Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition.
ABSTRACT In this study, we have examined visual recognition memory in a patient, YR, with discrete hippocampal damage who has shown normal or nearly normal item recognition over a large number of tests. We directly compared her performance as measured using a visual paired comparison task (VPC) with her performance on delayed matching to sample (DMS) tasks. We also investigated the effect of retention interval between familiarisation and test. YR shows good visual recognition with the DMS task up to 10 s after the familiarisation period, but only shows recognition with the VPC task for the shortest retention interval (0 s). Our results are consistent with the view that hippocampal damage disrupts recollection and recall, but not item familiarity memory.
Article: Memory in Preferential Looking Tasks
- [Show abstract] [Hide abstract]
ABSTRACT: This commentary explains how the field of developmental cognitive neuroscience (DCN) holds the promise of a much wider interdisciplinary integration across sciences concerned with development: psychology, molecular genetics, neurobiology, and evolutionary developmental biology. First we present a brief history of DCN, including the key theoretical issues it addresses; then we comment on how the four articles in this special section exemplify a DCN approach and raise important theoretical and methodological issues for the field of DCN; and we close by considering the future of DCN, especially the key role developmental psychologists can play as DCN becomes increasingly interdisciplinary.Developmental Review - DEVELOP REV. 01/2007; 27(3):428-441.
- [Show abstract] [Hide abstract]
ABSTRACT: Over the past 60 years the neural correlates of human episodic memory have been the focus of intense neuroscientific scrutiny. By contrast, neuroscience has paid substantially less attention to understanding the emergence of this neurocognitive system. In this review we consider how the study of memory development has evolved. In doing so, we concentrate primarily on the first postnatal year because it is within this time window that the most dramatic shifts in scientific opinion have occurred. Moreover, this time frame includes the critical age (∼9 months) at which human infants purportedly first begin to demonstrate rudimentary hippocampal-dependent memory. We review the evidence for and against this assertion, note the lack of direct neurocognitive data speaking to this issue, and question how demonstrations of exuberant relational learning and memory in infants as young as 3-months old can be accommodated within extant models. Finally, we discuss whether current impasses in the infant memory literature could be leveraged by making greater use of neuroimaging techniques, such as magnetic resonance imaging (MRI), which have been deployed so successfully in adults.Developmental cognitive neuroscience. 01/2014; 9C:12-29.
Neuropsychologia 42 (2004) 1293–1300
Visual paired comparison performance is impaired in a patient with
selective hippocampal lesions and relatively intact item recognition
O. Pascalisa,∗, N. M. Hunkina, J. S. Holdstockb, C. L. Isaaca, A. R. Mayesb
aLGF Group, Department of Psychology, The University of Sheffield, Western Bank, Sheffield S10 2TP, UK
bDepartment of Psychology, University of Liverpool, Eleanor Rathbone Building, Bedford Street South, Liverpool L69 3BS, UK
Received 16 July 2003; accepted 16 March 2004
In this study, we have examined visual recognition memory in a patient, YR, with discrete hippocampal damage who has shown normal
or nearly normal item recognition over a large number of tests. We directly compared her performance as measured using a visual paired
comparison task (VPC) with her performance on delayed matching to sample (DMS) tasks. We also investigated the effect of retention
only shows recognition with the VPC task for the shortest retention interval (0s). Our results are consistent with the view that hippocampal
damage disrupts recollection and recall, but not item familiarity memory.
© 2004 Elsevier Ltd. All rights reserved.
Keywords: Recognition memory; Hippocampus; Amnesia; VPC
Evidence from lesion studies indicates that damage to the
medial temporal lobes impairs visual recognition memory
and episodic memory (Squire, 1992). There is consistent
evidence from studies in monkeys that a visual item recogni-
tion memory deficit occurs after damage to medial temporal
cortex sites that are adjacent to the hippocampal formation.
Selective lesions of either the entorhinal and perirhinal cor-
tex (Gaffan & Murray, 1992), or the perirhinal cortex and
parahippocampal cortex (Zola-Morgan, Squire, Amaral,
& Suzuki, 1989) or the perirhinal cortex alone (Meunier,
Bachevalier, Mishkin, & Murray, 1993) yielded severe
recognition memory loss. There is, however, conflicting
evidence on the effects of selective hippocampal lesions on
visual item recognition memory and disagreement about the
mnemonic role played by the hippocampus. Whereas, some
animal lesion studies, using the Delayed Non-Matching to
Sample (DNMS) task, have found that selective damage to
the hippocampal formation resulted in impairment at the
longest delays only (Zola-Morgan, Squire, Rempel, Clower,
& Amaral, 1992; Alvarez, Zola-Morgan, & Squire, 1995),
other studies have found no impairment of visual recogni-
tion memory ability (Murray & Mishkin, 1998). The effect
∗Corresponding author. Tel.: +44-114-222-6548.
E-mail address: email@example.com (O. Pascalis).
of a hippocampal lesion on visual recognition memory as
measured with the DNMS task is then still under debate
(see Bachevalier, Nematic, & Alvarado, 2003; Baxter &
Murray, 2001a for a discussion).
Human lesion studies have found similar conflicting re-
sults. Whereas, some studies have found clear visual item
recognition deficits after relatively selective hippocampal
damage (e.g., Cipolotti et al., 2001; Manns & Squire, 1999;
Manns, Hopkins, Reed, Kitchener, & Squire, 2003; Reed
& Squire, 1997), others have found little or no impairment
in item recognition memory (Mayes, Holdstock, Isaac,
Hunkin, & Roberts, 2002; Vargha-Khadem et al., 1997;
Yonelinas et al., 2002). The explanation of these conflicting
results is unknown, but most probably involves either differ-
ing extents and locations of hippocampal damage, differing
extents of damage or dysfunction in extra-hippocampal sites
critical for visual item recognition, or both (for example,
see Baxter & Murray, 2001a and b; Zola & Squire, 2001).
Aggleton and Brown (1999) have hypothesised that dam-
ollection, leaving familiarity-based item recognition mem-
ory intact. The evidence about whether hippocampal dam-
age leaves familiarity memory intact is conflicting. Whereas,
Yonelinas et al. (2002) found, using several methods of as-
sessment, that familiarity was preserved in patients who
probably suffered hippocampal damage caused by hypoxia
following a cardiac arrest, Manns et al. (2003) found that
0028-3932/$ – see front matter © 2004 Elsevier Ltd. All rights reserved.
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
familiarity was as impaired as recollection in a group of pa-
tients who had suffered hippocampal damage. Provided, as
many researchers assume, that relatively normal item recog-
gleton and Brown hypothesis is consistent with hippocam-
pal lesions causing only a mild item recognition deficit that
might not be detectable in single patients. In contrast, if hip-
pocampal lesions disrupt familiarity as well as recollection,
then they should severely disrupt item recognition memory.
Item recognition memory has been assessed not only di-
rectly through the use of tests such as DNMS, but also
indirectly with the Visual Paired Comparison (VPC) task
(McKee & Squire, 1993; Pascalis & Bachevalier, 1999; Zola
et al., 2000). The VPC task, which was developed by Fantz
(1964), is a common way to measure visual recognition in
preverbal and nonverbal individuals (Fagan, 1974; Pascalis
& Bachevalier, 1998). It exploits individuals’ attraction to
novelty in order to assess their recognition memory for pre-
viously seen stimuli. The basic procedure is as follows:
The participant is first presented with a stimulus for a fa-
miliarisation period. Later, the participant is presented with
the same stimulus paired with a novel one. The key mea-
sure is the length of time spent fixating each of the two
stimuli. Longer duration of looking towards one stimulus,
generally the novel one, indicates discrimination and, in-
directly, recognition memory. Long-term recognition mem-
ory has been shown during infancy with this task (Fagan,
1974; Pascalis, de Haan, Nelson, & de Schonen, 1998).
The type of memory assessed by this task in infants has
been controversial, but according to Nelson (1995), it tests a
pre-explicit form of memory. Recently, however, a study of
adults showed that novelty preference correlated with later
recognition of the non-preferred stimulus, which is consis-
tent with the view that it provides an indirect index of the
ability to show aware recognition of studied stimuli (Manns,
Stark, & Squire, 2000).
Performance on the VPC task, in both infant and adult
monkeys with damage to the medial temporal lobe that
included the hippocampal formation, amygdala and sur-
rounding tissue has been found to be abnormal (Bachevalier,
Brickson, & Hagger, 1993). Recently, Pascalis and
Bachevalier (1999) showed that adult monkeys with neona-
tal hippocampal lesions showed preference for novelty at
short delays of 10s, but not at longer delays of 30s to 24h,
whereas normal monkeys showed novelty preference at all
delays. Consistent with this study, other studies of monkeys
with selective lesions within the medial temporal lobe, have
shown that novelty preference depends on the integrity
of the hippocampal formation (Zola et al., 2000) as well
as the perirhinal cortex (Buffalo et al., 1999). In humans,
McKee and Squire (1993), using the VPC task, have shown
that amnesic patients with relatively selective hippocampal
damage also show abnormal novelty preference. The pa-
tients in this study also showed clearly impaired visual item
recognition when this was measured directly, although their
performance was above chance levels.
Although monkeys, who showed an impaired novelty
preference on the VPC task (Pascalis & Bachevalier, 1999),
showed close to normal recognition on a DNMS task
(Bachevalier, Beauregard, & Alvarado, 1999), this has not
been demonstrated in any human patients with relatively se-
lective hippocampal lesions. If a single dissociation can be
shown between VPC performance and a direct performance
measure of visual item recognition, this should help con-
strain hypotheses about the processes that underlie directly
measured recognition and VPC performance. To determine
whether this kind of single dissociation can be found in
humans, we have examined VPC performance in a patient,
YR, with discrete hippocampal damage who has shown
normal or nearly normal item recognition over a large num-
ber of tests (Mayes et al., 2002). We directly compared her
VPC performance with her performance on delayed match-
ing to sample (DMS) tasks. We also investigated the effect
of retention interval between familiarisation and test.
The participants were patient YR and five age- and
IQ-matched healthy control participants. YR, a female,
was 62-year-old at the time of testing and had developed a
memory impairment following a possible ischaemic infarct,
arising from the administration of an opiate drug to relieve
severe back pain 14 years previously. YR’s neuropathol-
ogy and neuropsychological profile are reported in detail
by Holdstock et al. (2000) and Mayes et al., in press. For
clarification, an overview of YR’s neuropathological and
neuropsychological details are included here.
Magnetic resonance imaging (MRI) was carried out in
September 1997 using a 1.5T SIGNA whole-body magnetic
imaging system (General Electric, Milwaukee, WI). A 3D
T1-weighted radio-frequency spoiled gradient echo (SPGR)
image revealed a selective lesion affecting the hippocampus
bilaterally along its full anterior–posterior extent. Volumet-
ric analysis indicated that the volumes of the hippocampi
(corrected for intracranial volume) were 2.5 and 3 S.D.s
smaller than the mean volumes in a group of healthy control
participants (matched for sex, age and IQ) on the right and
left, respectively. In contrast, there was no pathology evi-
dent in the parahippocampal gyrus, and the corrected vol-
ume of this region, which included the perirhinal, entorhinal
and parahippocampal cortices, was at least 1 S.D. greater
than that of the control participants. Although the amygdala
appeared small, there was no evidence of pathology. Frontal
lobe structures were intact, and grey to white matter ratios
were normal. There was some evidence of parietal lobe at-
rophy, but this was not atypical for a woman of YR’s age,
and her corrected parietal lobe volume was within the con-
trol range on the right, and only just below the control range
on the left.
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
Performance of YR on standardised tests of intellectual and memory
Tests Subtests YR’s performance
D&P People (verbal recall)
Names (verbal recognition)
Shapes (non-verbal recall)
Doors (non-verbal recognition)
Key: NART FSIQ: estimated full scale IQ from National Adult Reading
Test (Nelson, 1991); WAIS-R: Wechsler Adult Intelligence Scale, Revised
(Wechsler, 1981); WMS-R: Wechsler Memory Scales, Revised (Wechsler,
1987); WRMT: Warrington Recognition Memory Scale (Warrington,
1984); D&P: Doors and People Test (Baddeley et al., 1994).
aDenotes age-scaled scores.
YR’s performance on standardised tests of IQ and mem-
ory function given up to the time of scanning are shown in
Table 1. Her current FSIQ (WAIS-R; Wechsler, 1981) was
in the average range and, although she showed a decrement
of 13 points between her estimated pre-morbid IQ (NART;
Nelson, 1991) and her current IQ, this represented a drop
of <1 S.D. in IQ points. On tests of memory function, YR
showed a consistent pattern in that she had a severe im-
pairment on tests of verbal and non-verbal recall, but intact
performance on tests of verbal and non-verbal item recogni-
tion (see Mayes et al., 2002). This pattern of impairment is
shown clearly by her performance on the Doors and People
Test (Baddeley, Emslie, & Nimmo-Smith, 1994) on which
she scored below the fifth percentile on tests of recall, but at
the 50th percentile or above on tests of recognition. Her per-
formance on the verbal and visual subtests of the Warring-
ton Recognition Memory Test (WRMT; Warrington, 1984)
was also above the 50th percentile in both cases. The disso-
ciation between YR’s impaired visual as well as verbal re-
call and her relatively intact performance on tests of visual
and verbal item recognition respectively has been studied in
greater detail, and is reported by Mayes et al. (2002).
In addition to tests of memory, YR’s perceptual func-
tion was assessed with the Visual Object and Space Percep-
tion Battery (VOSP; Warrington & James, 1991). YR scored
within 1 S.D. of the mean of the normative sample for all
subtests, and performed better than the controls on one of
the four object perception subtests (Silhouettes) and three of
the four spatial subtests (Dot Counting, Position Discrimi-
nation, Cube Analysis).
Five control participants were recruited. These were
healthy, female volunteers who were matched to YR in
terms of age (mean age: 63.20 years, S.D.: 2.17) and
WAIS-R FSIQ (mean IQ: 101.60, S.D.: 5.03).
Different sets of stimuli were used in the VPC and DMS
2.2.1. VPC task
One hundred and sixty black and white slides of objects
and faces were used as stimuli. The size and brightness of
the objects were kept uniform on each slide. When projected
onto the screen, the size of the stimuli was 8cm × 10cm,
and when two stimuli were present, they were separated by
a 5cm gap.
2.2.2. Delayed matching to sample task (DMS)
eryday objects were selected. The photographs were pre-
sented on a computer screen to eight young healthy vol-
unteers, who were required to rate each photograph on a
scale of familiarity from 1 to 5. The 72 photographs were
then divided into six sets of 12, which were matched on the
familiarity rating. Three of the sets were designated ‘target’
sets and three were designated ‘distractor’ sets; each target
set was paired with a distractor set. Each pair of sets was
allocated to one of the three delay conditions (0, 5, 10s
delay). The photographs were saved as black and white
pictures, and were presented on a white background. All
pictures occupied a 7cm×8.5cm rectangle on the computer
screen. During study, single pictures were presented at the
centre of the screen. At test, two pictures were presented
side-by-side separated by a 5.5cm gap.
Seventy-two colour photographs of ev-
were selected from our database. The 72 faces were arranged
into 36 pairs, each of which comprised two faces that were
matched in gender, approximate age and physical appear-
ance. One member of each pair was designated the target
face, and the other was designated the distractor face. The
36 pairs were divided into three sets of 12 pairs. Each set
was allocated to one of the three delay conditions (0, 5, 10s
delay). All faces were presented on a white background, and
occupied a 12cm×12cm rectangle on the computer screen.
During study, single pictures were presented at the centre of
the screen. At test, two pictures were presented side-by-side
separated by a 2cm gap.
Seventy-two black and white novel faces
The two tasks were administered separately over several
sessions. The VPC task was administered first during four
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
sessions over a 1 month period. The DMS task was admin-
istered in one session 2 months later.
2.3.1. VPC task
YR and the controls were investigated individually. Ex-
perimental conditions were as follows. First, each partici-
pant was shown a single target stimulus to inspect during
a 5s familiarisation period. After a delay during which a
blank screen was presented, the participant was shown the
target object or face paired with a new stimulus, for 5s.
The left–right position of the novel stimulus was counter-
balanced across trials. The delays tested were no delay (i.e.,
the time taken to change the slide, which was around 1s), 5
and 10s. Twelve trials with faces and 12 trials with objects
were used at each delay. The trials for each delay and cat-
egory of stimulus were randomly intermixed and presented
over several testing sessions. Participants were told that they
were part of a vision study, and we explained to YR that she
was the control of a patient with a visual problem. Partici-
pants were instructed that one picture would appear on the
screen for a brief presentation followed by a brief period of
rest, then two pictures would be simultaneously presented.
They were asked only to “look at the screen as if you were
watching TV”. The dependent variable was actual looking
time directed to the new and to the old stimulus.
A video camera with a videotimer was fixed above the
screen and recorded participants’ eye movements onto
videotape. Stimulus fixation was indicated by corneal re-
flection of the stimuli. Inspection of the videotape after the
experiment allowed the time spent inspecting the right and
left images in the 5s recognition phase to be assessed.
2.3.2. DMS task
Each participant was exposed to a stimulus for 5s and in-
structed to remember it. After a brief delay (0, 5 or 10s),
during which a blank screen was presented, the participant
was shown the familiar (target) stimulus together with a
novel (distractor) stimulus. The participant was required to
point to the familiar stimulus. The two stimuli were pre-
sented side-by-side, and the left/right position of the famil-
iar/novel stimuli was counterbalanced across trials. There
were 12 trials at each of the three delays for objects and 12
trials at each of the three delays for faces. Each delay condi-
tion was run separately in the following order: objects 0, 5,
10s; faces 0, 5, 10s. The order of conditions was the same
for all participants. Within each condition, the stimuli were
presented in random order.
To determine whether there was a significant difference
between the novelty preference of YR and that of the control
participants on the VPC task, the difference in time spent
looking at the familiar and novel stimuli was analysed. Nov-
elty preference was defined as the time spent looking at the
Mean difference in time spent looking at novel and familiar pictures
Condition Control mean
A positive value indicate a novelty preference.
familiar stimulus subtracted from the time spent looking at
the novel stimulus. This was calculated for each participant
on each of the 12 trials in each condition. YR’s novelty
preference in each condition was then compared with that
of the control participants using a t-test. Since it cannot be
assumed that the variance of YR’s performance was equiv-
alent to that of the group of control participants, Welch’s
procedure, which tests for the significance of the difference
between means when the population variances are unequal
(Ferguson, 1976, p. 168), was adopted. The results of this
analysis are shown in Table 2. YR showed a similar nov-
elty preference to that of the controls for both objects and
faces at a 0s delay. However, for both types of material she
showed a significant difference in novelty preference from
the controls at delays of 5 and 10s.
not the novelty preference exhibited by YR and the control
participants was significantly above chance. These t-tests
showed that novelty preference in each individual control
participant was significantly above chance in each condition
(all P’s < 0.001). In contrast, YR’s novelty preference was
only significantly above chance in the ‘objects 0s’ condition
(t(11)= 2.478,P < 0.05)andthe‘faces0s’condition(t(11)
= 3.144, P < 0.01). In all other conditions, YR’s novelty
preference did not differ from chance (all P’s > 0.2). On
the DMS task, YR and all control participants had perfect
On the VPC task, YR showed normal novelty preference
at a 0s delay but was impaired relative to controls, and did
not show novelty preference, at increased delays of 5 and
task, which used the same types of object and face stimuli
as those used in the VPC task, was unimpaired at delays
of up to 10s. YR correctly recognised all the studied target
stimuli, even though she had not shown a novelty preference
in the VPC task.
YR’s abnormal novelty preference for faces and objects
as shown by the VPC task is consistent with previous re-
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
sults from humans and non-human primates. In monkeys,
a deficit has been observed after a 10s delay following a
specific lesion of the hippocampus (Zola et al., 2000), or
after a lesion of the perirhinal cortex (Buffalo et al., 1999),
or after a lesion of the hippocampal formation (Pascalis &
Bachevalier, 1999). A lesion of the area TE led to a deficit
without delay (Buffalo et al., 1999).
A human study involving patients with various aetiologies
showed that a deficit occurred between 2min and a 1h delay
(McKee & Squire, 1993). Some of this evidence suggests
that hippocampal damage, whether in humans or non-human
primates, disrupts VPC performance just as was found in
YR. In YR, an abnormality in novelty preference behaviour
became apparent at short delays of only 5s. The temporal
characteristics of YR’s abnormality are similar to those
observed in studies with monkeys (Pascalis & Bachevalier,
1999; Zola et al., 2000) but appear to differ from those of
the amnesic patients reported by McKee and Squire (1993).
McKee and Squire’s patients showed novelty preference at
a 2min delay but not after 1h. Although five of McKee and
Squire’s patients had midline diencephalic lesions, six of
them had relatively selective hippocampal lesions so they
should be expected to perform like YR. Unfortunately, Mc-
Kee and Squire did not report the novelty preference scores
for individual patients. Although the mean performance of
the group (53.1%) at the 2min delay was significantly above
chance (50%), the range of performance (50.6–59.0%)
suggests that there were some individual patients whose
novelty preference may not have differed from chance.
Furthermore, the mean performance of the amnesic group
was significantly impaired relative to the controls (64%),
and represented a 16% decrease in novelty preference when
compared with performance at a 0.5s delay (69.1%). This
can be contrasted with the controls who showed only a 4.1%
decrease in performance from a 0.5s (68.1%) to a 2min
delay. Thus, the VPC data from YR are not necessarily in-
consistent with those reported by McKee and Squire (1993)
as it is possible that some of McKee and Squire’s patients
may have presented a deficit similar to YR that is masked by
There remains the puzzle, however, why YR shows an
impaired novelty preference despite her ceiling level per-
formance on item recognition using DMS when this was
explicitly tested using the same types of materials and task
design. It is unlikely that the solution to this puzzle relates
to differences in the materials used in the two studies. There
is, however, another possible explanation which needs to
be considered briefly. Since running this study in 1999 and
2000, YR’s performance on a range of tests of intelligence,
perception and memory has shown deterioration, and she no
longer exhibits the consistent behavioural pattern described
above, which she had displayed up until early 1999. She
is currently being investigated clinically for a dementing
illness, and it is possible that, if confirmed, the disease may
have been progressing at the time of VPC testing. How-
ever, there was one clear exception to the cognitive decline
that became apparent on reassessment in 2000: YR’s face
recognition appeared to be intact. Moreover, on tests of
face recognition that were given over several years from
1995, she performed at slightly above the mean level of her
controls and showed no deterioration across time (Mayes
et al., 2002). Specifically, her performance on one of these
tests, which was modelled on the WRMT and administered
3 months before VPC testing, was normal. We can, there-
fore, argue that preference for novel faces can be impaired
at delays as short as 5s in a patient who not only showed
face recognition at ceiling levels on a DMS task using com-
parable delays to the VPC task, but also showed normal
performance on a more sensitive, conventional test of face
With respect to YR’s preference for novel over familiar
objects, we have weaker evidence for a dissociation between
impaired VPC performance and intact item recognition. We
data for YR collected at the time of the VPC testing and,
as for the faces, both YR and her controls performed at
ceiling levels in the objects DMS task. However, given that
the pattern of YR’s VPC and DMS performance was similar
for the faces and the objects, it remains plausible that a
performance and intact item recognition.
The present pattern of results is consistent with a study
of nonhuman primates which also indicated a single dis-
sociation between novelty preference and item recognition.
Bachevalier et al. (2003) found that adult hippocampal-
lesioned monkeys showed impaired novelty preference at
the same delay (60s) at which DNMS performance was nor-
mal. Further work is needed to determine whether other hu-
man patients with relatively selective hippocampal lesions
resemble YR in showing this single dissociation. Identify-
ing the correct explanation of such a single dissociation
will also require further research. Four distinct explanations
are worth considering. The first explanation is that YR’s
VPC impairment reflects an underlying motivational deficit.
The second explanation is that the VPC task is more sen-
sitive to deficits in the familiarity memory process that is
critical for good visual item recognition than is the DMS
task. The third explanation is that some patients with hip-
pocampal damage, such as YR, are able to compensate for
their impairments in recollection and familiarity memory
by using an alternative strategy. The fourth explanation is
that performance on VPC is affected by impairments in
The first explanation is that our measure of novelty pref-
erence (i.e. looking preferentially at the novel item relative
to the familiar item) does not reflect recognition memory
but instead reflects an underlying motivation to respond to
novelty per se. According to this explanation YR shows
an impairment on the VPC task because of some underly-
ing motivational deficit. This account seems unlikely for a
number of reasons. First, the nature of the VPC task (i.e.
passively looking at one picture preferentially over another)
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
seems unlikely to have a motivational component. Second,
this would not explain why YR’s deficit only became ap-
parent after a delay of 5s; at a delay of 0s she showed
normal VPC performance for both faces and objects. Third,
although hippocampal lesions have been associated with
deficits in exploration and curiosity (O’Keefe & Nadel,
1978), Honey, Watt, & Good (1998) showed that it is only
for novel combinations of stimuli (e.g. a tone and light that
had been seen previously, paired not with each other, but
with other stimuli) that hippocampally lesioned rats showed
a deficit in orienting to novelty; both lesioned and control
animals showed a normal orienting response to novel stimuli
per se (e.g. a pairing of a tone and light neither of which had
been seen previously). This is consistent with O’Keefe and
Nadel’s (1978) view of genuine novelty which they argue is
a reflection of a new configuration of stimuli (which them-
selves may already be familiar) within an environment. The
current experiment does not allow us to make a distinction
between detection of, and orienting to, novelty but we pro-
pose that YR’s deficit does not reflect a motivational deficit.
According to the second explanation, YR shows impaired
novelty preference because the VPC test is more sensitive to
familiarity memory deficits than the DMS test. This seems
implausible given that YR was performing slightly better
than her controls’ mean scores on face recognition tests
that were more demanding than recognising single faces
at short delays (Mayes et al., 2002). In other words, YR
was impaired at the VPC task, which does not demand
effort, whereas she performed better than the mean level
of her control participants on demanding face recognition
tests. Furthermore, we have directly demonstrated that YR
Holdstock et al., 2002) although her recall (Mayes et al.,
2002) and recollection (Mayes et al., in press) were severely
impaired. There is, therefore, good reason to suppose that
YR’s familiarity memory at least for faces was intact, and
that the dissociation between impaired novelty preference
and normal DMS performance was not a reflection of task
The third explanation is that some patients with relatively
selective hippocampal lesions are aware of their memory
deficit and are able to compensate for it by using an alter-
native strategy, which supports accurate performance on the
DMS test and other tests of item recognition, and which
does not depend on the integrity of the hippocampus as
has been postulated in monkey research (Bachevalier et al.,
2003; Ridley & Baker, 1991). Such an alternative strategy
would only be triggered when participants know that their
memory is being examined with the DMS test or equiva-
lent recognition tests. The VPC is an incidental memory
task so participants would not intentionally activate the
compensatory strategy and would, therefore, show a deficit.
This explanation implies that familiarity memory would be
impaired following hippocampal lesions if one could test
recognition in an incidental fashion. This, of course, is not
feasible if items are tested one at a time because participants
rapidly realise what is happening. Some findings are consis-
tent with amnesics having a problem with recognition when
encoding is largely incidental and, therefore, presumably
automatic (Mayes, MacDonald, Donlan, Pears, & Meudell,
1992), but the possibility has not been formally tested in hu-
man amnesic patients, and patients with relatively selective
hippocampal lesions in particular. If automatic “familiarity
memory” processing activates the hippocampus at retrieval
as well as at encoding, then YR’s VPC deficit could have
depended critically on her not realising what the task truly
involved throughout the test so that at no stage was she
intentionally remembering. Testing this hypothesis will be
extremely difficult. It is also implausible for two reasons.
First, there are no obvious candidates for the role of inten-
tionally directed compensatory processes that will produce
normal familiarity. Second, there is growing evidence that
the hippocampus is not engaged in normal people either
by encoding that produced subsequent familiarity mem-
ory (Davachi, Mitchell, & Wagner, 2003; Ranganath et al.,
2004) or by familiarity memory per se (Eldridge, Knowlton,
Furmanski, Bookheimer, & Engel, 2000).
The fourth explanation is that YR and most other pa-
tients with selective hippocampal damage have preserved
familiarity memory processes, which are mediated by the
perirhinal cortex and other intact extra-hippocampal struc-
tures, whether their encoding and retrieval are being in-
tentionally driven or are on “automatic pilot”. But there
is agreement that such patients have impaired recollection
and this also contributes to item recognition performance
(e.g. see Mandler, 1980). The VPC is a task that depends
on participants detecting a difference in familiarity between
two stimuli and orienting towards the more novel stimulus.
Use of the c-fos technique in rats has demonstrated that
the perirhinal cortex and area TE are activated by novel
visual items, but not novel visuo-spatial combinations of
familiar items, whereas the hippocampus is activated by
novel visuo-spatial combinations of familiar items, but not
by novel items (Wan, Aggleton, & Brown, 1999). This is
consistent with the hippocampus not playing a direct role
in the detection of novel items. YR’s impaired VPC per-
formance suggests that she was reacting to her impaired
recollection in the face of normal familiarity memory for
the faces and objects. Thus, although the novel items might
have been drawing her attention so might the familiar ones
because she was unable to recall why they were familiar.
The result would have been the absence of preference for
the novel items at the longer delays used in the VPC task.
Presumably, at the shortest delay (0s) YR was still able
to recollect why one of a pair of faces was familiar. One
implication of this prediction is that normal participants
may show reduced novelty preferences when the competing
stimulus is familiar, but not recollected. If this is found,
then VPC performance will have been shown to be sensitive
to mismatches between recollection and familiarity. This is
consistent with the view that hippocampal damage disrupts
recollection and recall, but not item familiarity memory.
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
The authors would like to thank Jim Stone for helpful
Aggleton, J. P., & Brown, M. W. (1999). Episodic memory, amnesia,
and the hippocampal-anterior thalamic axis. Behavioural and Brain
Sciences, 22, 425–489.
Alvarez, P., Zola-Morgan, S., & Squire, L. R. (1995). Damage limited to
the hippocampal region produces long-lasting memory impairment in
monkeys. Journal of Neuroscience, 15, 3796–3807.
Bachevalier, J., Nematic, S., & Alvarado, M. C. (2003). The medial
temporal structures and object recognition memory in nonhuman
primates. In L. R. Squire & D. L. Schacter (Eds.), Neurospsychology
of Memory (3rd ed.), (pp. 326–338). Guilford Press.
Bachevalier, J., Beauregard, M., & Alvarado, M. C. (1999). Long-term
effect of neonatal damage to the hippocampal formation and
amygdaloid complex on object discrimination and object recognition
in rhesus monkey (Macaca mulatta). Behavioral Neuroscience, 113,
Bachevalier, J., Brickson, M., & Hagger, C. (1993). Limbic-dependent
recognitionmemory in monkeys
NeuroReport, 4, 77–80.
Baddeley, A., Emslie, H., & Nimmo-Smith, I. (1994). Doors and People.
Thames Valley Test Company.
Baxter, M. G., & Murray, E. A. (2001a). Impairments in visual discrimi-
nation learning and recognition memory produced by neurotoxic lesions
of rhinal cortex in rhesus monkeys. European Journal of Neuroscience,
Baxter, M. G., & Murray, E. A. (2001b). Opposite relationship of
hippocampal and rhinal cortex damage to delayed nonmatching-to-
sample deficits in monkeys. Hippocampus, 11, 61–71.
Buffalo, E. A., Ramus, S. J., Clark, R. E., Teng, E., Squire, L. R., &
Zola, S. M. (1999). Dissociation between the effects of damage to
perirhinal cortex and area TE. Learning and Memory, 6, 572–599.
Cipolotti, L., Shallice, T., Chan, D., Fox, N., Scahill, R., & Harrison, G.
et al., (2001). Long-term retrograde amnesia the crucial role of the
hippocampus. Neuropsychologia, 39, 151–172.
Davachi, L., Mitchell, J. P., & Wagner, A. D. (2003). Multiple routes
to memory: distinct medial temporal lobe processes build item and
source memories. Proceedings of the National Academy of Sciences
of the United States of America, 100, 2157–2162.
Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y., &
Engel, S. A. (2000). Remembering episodes: a selective role for the
hippocampus during retrieval. Nature Neuroscience, 3, 1149–1152.
Fagan, J. F. (1974). Infant recognition memory: the effects of length of
familiarization and type of discrimination task. Child Development,
Fantz, R. L. (1964). Visual experience in infants: decreased attention to
familiar patterns relative to novel ones. Science, 146, 668–670.
Ferguson, G. A. (1976). Statistical Analysis in Psychology and Education
(4th ed.). Tokyo: McGraw-Hill.
Gaffan, D., & Murray, E. A. (1992). Monkeys (Macaca fascicularis)
with rhinal cortex ablations succeed in object discrimination learning
despite 24-h intertrial intervals and fail at matching to sample despite
double sample presentations. Behavioural Neuroscience, 106, 30–38.
Holdstock, J. S., Mayes, A. R., Cezayirli, E., Isaac, C. L., Aggleton, J.
P., & Roberts, N. (2000). A comparison of egocentric and allocentric
spatial memory in a patient with selective hippocampal damage.
Neuropsychologia, 38, 410–425.
Holdstock, J. S., Mayes, A. R., Roberts, N., Cezayirli, E., Isaac,
C. L., & O’Reilly, R. C. et al., (2002). Under what conditions
is recognition spared relative to recall after selective hippocampal
damage? Hippocampus, 12, 341–351.
Honey, R. C., Watt, A., & Good, M. (1998). Hippocampal lesions disrupt
an associative mismatch process. Journal of Neuroscience, 18, 2226–
Mandler, G. (1980). Recognizing: the judgement of previous occurrence.
Psychological review, 87, 252–271.
Manns, J. R., & Squire, L. R. (1999). Impaired recognition memory on
the Doors and People Test after damage limited to the hippocampal
region. Hippocampus, 9, 495–499.
Manns, J. R., Stark, C. E. L., & Squire, L. R. (2000). The
visual paired-comparison task as a measure of declarative memory.
Proceedings of the National Academy of Sciences of the United States
of America, 97, 12375–12379.
Manns, J. R., Hopkins, R. O., Reed, J. M., Kitchener, E. G., & Squire, L.
R. (2003). Recognition memory and the human hippocampus. Neuron,
Mayes, A. R., MacDonald, C., Donlan, L., Pears, J., & Meudell, P. R.
(1992). Amnesics have a disproportionately severe memory deficit for
interactive context. Quarterly Journal of Experimental Psychology,
Mayes, A. R., Holdstock, J. S., Isaac, C. L., Hunkin, N. M., & Roberts,
N. (2002). Relative sparing of item recognition memory in a patient
with adult-onset damage limited to the hippocampus. Hippocampus,
Mayes, A. R., Holdstock, J. S., Isaac, C. L., Montaldi, D., Grigor, J., &
Gummer, A. et al., in press. Associative recognition in a patient with
selective hippocampal lesions and relatively normal item recognition.
McKee, R. D., & Squire, L. R. (1993). On the development of declarative
memory. Journal of Experimental Psychology: Learning, Memory and
Cognition, 19, 397–404.
Meunier, M., Bachevalier, J., Mishkin, M., & Murray, E. A. (1993).
Effects on visual recognition of combined and separate ablations of
the entorhinal and perirhinal cortex in rhesus monkey. Journal of
Neuroscience, 13, 5418–5432.
Murray, E. A., & Mishkin, M. (1998). Object recognition and location
memory in monkeys with excitotoxic lesions of the amygdala and
hippocampus. Journal of Neuroscience, 5, 68–82.
Nelson, C. A. (1995). The ontogeny of human memory: a cognitive
neuroscience perspective. Developmental Psychology, 3, 723–738.
Nelson, H. E. (1991). National Adult Reading Test (2nd ed.). London:
O’Keefe, J. & Nadel, L. (1978). The Hippocampus as a Cognitive Map.
Oxford University Press.
Pascalis, O., & Bachevalier, J. (1998). Face recognition in primates: a
cross species study. Behavioural Processes, 43, 87–96.
Pascalis, O., & Bachevalier, J. (1999). Neonatal aspiration lesions of
the hippocampal formation impair visual recognition memory when
assessed by paired-comparison task but not by delayed nonmatching-to-
sample task. Hippocampus, 9, 609–616.
Pascalis, O., de Haan, M., Nelson, C. A., & de Schonen, S. (1998).
Long-term recognition memory for faces assessed by visual paired
comparison in 3- and 6-month-old infants. Journal of Experimental
Psychology: Learning, Memory and Cognition, 24, 249–260.
Ranganath, C., Yonelinas, A. P., Cohen, M. X., Dy, C. J., Tom, S. M.,
& D’Esposito, M. (2004). Dissociable correlates of recollection and
familiarity within the medial temporal lobes. Neuropsychologia, 42,
Reed, J. M., & Squire, L. R. (1997). Impaired recognition memory in
patients with lesions limited to the hippocampal formation. Behavioural
Neuroscience, 111, 667–675.
Ridley, R. M., & Baker, H. F. (1991). A critical evaluation of monkey
models of amnesia and dementia. Brain Research Review, 16, 15–37.
Squire, L. R. (1992). Declarative and nondeclarative memory: multiple
brain systems supporting learning and memory. Journal of Cognitive
Neuroscience, 4, 232–243.
Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van
Paesschen, W., & Mishkin, M. (1997). Differential effects of early
O. Pascalis et al./Neuropsychologia 42 (2004) 1293–1300
hippocampal pathology on episodic and semantic memory. Science,
Wan, H., Aggleton, J. P., & Brown, M. W. (1999). Different contributions
of the hippocampus and perirhinal cortex to recognition memory. The
Journal of Neuroscience, 19, 1142–1148.
Warrington, E. K. (1984). Recognition Memory Test. London: NFER-
Warrington, E. & James, M. (1991). Visual Object and Space Perception
Battery. Thames Valley Test Company.
Wechsler, D. (1981). Wechsler Adult Intelligence Scale, Revised. New
York: Psychological Corporation.
Wechsler, D. (1987). Wechsler Memory Scale, Revised. New York:
Yonelinas, A. P., Kroll, N. E., Quamme, J. R., Lazzara, M. M., Sauve,
M. J., & Widaman, K. F. et al., (2002). Effects of extensive temporal
lobe damage or mild hypoxia on recollection and familiarity. Nature
Neuroscience, 5, 1236–1241.
Zola, S. M., & Squire, L. R. (2001). Relationship between magnitude
of damage to the hippocampus and impaired recognition memory in
monkeys. Hippocampus, 11, 92–98.
Zola, S. M., Squire, L. R., Teng, E., Stefanacci, L., Buffalo, E. A., &
Clark, R. E. (2000). Impaired recognition memory in monkeys after
damage limited to the hippocampal region. Neuroscience, 20, 451–463.
Zola-Morgan, S., Squire, L. R., Amaral, D. G., & Suzuki, W. A.
(1989). Lesions of perirhinal and parahippocampal cortex that spare
the amygdala and hippocampal formation produce severe memory
impairment. Journal of Neuroscience, 9, 4355–4370.
Zola-Morgan, S., Squire, L. R., Rempel, N. L., Clower, R. P., & Amaral,
D. G. (1992). Enduring memory impairment in monkeys after ischemic
damage to the hippocampus. Journal of Neuroscience, 12, 2582–2596.