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Aging Reduces Veridical Remembering But Increases False Remembering: Neuropsychological Test Correlates of Remember-Know Judgments

Aging and false memory
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39 views10 pages

Aging Reduces Veridical Remembering But Increases False Remembering: Neuropsychological Test Correlates of Remember-Know Judgments

Aging and false memory
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© © All Rights Reserved
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Neuropsychologia 47 (2009) 21642173

Contents lists available at ScienceDirect

Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Aging reduces veridical remembering but increases false remembering:


Neuropsychological test correlates of rememberknow judgments
David P. McCabe a, , Henry L. Roediger III b , Mark A. McDaniel b , David A. Balota b
a
b

Department of Psychology, Colorado State University, Fort Collins, CO 80523-1876, United States
Washington University in St. Louis, United States

a r t i c l e

i n f o

Article history:
Received 3 March 2008
Received in revised form 4 September 2008
Accepted 21 November 2008
Available online 30 November 2008
Keywords:
Human memory
Episodic memory
Cognitive aging
Rememberknow
Meta-analysis
Frontal functioning
Medial-temporal functioning
Signal detection

a b s t r a c t
In 1985 Tulving introduced the rememberknow procedure, whereby subjects are asked to distinguish
between memories that involve retrieval of contextual details (remembering) and memories that do not
(knowing). Several studies have been reported showing age-related declines in remember hits, which has
typically been interpreted as supporting dual-process theories of cognitive aging that align remembering
with a recollection process and knowing with a familiarity process. Less attention has been paid to remember false alarms, or their relation to age. We reviewed the literature examining aging and remember/know
judgments and show that age-related increases in remember false alarms, i.e., false remembering, are as
reliable as age-related decreases in remember hits, i.e., veridical remembering. Moreover, a meta-analysis
showed that the age effect size for remember hits and false alarms are similar, and larger than age effects
on know hits and false alarms. We also show that the neuropsychological correlates of remember hits
and false alarms differ. Neuropsychological tests of medial-temporal lobe functioning were related to
remember hits, but tests of frontal-lobe functioning and age were not. By contrast, age and frontal-lobe
functioning predicted unique variance in remember false alarms, but MTL functioning did not. We discuss
various explanations for these ndings and conclude that any comprehensive explanation of recollective
experience will need to account for the processes underlying both remember hits and false alarms.
2008 Elsevier Ltd. All rights reserved.

Endel Tulving has made greater contributions to the study


of retrieval processes than any other researcher. Tulving and
Pearlstone (1966) distinguished between information available in
memory (what is stored) and information that is accessible on a
particular test (what is retrievable with certain cues). Although
psychologists and neuroscientists would hope to determine all the
information that is stored or available in memory, no techniques
(psychological or physiological) can ever permit us to know for
sure. Rather, our techniques only permit us to know what information is accessible on a particular test, with a certain set of cues,
under specic encoding and retention conditions. The distinction
between availability and accessibility seems widely (if not universally) accepted in writings of cognitive psychologists, but it still has
not penetrated all scientic elds of memory. The primary method
of examining variations in accessibility is by changing retrieval
cues during the test, for example, comparing free and cued recall
(as in Tulving & Pearlstone, 1966). Certain types of cues greatly
increase accessibility relative to free recall (e.g., category names for
lists composed of category members), whereas other types of cues
that would seem to be valid ones (e.g., items from the list used to

Corresponding author. Tel.: +1 970 491 3018.


E-mail address: [email protected] (D.P. McCabe).
0028-3932/$ see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2008.11.025

cue other list items) can actually decrease accessibility (Slamecka,


1968).
In the 1970s Tulving continued to pioneer the study of retrieval
processes with a series of publications on the encoding specicity
principle (e.g., Tulving & Thomson, 1973; among many others).
Many experiments on encoding specicity involve the simultaneous manipulation of study conditions and test conditions. For
example, one may have two encoding conditions (say A and B). Then
test conditions are created such that one type of test is intended to
match or recreate the encoding of the A condition (call it test condition A ) and another test condition is intended to re-arouse the
encoding condition in B (test condition B ). In most experiments,
when the test condition matches the encoding condition (A and
A ; B and B ) performance is better than when the conditions mismatch (A and B ; B and A ). This outcome in many experiments
caused Tulving and his colleagues to introduce the encoding specicity principle. Stated in brief, the idea is that encoding consists
of certain features of an event being coded and represented in a
memory trace; retrieval cues are effective to the extent that features extracted from the cue match or complement those in the
trace (Tulving, 1983).
Another key contribution by Tulving to the study of retrieval
processes occurred in the 1980s. Students of memory typically measure accessibility through a variety of methods (e.g., free recall,

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

2165

Fig. 1. Number of citations for Tulving and Thomson (1973), Craik and Tulving (1975), Tulving and Schacter (1990) and Tulving (1985) plotted by year of citations..

cued recall, recognition), with the implicit assumption seeming


to be that the experience of retrieving a memory was much the
same in all cases (or at least researchers did not make distinctions). However, in an important paper in 1985, Tulving argued that
psychologists ought to study peoples reported phenomenological
experience while they retrieve events from memory. He argued that
there could be at least two types of experience, remembering and
knowing, and he developed a pioneering method to permit subjects to distinguish between the two states of conscious awareness
during retrieval. Subjects reported that a retrieved experience was
remembered if they could think back to the moment the experience occurred and recollect details of the event, or reported that
the experience was one that they knew if it had occurred in the
experiment but the precise moment of occurrence could not be
recalled.
As in other introspective techniques, instructions to the subjects matter greatly. Despite some disbelief from the scientic
public, researchers soon worked out good instructions that subjects could readily understand (Gardiner, 1988; Rajaram, 1993),
and a large body of research has now been conducted with the
remember/know procedure with generally consistent results (see
Gardiner, 2008, for a review).
Tulvings (1985) remember/know distinction certainly qualies
as a seminal contribution in experimental psychology by any standard, with the paper garnering 838 citations through the end of
2007. This paper is the fourth most cited of Tulvings journal articles,
with the three most cited papers being Tulving and Thomson (1973;
1470 total citations), Craik and Tulving (1975; 1463 total citations),
and Tulving and Schacter (1990; 1040 total citations). The citation
counts plotted by year (through 2007) for these three papers are
shown in Fig. 1. The gure makes clear that the three most highly
cited Tulving papers were very inuential very soon after publication and have been fairly constant in their inuence or have waned
a bit. However, the 1985 paper took some time after publication to
catch on. Part of the reason for this initial indifference to the paper
may have been that it was published in Canadian Psychology, which
has relatively few subscribers outside of Canada. It probably also
took Gardiners (1988) important replication and extension of Tulvings demonstration experiment to make the technique noticed.
At any rate, the R/K procedure has had a steadily increasing number of citations since the mid-1990s as researchers became more
interested in studying retrieval experience.
Another major reason for the popularity of the rememberknow
procedure is the identication of remembering and knowing with
distinct neural systems, or cognitive processes. Tulving (1985)
suggested that remembering involved retrieval from the episodic

memory system, whereas knowing reected retrieval from the


semantic memory system. More recently dual-process memory
theorists have aligned remembering with a recollection process and
knowing with a familiarity process1 .
1. False remembering
The majority of published studies using the rememberknow
paradigm have primarily been concerned with recollection of studied events. One major exception to this generalization is the study of
false memories for associatively related lures in the DRM paradigm
(Deese, 1959; Roediger & McDermott, 1995). Certainly one of the
most dramatic ndings in the false memory literature is that
lures such as sleep that are strongly related to studied items (bed,
rest, awake, tired, etc.) receive remember responses on recognition tests at levels that are often comparable to the hit rates for
studied items. Although many explanations have been proposed
for these high rates of false remembering for associatively related
items (e.g., Brainerd & Reyna, 2005; Lampinen, Meier, Arnal, &
Leding, 2005; Roediger, Watson, Gallo, & McDermott, 2001), less
attention has been paid to false remembering of ostensibly unrelated items on standard rememberknow tests, which is typically
low (e.g., 3% according to Gardiner, Ramponi, & RichardsonKlavehns, 2002 meta-analysis). Despite low levels of remember
false alarms for unrelated lures, researchers have recently demonstrated systematic effects of false remember responses to unrelated
distracters (e.g., response bias effects; Wixted & Stretch, 2004).
Moreover, it has been noted that the very existence of remember false alarms is problematic for most dual-process theories of
memory (Higham & Vokey, 2004; Wixted & Stretch, 2004), because
dual-process theorists have argued that new items cannot truly
be recollected because they were not actually studied (Eldridge,
Sarfatti, & Knowlton, 2002; Yonelinas, Kroll, Dobbins, Lazzara, &
Knight, 1998).
There are two possible solutions to the problem posed by
remember false alarms for dual-process theories of memory
(Higham & Vokey, 2004). One solution is to assume that either a
recollection or familiarity process can give rise to the experience of
subjective recollection, i.e., remembering. Thus, recollective experience as captured by remember judgments could be caused by a
recollection process or by strong feelings of familiarity. This idea

1
Because the distinction between systems and processes have blurred in recent
years, we will refer to systems and process theories collectively as dual-process
theories.

2166

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

has recently been incorporated into several strength-based dualprocess theories (e.g., Rotello, Macmillan, & Reeder, 2004; Wixted
& Stretch, 2004). Another possible solution, based on the notion
that memory judgments are attributional in nature (Jacoby, Kelley,
& Dywan, 1989), is to assume that recollective experience can be
cued by a test item regardless of whether it was studied, provided the item acts as an effective retrieval cue (cf., Tulving, 1974).
For example, false remembering might be caused by confusions
between test words and similar studied words (e.g., money was
studied and cash was on the test), but false remembering may also
result from source misattributions for items that are unrelated to
studied items, e.g., when a new item cues recollection of an extraexperimental event that is erroneously misattributed to the study
episode (McCabe & Geraci, in press). For example, imagine the word
trial was a lure on a rememberknow recognition test, and that trial
was also the clue for an answer in a crossword puzzle a subject had
completed that morning, prior to the experiment. The subject may
recollect thinking of synonyms or words related to trial, and misattribute that recollection to the study episode. Thus, according to this
source misattribution explanation of remember false alarms, these
responses reect source memory errors (cf., Roediger et al., 2001),
and these source confusions would be expected to increase with
age (Johnson, Hashtroudi, & Lindsay, 1993). This hypothesis is similar to a recent proposal by Dodson and colleagues (Dodson, Bawa,
& Slotnick, 2007; Dodson, Bawa, & Krueger, 2007), who have shown
that age-related source memory impairments can be explained by
misrecollection of sources, rather than declines in veridical recollection of sources.
2. A meta-analysis of age-related changes in
rememberknow hits and false alarms
It is well established that aging is related to declines in recollection of studied items as measured by so-called objective
measures, including source memory (Johnson et al., 1993) and
process dissociation estimates (Jennings & Jacoby, 1997). These
measures are corroborated by subjective experience measures, such
as memory characteristic questionnaires (Gallo & Roediger, 2003;
Mather, Henkel & Johnson, 1997) and remember responses using
the rememberknow paradigm (Bastin & Van der Linden, 2003;
Parkin & Walter, 1992). In most previous rememberknow studies
including older adults, the study has been motivated by dualprocess memory explanations; therefore, the studies have focused
on age difference in veridical remembering of studied items. However, because remember false alarms can be very informative with
respect to understanding the memory processes related to recollection (Higham & Vokey, 2004), a systematic examination of age
effects on false remembering could be informative with respect
to understanding the nature of recollection. It is unclear whether
aging typically inuences remember false alarms in the standard
remember/know paradigm, i.e., with unrelated lures, because these
data typically have not been considered theoretically relevant by
most authors, and thus, even when age differences in remember
false alarms are reported, they are typically not discussed.
In order to discover whether aging inuences false remembering
(in addition to veridical remembering) in standard remember/know recognition studies, we compared remember responses
for studied and new items, i.e., remember hits and false alarms,
for all published studies employing a standard (i.e., studied items
and unrelated lures) remember/know recognition test with healthy
younger and older adults. The average level of remember responses
for both the unrelated lures and studied items are reported in
Table 1. In all cases the values reported are raw percentages of
remember hits and false alarms out of the total number of studied items or lures (see Appendix A for more details regarding study
identication and inclusion criteria). As expected, the average level

of remembering for studied items for younger adults across the 27


studies (weighted for sample size) was greater for younger adults,
.542, than for older adults, .396. The robustness of this nding is
evinced by comparing the number of studies in which younger
adults show more remembering than older adults for studied items,
with 23 of the 27 studies conforming to this pattern (with the other
four showing the opposite pattern; Wilcoxon Signed Rank Z = 3.83,
p < .001). More germane for present purposes are the remember
false alarm data. Averaged across the 27 studies, older adults had
more than twice as many remember false alarms (.064) than did
younger adults (.025). Although this mean difference is small compared to the mean difference in veridical remembering, this nding
is quite reliable, with 25 of the 27 studies conforming to this pattern
(the other two were ties; Wilcoxon Signed Rank Z = 4.03, p < .0001).
A similar pattern was found for estimates of the proportion of
remember responses out of the number of items called old, i.e.,
R/(R + K), with weighted means of .66 for younger adults and .57 for
older adults for hits, and .25 for younger adults and .37 for older
adults for false alarms.
In order to better assess the overall magnitude of age differences in veridical and false remembering in published studies, we
conducted a meta-analysis of the studies that were included in
Table 1.2 As shown in Fig. 2, the absolute magnitude of the effect size
comparing older and younger adults remember response rates for
veridical remembering (d = .68) and false remembering (d = .61)
were similar, i.e., they were both in the medium-large range based
on Cohens (1988) criteria, and the magnitude of the 95% condence intervals overlapped (indicating that the effect size did not
differ; see Table 2). These data can be contrasted with the smaller
age effects for Know hits (d = .03) and false alarms (d = .36). Thus,
based on our review of the extant rememberknow literature, we
can conclude that age-related effects on knowing are small, but agerelated increases in false remembering are just as common, and just
as large, as age-related decreases in veridical remembering. This
remember mirror effect must be explained by any comprehensive
account of age-related changes in retrieval experience.
2.1. Neuropsychological correlates of age-related changes in
memory performance
Age-related declines in different indices of recollection, including source memory, process-dissociation estimates, and veridical
remembering, have been linked to age-related declines in medialtemporal lobe and frontal-lobe functioning (Glisky, Polster, &
Routhieaux, 1995; Glisky, Rubin, & Davidson, 2001; Henkel,
Johnson, & DeLeonardis, 1998; Prull, Dawes, Martin, Rosenberg,
& Light, 2006). Recent neuroanatomical and functional research
indicate that frontal and medial-temporal systems that support
memory function are affected by aging more than many other
brain areas (see Buckner, Head, & Lustig, 2006, for a review).
Moreover, a review of neuroimaging and patient data indicates
that both medial-temporal lobes and frontal lobes are related to
remembering (Skinner & Fernandes, 2007). These ndings are consistent with the component-process model of episodic memory
(Moscovitch, 1992; Moscovitch & Winocur, 1992), which proposes
that the medial-temporal lobes are responsible for binding during encoding and cue-dependent retrieval of episodic memories,
whereas the frontal lobes are involved in strategic aspects of both
encoding and retrieval (Wheeler, Stuss, & Tulving, 1997), which
includes specication of retrieval cues and post-retrieval monitoring, i.e., working with memory (Moscovitch & Winocur, 1992).

2
Because variability could not be assessed for four of the published studies these
were not included in the meta-analysis (see Appendix A for details).

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

2167

Table 1
Average percentage of remember and know hits and false alarms (FAs) in published studies using the rememberknow procedure with younger (YA) and older adults (OA).
Remember

Know

Hits

FAs

Hits

FAs

YA

OA

YA

OA

YA

OA

YA

OA

Parkin and Walter (1992; Expt 1)a


Parkin and Walter (1992; Expt 2)a
Mantyla (1993; Expt 1)
Mantyla (1993; Expt 2)
Perfect et al. (1995; Expt 1)
Perfect et al. (1995; Expt 2a; Shallow LOP)
Perfect et al. (1995; Expt 2a; Deep LOP)
Perfect et al. (1995; Expt 2b)
Norman and Schacter (1997; Expt 1; Explanation)
Norman and Schacter (1997; Expt 1; No Explanation)
Perfect and Dasgupta (1997)
Schacter, Koutstaal, Johnson, Gross, and Angell (1997; Expt 1; 3 repetitions)
Schacter et al. (1997; Expt 2)
Friedman and Trott (2000)a
Lvdn, Rnnlund, and Nilsson (2002)b
Clarys et al. (2002)b
Bastin and Van der Linden (2003)
Bunce (2003)c
Comblain, DArgembeau, Van der Linden, and Aldenhoff (2004)
DArgembeau and Van der Linden (2004)
Bunce and Macready (2005)
Duarte, Ranganath, and Trujillo (2006)
Prull et al. (2006)
Bugaiska et al. (2007)
Parks (2007)
Duarte et al. (2008)
Skinner and Fernandes (in press)

.52
.37
.54
.43
.53
.40
.68
.76
.54
.53
.74
.63
.55
.50
.77
.72
.40
.49
.57
.49
.55
.59
.58
.30
.41
.54
.35

.20
.12
.26
.24
.18
.34
.69
.25
.55
.51
.48
.47
.35
.43
.53
.52
.30
.38
.33
.40
.49
.53
.36
.18
.31
.59
.40

.00
.02
.05
.03
.05
.00
.01
.01
.01
.01
.02
.02
.05
.02
.02
.07
.04
.02
.01
.08
.00
.04
.02
.02
.01
.02
.03

.01
.02
.05
.05
.07
.03
.02
.03
.10
.05
.08
.03
.11
.06
.06
.10
.10
.02
.03
.15
.02
.10
.08
.03
.04
.08
.15

.24
.44
.12
.11
.13
.09
.15
.10
.05
.04
.22
.14
.16
.22
.15
.10
.14
.21
.09
.10
.22
.12
.14
.16
.15
.19
.21

.49
.59
.10
.19
.53
.20
.08
.39
.22
.21
.22
.15
.14
.23
.13
.33
.13
.42
.24
.22
.27
.17
.33
.29
.17
.26
.30

.03
.04
.02
.03
.05
.05
.01
.02
.07
.06
.05
.06
.17
.04
.05
.05
.11
.03
.04
.11
.01
.15
.07
.06
.10
.11
.11

.08
.06
.03
.04
.03
.05
.01
.08
.10
.06
.09
.06
.17
.06
.08
.09
.17
.04
.08
.17
.05
.17
.14
.07
.13
.17
.15

Mean
Mean weighted by sample size

.536
.542

.385
.396

.025
.025

.062
.064

.245
.260

.267
.258

.063
.064

.090
.096

a
b
c

This study was not included in the meta-analysis reported in Table 2 because effect sizes could not be calculated for remember hits or false alarms.
Weighted average of the two oldest groups.
Note that in OA Mean, combining high- and low-frontal groups (.023), was greater than the YA Mean (.016), though both round to .02.

Many researchers have adopted a neuropsychological test


approach to examining the relative contributions of medialtemporal and frontal brain functioning to age-related changes in
episodic memory (Butler, McDaniel, Dornburg, Price, & Roediger,
2004; Glisky et al., 1995, 2001; Henkel et al., 1998; Roediger
& McDaniel, 2007). The general approach has been to examine
whether there are different patterns of correlations between tests
of frontal-lobe and medial-temporal lobe functioning, and different
memory tasks or indices. For example, tests of medial-temporal
lobe functioning have been found to be related to item recognition but not source recognition, whereas the opposite was true for

frontal-lobe functioning (Glisky et al., 1995, 2001). More recently,


age-related increases in false recall and false recognition have been
shown to be related to frontal-lobe functioning, even when medialtemporal functioning was equivalent in the sample (Butler et al.,
2004; Dornburg & McDaniel, 2006; Roediger & McDaniel, 2007;
but see Balota et al., 1999).
The present study addresses the issue of age-related increase
in false remembering on standard remember/know tests, and
attempts to shed light on the neuropsychological test correlates
of veridical and false remembering. Two different remember/know
tests one in which subjects saw or heard words at study and the
other on which subjects read or generated words were completed
by each of over 200 subjects ranging in age from 18 to 90 years.
Additionally, several neuropsychological tests of FL and MTL functioning were administered. Our primary interest was in examining
whether the neuropsychological correlates of veridical and false
memory differed.

Table 2
Effect sizes for remember and know hits and false alarms in published studies
comparing younger adults (YA) and older adults (OA) using the rememberknow
paradigm.

Fig. 2. Weighted mean effect size for age group (older adult minus younger adult)
for remember and know hits and false alarms. Note that the effect size for remember
hits is negative, representing less remembering for older adults. Error bars represent
95% condence intervals.

Item and response type

YA, N

OA, N

95% CI

QW

LL

UL

Remember hits
Remember false alarms
Know hits
Know false alarms

24
24
24
24

674
674
674
674

711
711
711
711

.68
.61
.03
.36

.57
.50
.08
.26

.78
.72
.14
.47

100.17
32.52
147.18
30.34

k: # of studies; N: number of subjects; d: Cohens d (effect size); CI: condence


interval; LL: lower limit; UL: upper limit; QW : Cochrans Q.

2168

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

Table 3
Demographic characteristics and neuropsychological test performance.
Variable

Age group

Age, r

Younger

Middle-age

Older

N
Age
Age range
% females
Education (high school = 12)
Self-reported health (max = 5)
No. of medications
Shipley vocabulary (max = 40)

67
30.0 (7.5)
1842
61
15.3 (2.3)
4.3 (0.9)
0.9 (1.3)
33.0 (4.1)

67
53.6 (6.4)
4364
58
15.4 (2.5)
4.2 (0.8)
1.6 (1.7)
34.0 (3.6)

68
77.0 (6.8)
6590
57
15.0 (2.9)
4.1 (0.6)
3.0 (2.4)
34.5 (3.4)

.01
.09
.46
.20

Frontal-lobe functioning (FLF) tests


Backward digit span
Mental arithmetic
Mental control
Verbal uency (FAS)
Wisconsin card sorting
FLF composite

7.9 (2.5)
13.3 (2.8)
30.7 (4.2)
46.3 (11.3)
18.0 (7.3)
.39 (0.78)

8.0 (2.6)
14.0 (3.0)
29.0 (5.1)
42.3 (12.4)
24.9 (13.6)
.23 (0.96)

6.9 (2.2)
12.4 (3.0)
26.0 (5.2)
39.2 (10.5)
37.8 (16.1)
.62 (0.95)

.18
.11
.35
.18
.54
.39

Medial-temporal lobe functioning (MTLF) tests


Logical memory
Verbal paired associates
California verbal learning test
MTLF composite

32.6 (7.3)
23.4 (6.7)
8.2 (2.3)
.36 (1.03)

31.8 (6.6)
19.7 (9.2)
7.8 (1.8)
.17 (0.88)

28.9 (7.3)
16.5 (7.9)
6.4 (2.0)
.52 (0.87)

.22
.35
.22
.38

3. Method
3.1. Subjects
Subjects were 202 adults (120 females) aged 1890 from the
Saint Louis metropolitan area who participated in this study as part
of a larger study on aging and cognition (see McCabe, Roediger,
McDaniel, Balota, & Hambrick, submitted for publication, for more
details). Subjects were recruited from the Volunteers for Health participant pool which is maintained at the Washington University in
St. Louis School of Medicine for purposes of screening and matching
potential research participants with appropriate studies. Although
age was a continuous variable, for purposes of presentation age
was grouped in to three roughly equal numbers of subjects for
data presentation purposes. Demographic characteristics for each
of these groups are presented in Table 3. There were no signicant differences for age groups for percentage of female subjects
(59%), self-reported health (4.2), or number of years of education
(15.2; all Fs < 1.09). Age was positively correlated with the number
of medications participants took on a regular basis (r = .46), and with
Shipley vocabulary scores (r = .20; ps < .01). All subjects who were
included in the analysis had a minimum of high school education
and scored 26 or greater on the Mini Mental Status Exam (Folstein,
Folstein, & McHugh, 1975; see Section 4 for exclusion criteria).
3.2. General procedure
Participants were tested in two sessions, each lasting approximately 2.5 h. The rst session included the medial-temporal lobe
and frontal-lobe tests, while the second session included the
rememberknow recognition tests, vocabulary test, and demographic questionnaire. The sessions were at least one week apart,
but never more than three weeks apart. Other tests were included
that are not reported as part of this study (see McCabe et al.,
submitted for publication for details).
3.2.1. Frontal-lobe functioning
The frontal lobe (FL) functioning factor was based on ve measures (Glisky et al., 1995), each of which taxed working memory,
and has been shown to be related to the frontal lobes (e.g., see
Glisky & Kong, 2008, p. 818, for a review of evidence for the relation between these tests and functioning of the frontal lobes). These

tests included (1) the Wisconsin Card Sorting Test (WCST; Heaton,
1993; number of perseverative errors), (2) the verbal uency task
(using the letters F, A, and S; Thurstone, 1938), (3) Mental Arithmetic from the WAIS (Wechsler, 1997a), (4) Mental Control from
the WAIS (Wechsler, 1997a), and (5) Backward Digit Span from the
WMS-3 (Wechsler, 1997b).
3.2.2. Medial-temporal lobe functioning
The medial-temporal lobe (MTL) functioning factor was based
on three measures (Glisky et al., 1995), each of which requires cued
recall or free recall, which engage medial-temporal brain areas (see
Yonelinas et al., 2002). These included logical memory I (WMS3; Wechsler, 1997b), verbal paired associates I (WMS-3; Wechsler,
1997b), and the California verbal learning test (CVLT; list 1 recall;
Delis, Kramer, Kaplan, and Ober, 2000).
3.2.3. Rememberknow recognition tests
Two rememberknow recognition tests were completed by
each subject. The stimuli for the tests included a pool of 280
medium-frequency concrete nouns. Log word frequency based on
the Lund and Burgesss HAL (1996) 131 million word database varied between 6.3 and 12.3 (M = 8.7, S.D. = 1.0) according to the English
Lexicon Project database (Balota et al., 2007). Words ranged in
length from four to eight letters (M = 5.2, S.D. = 1.2), and were high
in concreteness (over 550 according to the MRC Psycholinguistic
Database; Wilson, 1988). All words were presented in 72-point Arial
font at the center of a 19-in. computer screen.
Half of the 280 words were randomly assigned to be used for
the readgenerate study-test condition (hereafter readgenerate
test) and the other half for seehear study-test condition (hereafter seehear test). The readgenerate test was completed about
an hour into the second session. For the readgenerate test subjects studied 80 words at a rate of one word every ve seconds.
Half of the words were read intact, and the other half were generated from an anagram, randomly intermixed. In order to identify a
word presented as an anagram subjects had to transpose two letters in the word that were underlined (e.g., SLIA). A practice phase
involved having subjects study and complete 10 anagrams by writing down the corresponding intact words on an answer sheet that
was provided. All subjects were able to do this perfectly.
After completing the study episode subjects completed two
tests, each of which included 20 words that had been read intact,

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

20 that had been generated from anagrams, and 20 new words. The
rst test was a source memory test in which subjects were asked
to determine, for each word, whether it had been read, generated,
or was new (results from that test were reported in Lyle, McCabe, &
Roediger, 2008, and will not be considered further here). For the second test, the rememberknow test, subjects were asked to decide
whether they had previously seen the word during the study period.
If they had not seen the word, they were instructed to press a key
marked N, to indicate the word was new. If they had seen the
word in the study list, they were instructed to judge whether the
word was recollected, in which case they pressed a key on the keyboard marked with an R, or if the word was studied but did not
include recollective details, they should press a key marked with a
K, to indicate that they know the word was presented. The term
recollect was used instead of remember because the word recollect
better describes the subjective experience of conscious recollection.
The difference between recollect and know responses was closely
based on the instructions by Rajaram (1993), and included examples of each dimension that could be used to provide a recollect
response, and detailed examples of recollect and know experiences
associated with normal daily activities.
The seehear study and test phase was the rst task completed
in the second session and was identical to the readgenerate test
with respect to materials and study and test procedures, except that
half the studied items were viewed on a computer screen, and half
were heard over headphones. Headphone volume was adjusted by
each subject while listening to a practice list prior to study. For the
seehear study list one word was presented every three seconds.
Subjects rst completed a source test determining whether they
heard or saw 40 studied and 20 new words, followed by the RK test
that included 40 different studied and new words.
4. Results
Results of statistical tests were signicant at p < .01, unless otherwise noted. Because age was a continuous variable, age correlations
are reported in addition to ANOVAs.
4.1. Neuropsychological test performance
There were age-related changes in performance on all of the
FL functioning tests except for mental arithmetic, though that difference was also in the expected direction (see Table 3). The FL
functioning composite score was computed by entering the ve
frontal tests into a principal component analysis, which created
a factor accounting for 48% of the variance in performance. The
factor loadings for each test were as follows: WCST: .63, verbal
uency: .60, mental arithmetic: .76, mental control: .76, backward
digit span: .70. There were also age-related changes in performance
on all of the MTL functioning tests. The MTL functioning composite score was computed in the same manner as the FL functioning
composite, which created a single factor accounting for 63% of the
variance in performance. The factor loadings for each test were as
follows: logical memory: .80, verbal paired associates: .81, CVLT:
.78. Each composite score is a z-score based on the tests comprising
that factor. The contribution of each test to the z-score is weighted
by the factor loading in the principal components analysis.
4.2. Recognition test performance
Table 4 displays the average percentage of remember and
know responses for studied and new items for each age group
for the readgenerate and seehear tests. We began our analyses
by examining whether there was a generation effect for remember and know responses (i.e., generated hits minus intact hits for
each response type). There was a generation effect for remember

2169

Table 4
Remembering and knowing.
Item and response types

Age group
Younger

Readgenerate test
Studied
Remember
Know
Overall

Middle

Older

age r

.39 (.02)
.36 (.02)
.75 (.02)

.40 (.03)
.36 (.03)
.76 (.02)

.37 (.02)
.39 (.03)
.75 (.02)

.02
.02
.00

.04 (.01)
.21 (.02)
.25 (.02)

.09 (.01)
.24 (.02)
.33 (.03)

.11 (.01)
.26 (.02)
.36 (.02)

.32*
.09
.23*

Recollection and familiarity estimates


1.62 (.08)
Recollection: Remember d
Familiarity: IRK
.60 (.03)

1.28 (.08)
.59 (.03)

.99 (.08)
.58 (.03)

.37*
.05

New
Remember
Know
Overall

Seehear test
Studied
Remember
Know
Overall

.31 (.02)
.35 (.02)
.66 (.02)

.31 (.02)
.34 (.02)
.65 (.02)

.29 (.02)
.37 (.03)
.66 (.02)

.04
.05
.01

New
Remember
Know
Overall

.02 (.01)
.17 (.02)
.20 (.02)

.05 (.01)
.23 (.02)
.28 (.03)

.09 (.02)
.19 (.02)
.28 (.02)

.27*
.06
.19*

Recollection and familiarity estimates


1.49 (.07)
Recollection: remember d
Familiarity: IRK
.52 (.02)

1.29 (.08)
.50 (.03)

.92 (.09)
.53 (.02)

.35*
.05

Indicates the correlation was signicant at p < .05.

responses, such that generated items received more remember responses (M = .45) than read items (M = .32), t(201) = 8.62,
but not for know responses (M = .38 for generated and .35 for
read), t(201) = 1.90. However, the generation effect for remember
responses was unrelated to age (r = .10). Because the generation
effect was not our primary interest in the current study, these data
will not be considered further.
As shown in Table 4, there was no age effect for know responses
for studied items or new items on the readgenerate test, but the
pattern differed for remember responses. As shown in Fig. 3 (Panel
A), collapsed across read and generated items, remember hits did
not differ as a function of age; by contrast, there was an age effect
for remember false alarms for new items (r = .32), indicating an agerelated increase in false remembering. Performance for remember
and know responses followed the same pattern for the seehear
condition, also shown in Table 4 and Fig. 3 (Panel B), with only the
remember false alarms for new items showing a relation to age
(r = .27).
4.3. Recollection and familiarity estimates
Recollection was estimated using remember d , i.e., by calculating the distance between the average of the remember
response distributions for studied and new items. Because data
indicate that remember responses are normally distributed (at
least under some circumstances; e.g., Rotello, Macmillan, Reeder,
& Wong, 2005), this estimate is likely more appropriate than
simply subtracting remember false alarms from remember hits
(Yonelinas, 2002) or using A (Bunce, 2003), each of which assumes
a rectangular distribution. Age was negatively correlated with Recollection for the readgenerate test (r = .37) and for the seehear
test (r = .35). Familiarity was estimated using the independence
rememberknow (IRK) procedure (i.e., know/(1 remember); see
Yonelinas, 2002, for details). The IRK estimates were uncorrelated
with age for the readgenerate and seehear tests. Thus, age was
related to Recollection but not Familiarity for both analyses, and

2170

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

and familiarity, age, FL functioning, and MTL functioning were all


correlated with recollection, following the opposite pattern of that
described for remember false alarms, but none of the predictors
was correlated with the IRK estimate.
4.5. Path model showing the effects of age, MTL, and FL
functioning on remember hits and false alarms

Fig. 3. Path analysis models examining the relation between (A) age, medialtemporal lobe functioning, frontal-lobe functioning, and remember hits and
remember false alarms, and (B) age, medial-temporal lobe functioning, frontal-lobe
functioning, and recollection. Note that solid lines indicate a signicant correlation,
dotted lines indicate a non-signicant correlation.

this was obviously driven by the age effects on false remembering because there was no age-related difference in hit remember
responses.
4.4. Correlations between neuropsychological test performance
and memory indices
Because the patterns of performance on the two memory measures were the same (see Table 4), and correlations did not differ,
we converted each measure to standardized scores and combined
them to create a single factor score for each subject. This composite
measure allowed better precision in computing regression models
and simplied presentation of the data.
Table 5 shows the correlations between age, FL functioning
and MTL functioning and each of the memory indices. For studied
items the only signicant correlation was between MTL functioning
and remember hits (r = .29), with better MTL functioning performance associated with more remember hits, whereas for new items
all three predictor variables were correlated with remember false
alarms. FL functioning and MTL functioning were both associated
with decreases in remember false alarms, whereas age was associated with an increase. FL functioning was associated with increases
in know false alarms as well. In terms of the estimates of recollection
Table 5
Correlation between age, frontal-lobe functioning (FLF) and medial-temporal lobe
functioning (MTLF) composite scores, and memory indices.
Measure

Age

Remember hits
Know hit
Remember false alarms
Know false alarms
Recollection (remember d )
Familiarity (IRK)

.03
.04
.34*
.08
.44*
.00

Indicates the correlation was signicant at p < .05.

FLF
.07
.12
.32*
.20*
.43*
.08

MTLF

We conducted path analyses in order to examine whether Age,


MTL functioning, and FL functioning accounted for unique variance in performance on remember hits, false alarms, or recollection
(remember d ). Model A, predicting remember hits and false alarms,
is shown in the top panel of Fig. 3. Age was negatively related to both
MTL and FL functioning, which were correlated with one another.
Of primary interest was the relation between MTL and FL functioning and remembering. MTL functioning was related to remember
hits, FL functioning was not. By contrast, FL functioning was related
to remember false alarms, but MTL functioning was not. Remember
hits and false alarms were also correlated with one another, which
is consistent with the notion that both of these measures share variance related to response criteria (see Wixted & Stretch, 2004). Age
also accounted for unique variance in remember false alarms, even
after controlling for MTL and FL functioning. Age was not related to
remember hits. This path was not included in the model because
there was no relation between these variables in the bivariate correlation (see Table 4) and inclusion of the path would have led to
model saturation (i.e., there would be zero degrees of freedom in
the model if that path were included).
Using a minimum criterion for acceptability of t as a CFI of
.90 (Hu & Bentler, 1995), and a RMSEA of <.10 (Browne & Cudeck,
1993), the t of Model A was good, 2 (1, N = 202) = 1.03, CFI = 1.00,
RMSEA = .013, p = .31). The overall age effect on remember hits was
.09, with a direct effect of .00 and an indirect effect of .09
(through MTL and FL functioning). The overall age effect on remember false alarms was .31, with a direct effect of .20 and an indirect
effect of .10. The nding that remember false alarms were related
to FL functioning and age, even after controlling for remember hits,
indicates that false remember responses were not simply the result
of changes in the response criterion. If remember false alarms were
simply a measure of response bias, as signal detection models of
remembering and knowing suggest (Butler et al., 2004; Wixted &
Stretch, 2004), then there should have been no unique variance
in false remember responses associated with other measures after
accounting for remember hits.
Model B, shown in the bottom panel of Fig. 3, is essentially identical to Model A, except that recollection (remember d ) was the
outcome measure, rather than remember hits and false alarms. This
model showed that both MTL and FL functioning were related to
Recollection. However, because the model was saturated, model
t statistics could not be computed. Nonetheless, the model offers
a graphical depiction of the intercorrelations between the variables, and shows that age, MTL functioning, and FL functioning,
all make signicant unique contributions to recollection. The overall age effect on recollection in the model was .43, with a direct
effect of .23, and an indirect effect of .21 (through MTL and FL
functioning).
5. General discussion

.29
.12
.24*
.10
.57*
.10

In the current study, we reported data from two remember


know tests administered to a life span sample of adults (aged
1890). The results from both tests, using similar materials but
different encoding tasks, were consistent in showing age-related
increases in false remembering (i.e., remember responses to new,
unstudied items) despite the fact that no age differences existed

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

in veridical remembering (i.e., remember responses for studied


items). Despite the lack of age differences for veridical remembering, performance on a battery of tasks related to medial-temporal
lobe functioning was positively correlated with veridical remembering. By contrast, false remembering was uniquely related to
age and frontal-lobe functioning, in addition to being related to
medial-temporal lobe functioning. Recollection (estimated using
d ) declined with age, and increased with medial-temporal lobe
functioning and frontal-lobe functioning, but Familiarity (estimated using the IRK procedure; Yonelinas, 2002) was not related
to age or neuropsychological functioning.
In our review of aging studies employing the rememberknow
paradigm, we found that both veridical and false remembering were
affected by age, such that aging decreases veridical remembering
and increases false remembering. In a sense, these data are not surprising, but the nding that the age effects are of similar magnitude
for veridical and false remembering is noteworthy, and perhaps
unexpected. Another noteworthy nding from the meta-analysis
is that the age effect on false remembering is larger than the age
effect on false knowing responses. This is unexpected because it is
commonly assumed that age-related increases in false alarms are
driven by an over-reliance on familiarity in older adults resulting
from declines in recollection (Buchler & Reder, 2007; Multhaup,
1995). However, the large age-related increase in false remembering coupled with the smaller age-related increase in false knowing
suggests that the typical age-related increase in false alarms is due
to older adults increased likelihood of experiencing recollection for
new, unstudied items (Jacoby, Bishara, Hessels, & Toth, 2005; Meade
& Roediger, 2006). This nding is consistent with recent suggestions
that age-related declines in memory performance are often related
to misrecollection of features of studied events, rather than familiarity in the absence of recollection of studied events (Dodson, Bawa,
& Krueger, 2007).

6. Neuropsychological correlates of veridical and false


remembering
The nding that remember hits and false alarms had different neuropsychological test correlates indicates that different
processes are involved in each type of response. Specically,
medial-temporal lobe functioning was the only variable included
in this study that was correlated with remember hits. This is
consistent with the idea that remember hits are dependent
on an associative, cue-dependent memory system (Moscovitch,
Fernandes, & Troyer, 2001). Interestingly, despite reasons to believe
that remember hits should also be related to frontal-lobe functioning (e.g., Wheeler et al., 1997), this relationship failed to
materialize in the present dataset (note though, that this lack of
relation is not anomalous; Bastin & Van der Linden, 2003; Bunce
& Macready, 2005; Perfect, Williams, & Anderton-Brown, 1995;
Perfect & Dasgupta, 1997; Prull et al., 2006). Based on this nding, we believe that there is an increased reliance on FL functioning
under conditions of uncertainty at retrieval. For example, if a new
item cues partial recollection of information from a context other
than the study episode, FL functioning is important to determine
whether that partial recollection arose from the study episode or
some other non-experimental context. In this respect, remember
false alarms appear to be particularly reliant on decision processes
engaged at retrieval, whereas remember hits are much more likely
to be based on information that is well bound to the study context,
perhaps overshadowing individual differences related to decision
processes, and therefore FL functioning, that might be involved.
Several related explanations exist for how the frontal lobes are
involved in retrieval. For example, some have argued that frontal
functioning is important for specifying retrieval cues and/or moni-

2171

toring the output of the medial-temporal lobe system (Moscovitch


& Winocur, 1992). With respect to understanding the role of frontallobe functioning in false remembering, it is important that retrieval
cues match the study context if subjective recollection (i.e., remembering) is to be accurate. If retrieval is not appropriately constrained
to the study episode (Jacoby et al., 2005; Tulving, 1983), new
items can elicit recollective responses that may inappropriately
be attributed to the study episode. This interpretation of the role
of FL functioning in remember false alarms is consistent with the
idea that these responses are source misattributions (McCabe &
Geraci, in press), such that they reect recollection of events from
an episode other than the study session, in addition to recollection of items from the study session (cf., Roediger & McDermott,
1995). The nding that false remembering was uniquely related
to frontal-lobe functioning and age underscores the importance of
false remembering, even for unrelated lures, as a target of theoretical investigation. Indeed, false remembering will need to be
explained by any comprehensive account of subjective recollection.
We also estimated recollection and familiarity processes from
the rememberknow paradigm based on the methods proposed by
Yonelinas (2002). The nding that neither age, nor neuropsychological functioning, was related to the IRK estimate of familiarity (or to
know hits for that matter) is consistent with the notion that knowing is related to familiarity-based responding, rather than reecting
controlled processing. Alternatively, recollection was related to
medial-temporal lobe functioning, frontal-lobe functioning, and
age, supporting the notion that control processes underlie remembering. We should note too that the same pattern of relations with
age and neuropsychological functioning was found for both recollection and false remembering, owing to the fact that the estimate of
recollection incorporates remember false alarms. Thus, in estimating recollection, it appears that remembering for studied items does
not give as accurate an estimate of the recollection process as does
an estimate based on remember hits and remember false alarms.
Because the lack of age differences in remember hits in the current study is an unusual nding, we next consider possible reasons
for this result. First, it is important to note that the levels of veridical
remembering were low in this study, as compared to other studies of aging and rememberknow judgments. Averaged across the
readgenerate and seehear tests the level of remember hits was
.35 for younger adults, and .33 for older adults. This level of remember hits is lower than remember hit rates for younger adults in 24
of the 27 studies reviewed in Table 1. Also note that the level of
remembering for older adults in the current study is not unusual
(.39, on average in the meta-analysis). Thus, our null age effect is
probably related to a suppression of conscious recollection in young
adults, rather than an enhancement of recollective experience for
older adults. Support for this idea comes from a consideration
of the relation between remember hits and age effect sizes from
the meta-analysis. There was a clear relation between the level of
younger adults remember hits and the age effect size, indicating
that for studies in which the level of younger adults remember hits
was lower, the magnitude of the age effect was smaller (r = .43,
p < .05; note that larger age effects are larger negative numbers).
By contrast, there was also a clear relation between older adults
remember hits and the magnitude of the age effect, but in the opposite direction (r = .49, p < .05). That is, for studies in which older
adults remember hits were lower, the magnitude of the age effect
was greater.
One possible reason that younger adults might have had lower
than average levels of remember hits in the current study is that
we used study lists that were longer than average (i.e., 80 words in
our experiments), and longer list lengths are associated with lower
levels of remembering in younger adults (cf., Cary & Reder, 2003).
Another possibility is that having the source memory test prior to
the rememberknow test somehow biased responding or changed

2172

D.P. McCabe et al. / Neuropsychologia 47 (2009) 21642173

retrieval strategies on the rememberknow test, though this seems


unlikely based on research with younger adults showing the order
of these tests has no effect on remembering and knowing (Wais,
Mickes, & Wixted, 2008). A third possible reason is that the younger
adults in this study were not college students, and thus, they may
not have been as well practiced at remembering large amounts of
information as younger adults in typical cognitive aging studies.
Regardless of the exact reason for our lack of age differences in
remember hits, a target for future research is to replicate the current
ndings using paradigms that reveal prototypical patterns of age
differences in both remember hits and false alarms.
7. Conclusions
Tulvings (1985) introduction of the rememberknow paradigm
has sparked considerable interest and debate among psychologists
and neuroscientists for over 20 years. The original theory proposed
remembering and knowing as states of consciousness associated
with distinct memory systems. We found some support for this
idea, at least with regard to remembering, because recollection was
correlated with medial-temporal lobe and frontal-lobe functioning.
However, familiarity (as derived from knowing) was uncorrelated
with neuropsychological test performance and age. The most noteworthy nding from the current study is that false remembering
was most closely associated with neuropsychological functioning
and age. Additionally, the meta-analysis of rememberknow judgments shows that age affects veridical and false remembering to a
similar degree, and more than it affects knowing. Indeed, the current study adds to the growing consensus that both veridical and
false recollection must be explained by any comprehensive theory
of memory.
Appendix A. Methodology for meta-analysis of remember
data from published studies
Published studies using the rememberknow procedure to
compare healthy younger and older adults were identied by
reviewing citations in existing papers, and by searching the
PsycINFO database. PsycINFO searches included the term aging
with remember and know, and aging with recollective, and
aging with recollection. The matches returned for these searches
were then inspected to determine whether the study included a
standard rememberknow recognition test and at least one group
of younger adults (under 45 years of age), and a group of older adults
(age 60 or older). The study was included in Table 1 if the percentage of remember responses was reported for both studied items
and new items (or could be computed), and the remember false
alarm rate was greater than zero for at least one age group. When
necessary, levels of remembering were estimated by visual inspection of gures. Remember response levels were averaged across
within-subject manipulations when necessary, and only responses
for unrelated lures were included.
Studies were included in the meta-analysis if they allowed an
estimation of effect sizes for remember responses for studied or
new items, either from standard deviations, standard errors, or F
or t values. In some cases these data were obtained by contacting
the authors directly if the necessary statistics were not reported.
We were able to obtain enough data to compute effect sizes for 24
of the 27 studies. Statistics for the effect size analysis are included
in Table 2. There was substantial heterogeneity across the studies for remember hits (p < .00001) as evidenced by a signicant Q
statistic (the Q statistic is similar to a one-way ANOVA in terms of
assessing variability across studies). However, we do not consider
this nding to be problematic in the present analysis because we
were interested only in estimating the overall effect size for age,

and because all the studies included estimates of remember hits


and false alarms for both age groups, all inuences on performance
are the same across hits and false alarms and response types. The Q
statistic did not reach conventional signicance levels for remember false alarms (p = .07). There was signicant heterogeneity for
know hits (p < .00001), but not for know false alarms as well.
Because the variance measured by studies with larger sample
sizes is more precise and can introduce bias in effect size analysis (Hedges & Olkin, 1985) we examined the correlations between
sample size and effect size across studies as well. The correlations
were not signicant for remember hits (r = .05) or false alarms
(r = .21), or for know hits (r = .39) or false alarms (r = .36). Because
false remember responses were near oor in many of the studies,
and could potentially be biased by restriction of range (the range
averaged across age groups was .02.11), we also examined whether
the effect sizes were related to the overall level of false remembering across studies. The correlation between effect size for false
remembering and level of false remembering was not signicant
(r = .09). Thus, the effect sizes did not appear to be inuenced greatly
by the number of subjects in each study or the overall level of false
remembering, indicating that the effect size equivalence for studied
and new items was not an artifact of these factors.
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