Neuroscience Letters 458 (2009) 140–143

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Neuroscience Letters
journal homepage: www.elsevier.com/locate/neulet

Association of KIBRA and memory

Timothy C. Bates a,∗ , Jackie F. Price b , Sarah E. Harris a , Riccardo E. Marioni b , F. Gerry R. Fowkes b ,
Marlene C. Stewart b , Gordon D. Murray b , Lawrence J. Whalley c , John M. Starr d , Ian J. Deary a
a
Department of Psychology, University of Edinburgh, 7 George Square, EH89JZ, Scotland, UK
b
Division of Community Health Sciences, University of Edinburgh, Scotland, UK
c
Department of Mental Health, University of Aberdeen, Scotland, UK
d
Geriatric Medicine Unit, University of Edinburgh, Scotland, UK

a r t i c l e i n f o a b s t r a c t

Article history: We report on the association of KIBRA with memory in two samples of older individuals assessed on
Received 15 January 2009 either memory for semantically unrelated word stimuli (Rey Auditory Verbal Learning Test, n = 2091),
Received in revised form 21 April 2009 or a measure of semantically related material (the WAIS Logical Memory Test of prose-passage recall,
Accepted 22 April 2009
n = 542). SNP rs17070145 was associated with delayed recall of semantically unrelated items, but not
with immediate recall for these stimuli, nor with either immediate or delayed recall for semantically
Keywords:
related material. The pattern of results suggests a role for the T → C substitution in intron 9 of KIBRA in a
Memory
component of episodic memory involved in long-term storage but independent of processes shared with
KIBRA
AVLT
immediate recall such as rehearsal involved in acquisition and rehearsal or processes.
Logical memory © 2009 Published by Elsevier Ireland Ltd.
Association

Papassotiropoulos et al. [17] recently reported an association of an
intronic substitution in KIBRA with better 5 min- and 24 h-delayed
recall of a list of unrelated nouns. Understanding this associa-
tion provides both an opportunity for fractionating the complex
memory phenotype into biologically distinct components and the
potential for novel therapeutic interventions in successful aging and
memory retention.
The improved performance in T-carriers of the rs17070145 SNP
was initially discovered in a pooled-DNA genome-wide association
study of 351 Swiss subjects aged 18–48 years. In the second sample
of 256 adult US subjects, this SNP again showed association with
30-min delayed recall performance (but not immediate recall) on
the Rey Auditory Verbal Learning Test (AVLT)—a standardized test
of learning a list of 30 unrelated nouns [AVLT: [15]], and improved
scores on Buschke’s Selective Reminding Test. Finally, in a sam-
ple of 424 18–28-year-old Swiss adults, T-allele carriers showed
improved 10-min delayed recall of semantically unrelated picture
stimuli. In none of these samples was KIBRA associated with pro-
cesses of attention or working memory, nor with immediate recall.
These three coherent findings suggest that KIBRA is specific for a
process affecting the retention of information across a delay, but
which does not alter short-term storage, rehearsal, or retrieval. As
learning of unrelated information was affected for both verbal and
∗ Corresponding author. Tel.: +44 131 6511945; fax: +44 131 6511771.
E-mail address: tim.bates@ed.ac.uk (T.C. Bates).
visual stimuli, the effect may be independent of stimulus modality
[17].
Since the initial report, three reports on replication attempts
have been published. In a small sample (64 subjects recruited for
studies on cognition in normal aging), Schaper et al. [20] reported
a trend to better delayed recall on a German version of the AVLT,
and a significant relationship of KIBRA with immediate recall and
delayed recognition. On the other hand, Need et al. [16] reported
no support for association of rs17070145 with either immediate
or 30-min delayed recall in 384 German individuals aged 22–75
tested on the AVLT. Of 42 additional KIBRA SNPs tested only one
reached nominal significance (0.03) and this was not in LD with
rs17070145. This group also found no support for association for
rs17070145 in 300 individuals of European background aged 18–77
tested on immediate recall following a single presentation of 12
unrelated words, nor for immediate or 30-min delayed recall of
prose-passage recall in an overlapping sample of 76 individuals.
The status and phenotype of KIBRA are thus important but
currently unclear. Here we report data from two samples, one
of 2091 subjects from the general population participating in a
clinical trial tested on the AVLT (an exact replication phenotype of
one of the Papassotiropoulos studies) and the second sample of 542
subjects from a study of normal aging tested on a prose-passage
memory task (the Logical Memory subscale of the Wechsler
Memory Scale—Revised [LMT: 24]). These samples allowed us to
examine immediate and delayed memory for related and unrelated
information, with 99% power to detect an effect similar to that
demonstrated previously for episodic memory in both samples

0304-3940/$ – see front matter © 2009 Published by Elsevier Ireland Ltd.

doi:10.1016/j.neulet.2009.04.050
 T.C. Bates et al. / Neuroscience Letters 458 (2009) 140–143 141

Table 1
AVLT Memory Marginal Means (and SDs) for AAA sample by T-carrier status.

Female Male Female Male

AVLT trial CC C|T/T CC C|T/T NA

Trial 1 5.53 (1.78) 5.64 (1.82) 4.97 (1.68) 5.23 (1.83) 5.48 (1.78) 5.18 (1.38)
Trial 2 8.38 (2.29) 8.39 (2.30) 7.31 (2.10) 7.60 (2.01) 8.33 (2.48) 7.06 (2.22)
Trial 3 10.18 (2.45) 10.16 (2.41) 8.86 (2.52) 9.11 (2.41) 10.13 (2.34) 8.47 (2.00)
Trial 4 11.98 (2.45) 11.94 (2.38) 10.43 (2.66) 10.87(2.48 11.86 (2.46) 10.76 (2.08)
Trial 5 (list B) 5.03 (1.93) 5.04 (1.98) 4.41 (1.85) 4.88(1.82) 4.79 (1.82) 4.41 (1.12)
Trial 6 (delay) 10.02 (3.21) 9.72 (3.20) 8.17 (3.03) 8.56 (3.22) 9.51 (3.38) 7.71 (3.29)
Trial 7 10.15 (3.35) 9.86 (3.43) 8.11 (3.27) 8.44 (3.37) 9.24 (3.59) 6.82 (2.72)

and retained 95% power to detect an effect less than one-tenth of
the reported magnitude [18].
Sample one was recruited as a community sample from gen-
eral practices throughout central Scotland for the Aspirin for
Asymptomatic Atherosclerosis (AAA) randomized controlled trial
of aspirin in the prevention of cardiovascular events and death in
subjects with asymptomatic atherosclerosis (total n = 3350) [1]. The
subjects in this analysis consisted of all 2091 subjects from the origi-
nal 3350 recruited into the trial who: (a) were still alive after 5 years,
when the cognitive testing was done and (b) agreed to undergo
the cognitive testing and to provide a DNA sample. There were no
other inclusion criteria and recruitment was random with respect to
aspirin/placebo condition (allocation to which also was random). To
recruit subjects for the AAA trial, over 28,000 subjects aged over 50
years from the general population of central Scotland agreed to be
assessed for asymptomatic atherosclerosis and possible inclusion
in the trial. This screened population was found to be representa-
tive of the general population of central Scotland in terms of age, sex
and deprivation category of residence. Subjects were then selected
for participation in the trial on the basis of evidence of asymp-
tomatic atherosclerosis and therefore poorer cardiovascular risk
factor profile. Compared to those not tested, subjects that under-
went cognitive testing were on average slightly younger, more likely
to be female and had a slightly better cardiovascular risk factor pro-
file. Thus, the AAA Trial sample is a community-based sub-group
broadly representative of the general population.
AAA subjects underwent cognitive testing between 4 and 7 years
after recruitment into the trial when they were aged 55–82 years
(mean 67.3). The test battery was administered in a quiet room
either in a research clinic or at the patient’s home by a trained
researcher. The order of tests in the battery was predetermined.
Sample two consisted of 542 members of the Lothian Birth
Cohort 1921 (LBC1921) [8]. All subjects were born in 1921, and
participated in the Scottish Mental Survey 1932, involving admin-
istration of the Moray House Test (MHT) of intelligence at age 11.
They have been traced and given both follow-up general ability tests
as well as a number of additional measures of cognitive and non-
cognitive function [8]. Subjects were a mean age of 79 at the time of
testing for the present study, with a very narrow range. All subjects
lived independently in the community.
Genotyping was performed in the AAA Trial sample using either
Competitive Allele Specific PCR (KASPar) or Taqman chemistry from
Applied Bioscience, as appropriate for the sample through vali-
dation assays, and in the LBC1921 sample using TaqMan. Primer
information is available on request.
Genotypes were analyzed using PEDSTATS [25] to check
Mendelian errors, sample identity as well as Hardy-Weinberg
equilibrium. Where zygosity or sample identities were suspected,
sample histories were reviewed and when necessary, genotyping
was repeated with DNA isolated from a backup sample: typing
failed for 13 individuals in the LBC1921 and for 43 individuals in
the AAA Trial sample.
Immediate and delayed memory was assessed in the AAA sam-
ple using the AVLT, consisting of 5 learning trials of a 15-word list,
an interference trial learning the second list, and subsequent recall,
and recognition memory trials for the original list. Subjects also
completed the Raven’s Progressive Matrices: (RAVEN) [19], a test
of non-verbal reasoning scored as number of items completed cor-
rectly within 20 min.
For the LBC sample, memory was assessed using the Wechsler
Logical Memory Test [24]. Participants were read aloud two themat-
ically independent stories, with an immediate recall task following
the story, encouraging word-for-word recall. After a 30-min delay,
during which a standard set of intervening tasks occurred, partic-
ipants were asked to recall the stories without having heard them
again. The Wechsler Memory Test used in the LBC sample is com-
mon in memory and cognitive impairment research. It correlates
around 0.4 with the AVLT reflecting substantial overlap, but also
distinct demands of learning and recall of prose-based rather than
unrelated word material [13]. In addition to the LMT, subjects had
available general cognitive ability measures at age 11 [6,21] and
including, at age 79 the Raven, administered as in the AAA sample.
LMT scores were normally distributed about a mean of 31.7
(range 2–73, SD = 12.8, 2 missing) and AVLT scores (sum of first
5 trials + interference and recall trials) had a mean of 63.4 (range
14–102, SD = 16.57, NA = 349). Tables of marginal means and SDs for
the memory test scores separately for sex and genotype using a
strict exclusion criterion of MMSE > 27 are given in Tables 1 and 2
for the LBC and AAA samples respectively. Counts of C/C, C/T, and
T/T genotypes were 254, 218 and 57 sample and 1040, 1020, and
203 in the 2359 genotyped members of the AAA Trial sample. The
minor (T) allele frequency was 31% in both the AAA LBC1921 sam-
ples. Analyses of KIBRA reported here used the two-level T-carrier
status variable, as used in Papassotiropoulos et al. [17].
As prior reports suggest that KIBRA affects only delayed recall,
and is unrelated to learning-phase or immediate recall perfor-
mance [17], we examined the effect of KIBRA on AVLT delayed
recall performance, controlling for differences in initial learning.
This was accomplished by creating a variable summing items
correctly recalled on the 5 AVLT learning trials as a measure of
initial learning, then using multiple regression to test the relation-
ship of delayed recall performance to T-carrier status, controlling
for the initial learning measure, age and sex. This analysis was
significant (adjusted R2 0.66, F(4,1926) = 936, p < 2.2e−16) and,
importantly, KIBRA T-carrier status significantly affected delayed
recall (beta = −0.26, t = −2.890, p = 0.004). The effect of prior learn-
ing was of course highly significant (t = 57.532, p < 2e−16). Age was
Table 2
Logical Memory Marginal Means (and SDs) by T-carrier Status for LBC sample.
Sex
Female Male
Genotype: CC C|T/T CC C|T/T
Logical memory 32.29 (12.61) 32.41 (11.94) 34.40 (15.24) 32.73 (10.63)
total
Immediate recall 19.29 (6.25) 19.33 (5.74) 20.30 (7.61) 19.74 (5.28)
Delayed recall 13.00 (6.81) 13.08 (6.68) 14.10 (7.98) 12.99 (5.90)
142 T.C. Bates et al. / Neuroscience Letters 458 (2009) 140–143
not significant (p = 0.82: suggesting that the effects of age were
accounted for by controlled for learning across the immediate-
learning trials), and sex had a marginal effect (p = 0.049), with
males recalling 0.2 fewer items than females on average. To avoid
confounding mild cognitive impairment with normal variation in
memory, initial analyses excluded subjects if they scored less than
24 on the Mini-Mental State Examination (MMSE) [10] a widely
used screening test for dementia. However, in all cases analyses
were similar whether using strict MMSE criteria for exclusion, mod-
erate criteria, or no exclusion criterion. Similarly controlling for
Raven’s Matrices score (intelligence) did not alter the association
of KIBRA to delayed recall performance, and neither Raven’s nor
MMSE were related to KIBRA (tested using linear models treating
these as DVs, with KIBRA status, age, and sex as IVs, p = 0.68 and
0.84 respectively). Importantly, and unlike the original report [17],
delayed recall was not significantly associated with KIBRA status
when initial learning was not controlled (p = 0.98). While KIBRA was
related to specifically to delayed recall controlling for initial per-
formance on the learning trials, learning trial performance itself
was unrelated to KIBRA status (p = 0.339). Thus results suggested an
effect of KIBRA, of modest size and specific to forgetting over the
delay interval.
Analyses of Wechsler Logical Memory Test performance in the
LBC sample showed no association of KIBRA to immediate or
delayed recall. The mean LMT scores for the “CC” and “T-carrier”
groups were 32.3 and 31.5 respectively: a difference both in the
opposite direction to that reported, and non-significant (Welch 2-
sample t-test (t(497.7) = 0.72, p = 0.47, 95% CI: −1.38 to 3.00)). Unlike
delayed recall for semantically unrelated list material in the AAA
sample, KIBRA T-carrier status remained non-significant in a lin-
ear model of delayed prose-passage recall, controlling for sex and
immediate recall (F(1,523) = .48, p = 0.49). No effects of sex were
seen for prose-passage recall (p = 0.71). A large effect of intelli-
gence test scores on memory was found: both for ability measured
68 years earlier at age 11 (F(1,515) = 31.7, p < 0.00001) and concur-
rently, at age 79 (F(1,515) = 117.3, p < 0.000001)). However KIBRA
was unrelated to intelligence at either age 79 or 11 (p = 0.65 and 0.40
respectively), and controlling for intelligence in addition to sex did
not reveal any significant effect of KIBRA on immediate memory or
delayed memory controlling for immediate memory (p = 0.65 and
0.837 respectively).
In order to increase the sensitivity of the analyses to specific
effects of KIBRA on logical memory, we explored the effects of
controlling for components of the “genetic pathway” for cognition
and memory including the COMT Val158Met polymorphism [12],
KLOTHO [5], NCSTN [4] and APOE [7] in addition to the behavioral
controls of sex and immediate recall. Including these covariates
failed to alter the non-significant nature of the analyses, though
both APOE and COMT show significant associations with memory
in this sample [7,12].
The present result, indicating genetic effects specific to the
forgetting of unrelated-item material, independent of learning
rates and immediate recall, and leaving relational (prose-passage)
material unaffected, helps to locate the role of KIBRA within the neu-
roscience of memory, and emphasizes the articulated nature of the
memory system [14]. Two findings appear most important. Firstly,
attention to the precise phenotype of a gene is likely to be important
in successful replications. Second, while our understanding of the
genetics of human memory is in its infancy, knowledge of genetic
phenotypes help specify and validate psychological and biological
models of memory.
The effects of KIBRA on episodic memory appear in this sample
to be modest and specific for a particular cognitive component of
memory related to item-based recall, rather than affecting a broad
range of memory phenotypes. While both the Wechsler and AVLT
tests are common in memory and cognitive impairment research
and correlate around 0.4 [13], neuropsychological data indicate
that the AVLT is a more sensitive discriminator of traumatic brain
injury patients than is the Logical Memory Test [2]. While a lack
of semantic context might simply make the unrelated word recall
task harder, perhaps via a reduction in support for recollection, the
lack of association to immediate recall or to working memory in any
sample studied to date does, however, suggest that the KIBRA poly-
morphism is unrelated to differences in the encoding of information
or to short-term rehearsal processes. This suggests that KIBRA is
specific for processes involved in storage and/or recollection, specif-
ically in which storage and retrieval based on item-distinctiveness
(rather than semantic-relatedness) is required.
At a cognitive level, the Logical Memory Test rewards rela-
tional coding, while for the AVLT where specific items must be
recalled, encoding the distinctive elements of each word (item-
specific information) along with generating a context (relation
context for recalling all the words) will best support recall at a later
date. Deficits in either the distinctiveness of item representations,
or in the generation of context to organize recall are candidate pro-
cesses for the involvement of KIBRA in selective poor recall for AVLT
items while leaving LMT scores in tact.
At a biological level, structures involved in long-term mem-
ory include the medial temporal lobe (MTL [23]) especially the
hippocampus and perirhinal [3] and parahippocampal circuits
that converge on the entorhinal cortex and from there enter
the hippocampus [14], and the prefrontal cortices. Imaging data
in the original report of the significance of KIBRA for mem-
ory implicated the hippocampus [17] a finding supported by
lesion studies indicating that the hippocampus supports recall (as
opposed to recognition), especially of relational material [11]. Fur-
ther work is required to determine whether hippocampal system
deficits alone could cause a selective inability to recall item-
memory, leaving recall of relational material intact. Prefrontal
lesions are associated with difficulties in learning, particularly
semantic encoding in the case of anterior and posterior ven-
trolateral prefrontal cortex [9], rehearsal during learning, and
with effective recall of relational material [22]. Intact learning-
phase performance suggests that KIBRA is not involved in these
prefrontal processes. A range of lesion and studies suggest that
familiarity, assessed by item-recognition is dependent on intact
perirhinal cortex, with lesions outside this area not affecting item-
memory and lesions to this area disrupting item-memory [26].
A null effect for recognition, as opposed to recollection suggests
that KIBRA may not be involved in perirhinal familiarity-based
processing.
In summary the present findings support a role for KIBRA in
processes specific to the conscious recall of item-based material,
possibly reflecting hippocampal processing. The result suggests a
high degree of genetic specificity within the neuronal systems sup-
porting memory and underscore both the need for attention to
phenotype, and for research deploying sophisticated phenotypes
in large-scale genetic studies of human memory.
Conflict of interest
No author has any actual or potential conflict of interest, includ-
ing any financial, personal or other relationships with other people
or organizations that could inappropriately influence their work.
Disclosure statement
None of the authors’ institutions has contracts relating to this
research through which it or any other organization may stand to
gain financially now or in the future. Nor did any author or institu-
tion have any other agreements that could be seen as involving a
financial interest in this work.
 T.C. Bates et al. / Neuroscience Letters 458 (2009) 140–143 143

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