words) and thus did not need to learn new
links, their associative recognition performance was as good as that
of younger participants (Naveh-Benjamin, 2000, Experiment 4;
Naveh-Benjamin et al., 2003, Experiment 3). Finally, Naveh-
Benjamin et al. (2004) found that older adults demonstrated greater
difficulty with recognizing associations between different types of
information (face-name pairs) than with recognizing the individual
components (faces and names).
The purpose of the present study was to explore whether aging
affects associative recognition memory differently, depending on
the kind of associations that must be formed. More precisely, the
aim of this experiment was to compare the effect of age on recog-
nition of associations between information of the same type and on
recognition of associations between different types of information.
Previous works have indicated age-related differences on the recog-
nition of different kinds of associations (e.g., word-word, word-font,
face-name). But this was done in separate studies, so it was not
possible to determine whether aging disrupts one kind of associative
memory more than others. Therefore, we addressed the following
question within one experiment: does aging disrupt the encoding
and retrieval of all the kinds of associations similarly or can some
of them be more resistant to aging?
Concretely, in the present experiment, a group of young adults and
a group of older adults performed two associative recognition tasks.
One task tested memory for the associations between different kinds
of information (face-spatial location associations) and one task
assessed memory for the associations between information of the
same kind (face-face pairs). Moreover, these tasks used a multitrial
procedure (i.e., repeated exposure to the study material and repeated
test) in order to examine how quickly young and older adults learned
new associations. In addition, the two groups also performed an item
recognition (i.e., face recognition) task, so we could determine
whether a possible difficulty of older adults in associative memory
is disproportionate in contrast with item memory. Finally, to be able
to directly compare item and associative memory, we used the same
kind of test in all the tasks, namely a two-alternative forced-choice
recognition test (Chalfonte & Johnson, 1996; Naveh-Benjamin,
2000). The tasks were constructed after the procedure used in
the study by Vargha-Khadem, Gadian, Watkins, Connelly, Van
Paesschen, and Mishkin (1997), showing dissociation between
preserved recognition of items and same-information associations
and impaired recognition of different-information associations in
amnesic patients with damage limited to the hippocampus.
64 C. Bastin and M. Van der Linden

According to the ADH (Naveh-Benjamin, 2000), one would expect

older adults to show a disproportionate difficulty to encode and
recognize new associations, regardless of the components that must
be bound. However, different predictions could be made if one con-
siders that different types of associative memory can be distinguished,
depending on the processes they involve. Indeed, some authors
have proposed that same-information associations and different-
information associations may recruit distinct recognition processes
(Mayes et al., 2004; Mishkin, Vargha-Khadem, & Gadian, 1998;
Norman & O’Reilly, 2003; Vargha-Khadem et al., 1997). It is gener-
ally considered that recognition memory relies on at least two kinds
of processes: recollection of the contextual information about the
episode in which an item was encountered and familiarity, which is
merely knowing that an item occurred, without any recollection
(see Yonelinas, 2002, for a review of dual-process recognition mod-
els). As regards associative memory, Norman and O’Reilly (2003)
and Mayes et al. (2004) suggested that same-information associations
could be recognized on the basis of familiarity as well as recollection,
but that only recollection can discriminate between old and new
different-information associations. In that perspective, given that
aging affects recollection more than familiarity (e.g., Bastin & Van
der Linden, 2003; Clarys, Isingrini, & Gana, 2002; Jennings &
Jacoby, 1997; see Yonelinas, 2002, for a review), one would expect
age differences to be greater in different-information associative
memory (which depends on recollection) than in same-information
associative recognition (which could be supported by familiarity).

METHOD

Participants

A group of 25 young adults and a group of 25 older adults took part

in this experiment. There were 11 women and 14 men in each group.
The mean age was 25.88 years old (SD ¼ 2.09) for the young group
and 64.80 years old (SD ¼ 2.74) for the older group. The groups were
matched in terms of years of education (young group, 15.48
1.69;
older group, 15.44
1.56, t(48) ¼ 0.09, p > .93). On a vocabulary
test (Mill Hill, Part B, 33 items; Deltour, 1993), older adults per-
formed better than the young group (young group, 25.16
2.76;
older group, 26.96
1.81, t(48) ¼ 2.72, p < .01). None of the parti-
cipants reported a neurological or a psychiatric condition that could
interfere with cognitive functioning. In addition, all the older parti-
cipants claimed being in good health and having good hearing and
Aging and Associative Memory 65

vision or appropriate correction for visual or auditory disorders when

necessary.

Materials and Procedure

The stimuli were 72 black-and-white photographs of unfamiliar faces,

representing men between 20 and 50 years old. No face had any
distinctive feature, such as a beard, a moustache, glasses, a scar,
baldness, or long hair. No background and no item of clothing were
visible. The photographs of faces were presented via a personal
computer. Each face was around 7 cm10 cm. The stimuli were semi-
randomly divided into three subsets of faces in order to create
three tasks, keeping the age range of the faces (20 to 50 years old)
equivalent between the subsets.1 There were two associative
recognition tasks (face-face associations and face-spatial location
associations) and one item (face) recognition task.
Participants were tested individually. The tasks were administered
during separate sessions with a delay of at least 24 h between each
task. In each group, the order of presentation of the tasks was differ-
ent for each participant, but the various sequences of presentation
were identical in all groups. In other words, each order was proposed
to one young adult and one older adult.

Associative Recognition
In each associative recognition task, the study-test sequence was
repeated until the participants obtained at least 11 correct responses
out of 12 or had received a maximum of 10 study-test trials. Each
study-test sequence was separated by a 30-s-long visuomotor distract-
ing task (drawing a cross in squares following a route), which also
served during the retention interval between study and test.

Face-Face Associations
In this task assessing recognition memory for associations between
stimuli of the same type, the participants saw 12 pairs of faces for
3 s each. They were instructed to try and remember the faces and their
association. After the visuomotor distracting task (for 30 s), the test
phase began. The test contained 12 test trials. A trial consisted in
the presentation of three faces. One face appeared on the top of the
1
Although the subsets of faces were not rotated among the tasks, the same pool of faces has
been previously used in recognition tasks that included a counterbalancing of the material
(Bastin & Van der Linden, 2003) and no item effect was found.
66 C. Bastin and M. Van der Linden

screen and two faces on the bottom. All the faces had been presented,
but only one of the bottom faces was associated with the top face.
The participants were asked to indicate whether the face previously
associated with the face on the top was the right or the left one.

Face-Spatial Location Associations

During the study phase of this task evaluating recognition of associa-
tions between different types of stimuli, 12 photographs of faces were
presented for 3 s each in one of the four corners of the computer
screen. By the end of the study list, each corner had been occupied
by three different faces. The participants were asked to try and
remember the faces and their spatial locations. After the presentation
of the 12 faces, the participants performed the visuomotor distracting
task for 30 s. Then they were presented with the test phase. There
were 12 test trials, each consisting of two faces (that had both been
previously presented) and a marker (a large black dot) in one corner
of the screen. The instruction was to indicate which of the two faces
had been presented in the corner designated by the marker.
Previous studies examining associative memory have compared
memory for the associations to memory for each of the individual
components (Chalfonte & Johnson, 1996; Naveh-Benjamin, 2000;
Naveh-Benjamin et al., 2003, 2004). Here we tested memory for faces
alone by means of a forced-choice recognition task (see below), but
we did not include a task assessing memory for the spatial location
itself because, in the present task, the demand associated with this
component is reduced. Indeed, as all the possible locations were actu-
ally occupied, it was not necessary for the participants to remember
which location was occupied and which one was not.

Forced-Choice Item Recognition

During the study phase of this task, 18 faces were presented one at a
time. Each face remained 1.5 s on the computer screen. Participants
were instructed to study the faces. Following a 30-s retention interval
during which the participants performed the same visuomotor dis-
tracting task as in the associative tasks (drawing a cross in squares
following a route), 18 pairs of faces, consisting of a target and a dis-
tractor, were presented. The two faces were side by side. Participants
had to say which one they had studied.
The purpose of this one-trial item recognition task was to give indi-
cation about how good item memory would be after one presentation
of the stimuli in the two associative tasks. To do so, isolated faces
(rather than associations) were presented under conditions that we
Aging and Associative Memory 67

tried to keep close to the conditions of encoding of item information

in the associative tasks. For instance, the presentation rate was
reduced for item recognition compared to associative recognition,
assuming that participants needed more time to encode two pieces
of information and their associations than one piece of information.
In addition, the number of stimuli was set following pilot work trying
to avoid ceiling effects, while remaining close to the number of stimuli
in the other tasks.

RESULTS

For each group, we calculated the mean proportion of correct

responses in the forced-choice item recognition task. In the two
associative recognition tasks, we computed in each group, the mean
proportion of correct responses obtained after one presentation of
the study items, the number of study-test sequences necessary to
reach the criterion (i.e., at least 11 correct responses out of 12),
and the slope of the learning curve. These scores are presented in
Table 1 and the learning curves in the associative tasks are shown
in Figure 1.
A 2 (age group)  3 (task) analysis of variance (ANOVA) was
conducted on the proportions of correct responses after one pre-
sentation of the stimuli. It indicated a main effect of age group,
F(1, 48) ¼ 12.82, p < .01: young adults performed globally better
than older adults. The main effect of task was also significant,

Table 1. Mean performance (and standard deviations) obtained by the young

and older participants in the item and associative recognition tasks
Young group Older group

M SD M SD

Item recognitiona .93 .07 .93 .06

Associative recognition
Face-face
1st sequencea .69 .12 .60 .14
Sequencesb 3.72 0.74 5.12 1.05
Slope 1.30 0.58 1.06y 0.52
Face-location
1st sequencea .69 .13 .56 .10
Sequencesb 2.84 0.75 5.00 1.47
Slope 2.01 0.99 1.34 1.27

Note.  p < .05;  p < .01; y p < .09; aproportion of correct responses; bnumber of study-test
sequences necessary to achieve the criterion of at least 11 correct responses out of 12.
68 C. Bastin and M. Van der Linden

Figure 1. Young and older groups’ learning curves and regression lines in
the face-spatial location and face-face recognition tasks.

F(2, 96) ¼ 130.57, p < .01. Performance was the best in the item
recognition task. The scores in this task were significantly better than
those in the face-spatial location and face-face associative recognition
task (ps < .01). Performance did not differ between these last two
(p > .28). The age group by task interaction was also significant,
Aging and Associative Memory 69

F(2, 96) ¼ 5.17, p < .01. This was due to the fact that the effect of
aging on the performance differed as a function of the task. There
was no age difference on the item recognition task, F(1, 48) ¼ 0.05,
p > .81, but there was an effect of age on the face-spatial location task,
F(1, 48) ¼ 14.11, p < .01, and on the face-face task, F(1, 48) ¼ 5.83,
p < .05. Moreover, in each group, the effect of the task was similar:
young as well as older participants performed better on the item recog-
nition task than on the associative tasks. In both groups, performance
did not differ between the face-face and face-spatial location tasks
(young: F(1, 48) ¼ 0.05, p > .82; old: F(1, 48) ¼ 1.71, p > .19).
In the associative tasks, the ability to learn the new associations
rapidly could be indexed by the number of study-test sequences that
were necessary to achieve the criterion of at least 11 correct responses
out of 12 and by the slope of the learning curve (see Table 1). An
ANOVA on the number of study-test sequences to criterion was per-
formed with age group (young versus old) as between-subject variable
and task (face-location and face-face) as within-subject variable.
Older participants needed more sequences than young adults to reach
the criterion, F(1, 48) ¼ 59.04, p < .01. Moreover, the effect of task
was significant, F(1, 48) ¼ 7.38, p < .01. The criterion was reached
more rapidly in the face-spatial location task than in the face-face
task. The interaction was not significant, F(1, 48) ¼ 4.26, p > .11.
As for the slope of the learning curve, an ANOVA with age group
and task (the two associative tasks) indicated that older adults
learned the associations more slowly than young adults did,
F(1, 47) ¼ 5.08, p < .05. Moreover, the slope of the learning curve
differed between the tasks, F(1, 47) ¼ 10.49, p < .01, with steeper
progression in the face-spatial location task than in the face-face task.
The interaction was not significant, F(1, 47) ¼ 1.85, p > .18. Finally,
visual inspection of the learning curves presented in Figure 1 suggests
that both groups showed linear improvement across trials in both
associative tasks. The linear regression lines for the recognition scores
as a function of trials were statistically significant in each group and
in each task, and were very similar between the groups and tasks
(young group: face-spatial location task, r2 ¼ 0.93, F(1, 3) ¼ 18.48,
p < .05; face-face task, r2 ¼ 0.96, F(1, 4) ¼ 43.87, p < .01; older
group: face-spatial location task, r2 ¼ 0.93, F(1, 8) ¼ 50.02, p < .01;
face-face task, r2 ¼ 0.97, F(1, 6) ¼ 117.46, p < .01).
Finally, in order to measure the size of the age effect, the point-
biserial correlations between the groups (the young group being
coded as 0 and the older group being coded as 1) and the scores on
the tasks (proportion of correct responses) were calculated, as
proposed by Cohen (1965). These correlations were .03 for the item
70 C. Bastin and M. Van der Linden

recognition task, .48 for the face-spatial location recognition task,

and .33 for the face-face recognition task. Cohen (1965) suggested
that a correlation of .20 reflects a small difference between the popu-
lation means, .40 a medium difference, and .60 a large difference. In
that perspective, one can consider that the age-related differences
were of small-to-medium size on face-face associative recognition,
and medium on face-spatial location recognition.

DISCUSSION

The goal of the present study was to examine whether the effect of
aging on associative memory differs as a function of the kind of asso-
ciations that must be formed. Globally, the results showed that older
participants demonstrated a disproportionate difficulty with the
recognition of associations compared to good item recognition.
Moreover, the effect of age was similar on the recognition of associa-
tions between different types of information (face-spatial location
associations) and on the recognition of associations between
information of the same type (face-face associations).
The finding of poor associative memory in the face of intact item
recognition is consistent with previous studies that indicated that
aging has differential effect on memory for item and memory for
associations. Indeed, aging has little effect on item memory, but dis-
rupts more specifically memory for the relationships between items,
or for the relationships between an item and its context (Chalfonte
& Johnson, 1996; Naveh-Benjamin, 2000; Spencer & Raz, 1995).
Moreover, the present results showed that not only did older parti-
cipants perform poorly on associative memory after one presentation
of the study material, but they also learned the new associations more
slowly than did younger participants. This confirms, and extends to
recognition memory, the age-related slower rate of learning found
on paired-associate cued-recall tasks (see Kausler, 1994, for a review).
Importantly, aging appeared to affect the recognition of associa-
tions between information of the same type as much as the recog-
nition of associations between different types of information.
Indeed, the ANOVAs showed that older adults’ proportion of correct
responses did not differ between the face-face associative task and the
face-spatial location associative task, as was also the case in the
young group.
Before concluding that the type of associations that must be
formed does not influence the effect of age on associative memory,
one must consider potential limits of the present study. First, one
potential confounding factor in the comparison between the two
Aging and Associative Memory 71

associative tasks is related to differences in the mapping of the asso-

ciations across the tasks. Whereas the face-face recognition task pro-
vided a one-to-one mapping (i.e., 12 different faces were paired with
12 other faces), the face-spatial location recognition task required a
many-to-one mapping (i.e., each spatial location was associated with
three different faces). It may be that, in the latter task, the effect of
aging on associative memory was due to a greater sensitivity to inter-
ference effects arising because each location was associated with
several items (cue overload effect). However, Schacter, Osowiecki,
Kaszniak, Kihlstrom, and Valdiserri (1994) showed that the age-
related differences in source memory (i.e., a form of associative mem-
ory) cannot be attributed to cue overload. Therefore, in light of
Schacter et al.’s results, it is plausible that the poorer performance
of the older adults in the face-spatial location task resulted mainly
from a difficulty with associative processes, rather than from inter-
ference due to the many-to-one mapping. Nonetheless, it would be
useful to examine in future research whether the similar age-related
differences on face-face and face-spatial location observed here would
also be found if a one-to-one mapping was used in both tasks. To do
so, the face-spatial location task could be modified, so that each face
is located in a different part of an array, with some spatial locations
remaining empty.
Second, item recognition was assessed by means of a separate one-
trial recognition task, which differed in terms of number of stimuli
and presentation rate from the associative tasks. A more appropriate
approach would be to use associative tasks, assessing recognition of
each individual components (faces and spatial locations if one use
an array) and recognition of the associations following a single
encoding phase (Naveh-Benjamin, 2000). Nonetheless, even if the
present procedure was not optimal, our aim was to examine whether
item memory was good in young and older adults after one learning
trial and whether, in these conditions, associative information (in
both the face-face and the face-spatial location tasks) were learned
more slowly by older adults compared to young adults. The results
appear to be consistent with this idea.
Therefore, the present results are in accord with an associative defi-
cit hypothesis, which suggests that the age-related differences on epi-
sodic memory can be, at least partly, attributed to a difficulty in
forming and retrieving the links between single units of information,
no matter what type of information they are (Naveh-Benjamin, 2000;
Naveh-Benjamin et al., 2004). In contrast, our findings do not sup-
port the hypothesis that memory for same-information associations
is less affected by aging than memory for different-information
72 C. Bastin and M. Van der Linden

associations. This prediction was driven from the view of associative

memory, which proposes that associations involving different kinds
of information necessitate recollection-based recognition, whereas
associations between the same kinds of information can be supported
by familiarity-based recognition (Mayes et al., 2004; Norman &
O’Reilly, 2003). As recollection decreases more than familiarity in
aging, one could expect greater age-related differences on different-
information associative memory than on same-information asso-
ciative memory. It seems thus that the current data do not fit this
prediction. In the next part of Discussion, we will address the implica-
tions of the present results in terms of the processes that contribute to
associative memory and the effect of neuroanatomical age-related
changes on memory for associations.
From a functional point of view, the fact that memory for all the
kinds of associations declines similarly with increasing age may be
interpreted as evidence for a reliance of associative recognition mem-
ory on recollection. It is indeed plausible that young participants used
mainly recollection to recognize face-face and face-spatial location
associations. Older adults’ poorer recognition memory could be
due to a predominant use of familiarity, because of their important
decline of recollection (Bastin & Van der Linden, 2003; Clarys
et al., 2002; Jennings & Jacoby, 1997; see Yonelinas, 2002, for a
review). It appears thus that familiarity is not sufficient to support
good associative recognition memory, even when two stimuli of the
same kind must be merged. This comforts the idea that associative
recognition is recollection dependant, as indicated by some studies
(Hockley & Consoli, 1999; Yonelinas, 1997). For example, Hockley
and Consoli (1999) asked young participants to report their states
of awareness when recognizing single words or word pairs. They
found that the participants claimed to recollect associations more
often than single items, and reported a feeling of familiarity, without
any recollection, more often for single items than for associations.
Thus, the present findings do no support a general distinction
between same-information associations and different-information
associations in terms of their reliance on recollection and familiarity
processes, such as the one proposed by Mayes et al. (2004) and
Norman and O’Reilly (2003). Indeed, it may not be usually true that
same-information associative recognition can benefit from familiarity
processes, whereas different-information associative recognition
requires recollection processes. Nonetheless, it remains possible that
there may be particular conditions under which familiarity can
significantly contribute to associative recognition. According to
Yonelinas (Yonelinas, Kroll, & Soltani, 1999; Yonelinas, 2002), one
Aging and Associative Memory 73

such condition could be when the components of the associations are

unitized so that they are encoded as a coherent whole. One example
is provided by the recognition of the associations between facial
features. Yonelinas et al. (1999) conducted an experiment in which
participants studied faces, constructed by associating some external
features (e.g., hair, ears, head shape . . .) with some internal features
(e.g., eyes, nose, mouth . . .). At test, they had to discriminate between
studied faces and rearranged faces, composed of the internal features
belonging to one studied face combined with the external features of
another studied face. The results showed that when the faces were
studied and tested in an upright orientation, familiarity significantly
supported the recognition of the intraface associations. In contrast,
when the faces were presented in an upside down orientation,
intraface associative recognition was only supported by recollection.
This suggests that when faces are encoded holistically, as in the
upright condition (Searcy & Bartlett, 1996), assessments of famili-
arity can benefit to associative recognition, but this is not the case
when the faces are encoded as conjunction of separate features
(upside down condition). As for the present study, it is plausible that
the face-face and face-spatial location associations were not encoded
as a coherent whole, thus hindering the reliance of associative
recognition on familiarity. Future research should further examine
the conditions under which associative recognition memory can be
supported by familiarity. One would expect age-related differences
to be reduced under such conditions.
In terms of the neuroanatomical changes in aging, an age-related
dysfunction of the hippocampus (see Kensinger & Corkin, 2003;
Raz, 2000; Uylings & de Brabander, 2002, for reviews) may be partly
responsible for the difficulty of older adults to encode new associa-
tions. Indeed, several models of the hippocampal function have
proposed that this structure plays a crucial role in the binding
of the separate components of an episode into a cohesive memory
trace (Aggleton & Brown, 1999; Eichenbaum, Otto, & Cohen,
1994; Moscovitch, 1992, 1994; Squire, 1992). In contrast, item
memory may depend on the cortices surrounding the hippocampus
(Aggleton & Brown, 1999), in which age-related changes seem smaller
than in the hippocampus itself (Raz, 2000). Nevertheless, the associ-
ative memory performance of the older participants in the present
study does not follow the same pattern as the one observed in amne-
sic patients with hippocampal damage. Indeed, hippocampal patients
have been found to be more impaired on different-information
associative memory than on same-information associative memory
(Mayes et al., 2001, 2004; Vargha-Khadem et al., 1997), whereas
74 C. Bastin and M. Van der Linden

the current results indicates a similar effect of aging on the two types
of associative memory. This discrepancy suggests that age-related
hippocampal dysfunction is not the sole responsible for the difficulty
of older adults in associative memory. In fact, aging is also
accompanied by changes in other brain regions, especially in the pre-
frontal cortex (Kensinger & Corkin, 2003; Raz, 2000). It is widely
accepted that the prefrontal cortex is involved in cognitive control
processes. In the domain of episodic memory, the prefrontal cortex
has been related to strategic encoding and retrieval of episodes
(Buckner & Wheeler, 2001; Simons & Spiers, 2003). Therefore, due
to a dysfunction of the prefrontal regions, older adults’ decline in
associative memory may also stem from a difficulty to strategically
encode new associations and monitor their retrieval (Moscovitch &
Winocur, 1992), independently of the nature of the associations. Con-
sistently, Naveh-Benjamin (2000) found that the associative memory
difficulty of older adults was larger under intentional encoding than
under incidental encoding conditions. As the participants in the
present study were instructed to encode the associations in prep-
aration for an upcoming memory test, young participants may have
spontaneously develop strategies in order to help them bind the
separate components into a memory trace, whereas older participants
may have failed to do so (Glisky, Rubin, & Davidson, 2001).
Finally, some studies have suggested that individual differences in
neuropsychological function among older adults may lead to various
patterns of age-related decline in memory performance (Davidson &
Glisky, 2002; Glisky, Polster, & Routhiaux, 1995; Glisky et al., 2001).
For example, Davidson and Glisky (2002) showed that the effect of
aging on recollection and familiarity was related to the degree of
frontal and=or medial temporal lobe (MTL) dysfunction. More
precisely, they divided a group of older participants into subgroups
according to the performance on measures sensitive to frontal lobe
or MTL function. Recollection was found to be impaired in the
low-frontal-function subgroups and in the low-MTL-function sub-
groups, but not in older adults with high frontal or MTL function.
In contrast, familiarity was poor in the low-MTL-function subgroup
only. In this context, it would be interesting to examine whether the
presence of age-related differences in the different types of associative
recognition tasks is determined by individual differences in the MTL
or frontal function among older participants.
In summary, the present study found disproportionate age-related
differences on associative recognition memory compared to intact
item recognition memory. This difficulty of older participants in
associative memory was evidenced by poor recognition abilities after
Aging and Associative Memory 75

one presentation of the study pairs, and also by slower rate of learn-
ing of the new associations when these ones were repeatedly pre-
sented. Moreover, the type of information that must be bound did
not seem to influence the effect of age on associative memory. Indeed,
the results indicated similar age-related decline on memory for asso-
ciations between the same kinds of information and on memory for
associations between different kinds of information. Therefore, these
findings provide further support to the ADH, which suggested that
part of the effect of aging on episodic memory can be explained in
terms of a general difficulty with the creation and retrieval of links
between individual components.

REFERENCES

Aggleton, J. P. & Brown, M. W. (1999). Episodic memory, amnesia, and the

hippocampal-anterior thalamic axis. Behavioral and Brain Sciences, 22, 425–489.
Bastin, C. & Van der Linden, M. (2003). The contribution of recollection and fam-
iliarity to recognition memory: A study of the effects of test format and aging.
Neuropsychology, 17, 14–24.
Buckner, R. L. & Wheeler, M. E. (2001). The cognitive neuroscience of remember-
ing. Nature Neuroscience, 2, 624–634.
Castel, A. D. & Craik, F. I. M. (2003). The effects of aging and divided attention on
memory for item and associative information. Psychology and Aging, 18, 873–885.
Chalfonte, B. L. & Johnson, M. K. (1996). Feature memory and binding in young
and older adults. Memory and Cognition, 24, 403–416.
Clarys, D., Isingrini, M., & Gana, K. (2002). Mediators of age-related differences in
recollective experience in recognition memory. Acta Psychologica, 109, 315–329.
Cohen, J. (1965). Some statistical issues in psychological research. In B. B. Wolman
(Ed.), Handbook of clinical psychology (pp. 95–121). New York: McGraw-Hill.
Craik, F. I. M. & McDowd, J. M. (1987). Age differences in recall and recognition.
Journal of Experimental Psychology: Learning, Memory and Cognition, 13, 474–479.
Davidson, P. S. R. & Glisky, E. L. (2002). Neuropsychological correlates of recollec-
tion and familiarity in normal aging. Cognitive, Affective, and Behavioral Neu-
roscience, 2, 174–186.
Deltour, J. J. (1993). Echelle de vocabulaire de Mill Hill de J.C. Raven. Adaptation
française et normes compare´es du Mill Hill et du Standard Progressive Matrices
(PM 38). Manuel. Braine-le-Château: Editions l’Application des Techniques
Modernes.
Eichenbaum, H., Otto, T., & Cohen, N. J. (1994). Two functional components of the
hippocampal memory system. Behavioral and Brain Sciences, 17, 449–518.
Glisky, E. L., Polster, M. R., & Routhieaux, B. C. (1995). Double dissociation
between item and source memory. Neuropsychology, 9, 229–235.
Glisky, E. L., Rubin, S. R., & Davidson, P. S. R. (2001). Source memory on older
adults: An encoding or retrieval problem? Journal of Experimental Psychology:
Learning, Memory and Cognition, 27, 1131–1146.
76 C. Bastin and M. Van der Linden

Hockley, W. E. & Consoli, A. (1999). Familiarity and recollection in item and

associative recognition. Memory and Cognition, 27, 657–664.
Jennings, J. M. & Jacoby, L. L. (1997). An opposition procedure for detecting age-
related deficits in recollection: Telling effects of repetition. Psychology and Aging,
12, 352–361.
Kausler, D. H. (1994). Learning and memory in normal aging. London: Academic
Press.
Kensinger, E. A. & Corkin, S. (2003). Neural changes in aging. In L. Nadel (Ed.),
Encyclopedia of cognitive science (pp. 70–78). London: Macmillian.
Mayes, A. R., Isaac, C. L., Holdstock, J. S., Hunkin, N. M., Montaldi, D., Downes,
J. J., MacDonald, C., Cezayirli, E., & Roberts, J. N. (2001). Memory for single
items, word pairs and temporal order of different kinds in a patient with selective
hippocampal lesions. Cognitive Neuropsychology, 18, 97–123.
Mayes, A. R., Holdstock, J. S., Isaac, C. L., Montaldi, D., Grigor, J., Gummer, A.,
et al. (2004). Associative recognition in a patient with selective hippocampal
lesions and relatively normal item recognition. Hippocampus, 14, 763–784.
Mishkin, M., Vargha-Khadem, F., & Gadian, D. G. (1998). Amnesia and the organi-
zation of the hippocampal system. Hippocampus, 8, 212–216.
Moscovitch, M. (1992). Memory and working-with-memory: A component process
model based on modules and central systems. Journal of Cognitive Neuroscience,
4, 257–267.
Moscovitch, M. (1994). Memory and working with memory: Evaluation of a compo-
nent process model and comparisons with other models. In D. L. Schacter &
E. Tulving (Eds.), Memory systems 1994 (pp. 269–310). Cambridge, MA: The
MIT Press.
Moscovitch, M. & Winocur, G. (1992). The neuropsychology of memory and aging.
In F. I. M. Craik & T. A. Salthouse (Eds.), The handbook of aging and cognition
(pp. 315–372). Hillsdale, NJ: Lawrence Erlbaum Associates.
Naveh-Benjamin, M. (2000). Adult age differences in memory performance: Tests of
an associative deficit hypothesis. Journal of Experimental Psychology: Learning,
Memory and Cognition, 26, 1170–1187.
Naveh-Benjamin, M., Guez, J., Kilb, A., & Reedy, S. (2004). The associative
memory deficit of older adults: Further support using face-name associations.
Psychology and Aging, 19, 541–546.
Naveh-Benjamin, M., Hussain, Z., Guez, J., & Bar-On, M. (2003). Adult age differ-
ences in episodic memory: Further support for an associative-deficit hypothesis.
Journal of Experimental Psychology: Learning, Memory and Cognition, 29, 826–837.
Norman, K. A. & O’Reilly, R. C. (2003). Modeling hippocampal and neocortical
contributions to recognition memory: A complementary learning systems
approach. Psychological Review, 110, 611–646.
Nyberg, L., Maitland, S. B., Rönnlund, M., Bäckman, L., Dixon, R. A., Wahlin, A.,
et al. (2003). Selective adult age differences in an age-invariant multifactor model
of declarative memory. Psychology and Aging, 18, 149–160.
Raz, N. (2000). Aging of the brain and its impact on cognitive performance: Inte-
gration of structural and functional findings. In F. I. M. Craik & T. A. Salthouse
Aging and Associative Memory 77

(Eds.), The handbook of aging and cognition (2nd ed., pp. 1–90). Mahwah, NJ:
Lawrence Erlbaum Associates.
Schacter, D. L., Osowiecki, D., Kaszniak, A. W., Kihlstrom, J. F., & Valdiserri, M.
(1994). Source memory: Extending the boundaries of age-related deficits.
Psychology and Aging, 9, 81–89.
Searcy, J. H. & Bartlett, J. C. (1996). Inversion and processing of components and
spatial-relational information in faces. Journal of Experimental Psychology:
Human Perception and Performance, 22, 904–915.
Simons, J. S. & Spiers, H. J. (2003). Prefrontal and medial temporal lobe interac-
tions in long-term memory. Nature Reviews: Neuroscience, 4, 637–648.
Spencer, W. D. & Raz, N. (1995). Differential effects of aging on memory for con-
tent and context: A meta-analysis. Psychology and Aging, 10, 527–539.
Squire, L. R. (1992). Memory and the hippocampus: A synthesis from findings with
rats, monkeys, and humans. Psychological Review, 99, 195–231.
Uylings, H. B. M. & de Brabander, J. M. (2002). Neuronal changes in normal human
aging and Alzheimer’s disease. Brain and Cognition, 49, 268–276.
Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van Paesschen, W.,
& Mishkin, M. (1997). Differential effects of early hippocampal pathology on
episodic and semantic memory. Science, 277, 376–380.
Whiting, W. L. & Smith, A. D. (1997). Differential age-related processing limitations
in recall and recognition tasks. Psychology and Aging, 12, 216–224.
Yonelinas, A. P. (1997). Recognition memory ROCs for item and associative infor-
mation: The contribution of recollection and familiarity. Memory and Cognition,
25, 747–763.
Yonelinas, A. P. (2002). The nature of recollection and familiarity: A review of 30
years of research. Journal of Memory and Language, 46, 441–517.
Yonelinas, A. P., Kroll, N. E. A., & Soltani, M. (1999). Recognition memory for
faces: When familiarity supports associative recognition judgments. Psychonomic
Bulletin and Review, 6, 654–661.