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The Journal of Neuroscience, March 15, 1998, 18(6):2268-2275
Perirhinal Cortex Ablation Impairs Visual Object
Identification
Mark J.
Buckley and
David
Gaffan
Department of Experimental Psychology, Oxford University, Oxford,
OX1 3UD, United Kingdom
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ABSTRACT |
Impairments in both recognition memory and concurrent
discrimination learning have been shown to follow perirhinal cortex ablation in the monkey. The pattern of these impairments is consistent with the hypothesis that the perirhinal cortex has a role in the visual
identification of objects. In this study we compared the performance of
a group of three cynomolgus monkeys with bilateral perirhinal cortex
ablation with that of a group of three normal controls in two tasks
designed to test this hypothesis more directly. In experiment 1 the
subjects relearned a set of 40 familiar concurrent discrimination
problems; the stimuli in each trial were digitized images of real
objects presented in one of three different views. After attaining
criterion they were tested on the same problems using similar, but
previously unseen, views of the objects. In experiment 2 the subjects
were tested on their ability to perform 10 of these familiar
discriminations with each problem presented in the unfamiliar context
of a digitized image of a unique complex scene. The subjects with
ablations were significantly impaired on both tasks. These results
demonstrate that the role of the perirhinal cortex is not restricted to
memory, and they support the hypothesis that the perirhinal cortex is
involved in visual object identification. We suggest that the
perirhinal cortex is crucially involved in processing coherent concepts
of individual objects. A deficit of this nature could underlie the
pattern of impairments that follow perirhinal cortex damage in both
visual object recognition memory and visual associative memory.
Key words:
monkey; macaque; learning; memory; object identification; perirhinal cortex; TE; inferior temporal cortex; temporal lobe
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INTRODUCTION |
It is well established that visual
recognition memory in the monkey, as tested by delayed matching and
nonmatching to sample (DMS and DNMS) with trial-unique objects, is
severely impaired after combined damage to the perirhinal and
entorhinal cortices or after damage to the perirhinal cortex alone
(Murray et al., 1989 ; Gaffan and Murray, 1992; Meunier et al., 1993;
Eacott et al., 1994). In contrast, after combined perirhinal and
entorhinal cortex ablation, impairments were not revealed in new
postoperative concurrent discrimination learning with 24 hr intertrial
intervals (Gaffan and Murray, 1992; Eacott et al., 1994). This appeared consistent with the hypothesis that concurrent discrimination learning
engaged a corticostriatal habit system, whereas DNMS engaged a limbic
memory system (Malamut et al., 1984; Mishkin and Petri, 1984; Overman
et al., 1990). However, recent studies have demonstrated that
concurrent discrimination learning is in fact impaired after perirhinal
cortex ablation alone (Buckley and Gaffan, 1997, 1998a). Because both
fornix transection (Gaffan, 1992) and amygdalectomy (Gaffan, 1994a)
have also been shown to impair discrimination learning with 24 hr
intertrial intervals, it is now evident that the limbic system is
involved in such learning. Thus, the perirhinal cortex can no longer be
regarded as either a structure primarily involved in short- as opposed
to long-term memory or as a structure primarily involved in memory as
opposed to habit. Clearly, the role of the perirhinal cortex in the
primate's visual learning and memory system needs to be reassessed in
light of the new behavioral data.
The impairments in new concurrent discrimination learning that were
shown to follow perirhinal cortex ablation were revealed using
manipulations to the basic task, which either increased the number of
incorrect choices in each trial, increased the number of problems in
each set, or displayed objects in different views (Buckley and Gaffan,
1997, 1998a). In addition, although DMS with large stimulus sets was
severely impaired after combined perirhinal and entorhinal cortex
ablation, DMS with small sets was not (Eacott et al., 1994). Therefore,
we suggested previously that the perirhinal cortex plays a role in the
visual identification of objects, because in both types of task
impairments were revealed only when the burden placed on the subject's
ability to identify multiple individual objects was sufficiently
heavy.
To test this hypothesis, in experiment 1 a group of monkeys with
perirhinal cortex ablations (PRh) and a group of normal controls (CON)
learned a 40-problem concurrent discrimination learning task to
criterion using digitized images of familiar views of each object. They
were subsequently tested on the same problems using similar but
previously unseen views. If perirhinal cortex ablation impairs object
identification, then we would predict that the PRh group would be
impaired when identifying new views of familiar objects. In experiment
2 the two groups of monkeys were required to relearn 10 of these
problems concurrently, this time with the objects presented in the
context of a digitized image of a complex scene. Likewise, if
perirhinal cortex ablation impairs object identification, we would
predict that the PRh group would be impaired when identifying familiar
objects presented in the unfamiliar context of a complex scene.
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MATERIALS AND METHODS |
Subjects
Six male cynomolgus monkeys (Macaca fascicularis)
took part in this experiment. They were housed either individually or
in pairs, in rooms with automatically regulated lighting, and they were
given water ad libitum. Before the experiments reported
here, three subjects had the perirhinal cortex ablated bilaterally
(PRh), whereas the other three subjects served as unoperated controls (CON). All six monkeys had identical pre- and postoperative experience in color discrimination and concurrent discrimination learning tasks in
a series of experiments that were performed before the present study
commenced, and they also completed a configural learning task and a
paired associate learning task between the two experiments reported
here (Buckley et al., 1997; Buckley and Gaffan, 1997, 1998a,b).
Surgery
The operations were performed in sterile conditions with the aid
of an operating microscope, and the monkeys were anesthetized throughout surgery with barbiturate (5% thiopentone sodium solution) administered through an intravenous cannula. The zygomatic arch was
removed, and the temporal muscle was detached from the cranium and
retracted. Surgery was performed on one hemisphere at a time. A bone
flap was raised over the frontal and temporal lobe. The medial and
posterior limits of the flap were in a crescent shape extending from
within 5 mm of the midline at the brow to the posterior insertion of
the zygoma. The anterior limit of the flap was the brow and the orbit.
Ventrally the flap extended from the posterior insertion of the zygoma
to the level of the superior temporal sulcus in the lateral wall of the
temporal fossa anteriorly. The ventral anterior part of this bone flap
was extended with a rongeur to the base of the temporal fossa. The dura
mater was cut to expose the dorsolateral frontal and lateral temporal
lobe. The frontal lobe was retracted from the orbit with a brain spoon
to enable access to the anterior medial temporal lobe. Pia mater was
cauterized, and the underlying cortex was removed by aspiration in the
lateral bank of the anterior part of the rhinal sulcus and in the
adjacent 2 mm of cortex on the third temporal convolution. The
monkey's head was then tilted to an angle of 120° from the vertical,
and the base of the temporal lobe was retracted from the floor of the
temporal fossa with a brain spoon. The posterior tip of the first part
of the ablation was identified visually, and the removal was then
extended in the lateral bank of the rhinal sulcus to the posterior tip
of the sulcus, again removing 2 mm of laterally adjacent tissue. The
dura mater was then sewn, the bone flap was replaced, and the wound was
closed in layers. This ablation was made in both hemispheres in a
single operation.
Histology
After the conclusion of all behavioral experiments, the animals
with ablations were sedated, deeply anesthetized, and then perfused
through the heart with saline solution (0.9%), which was followed by
formol saline solution (10% formalin in 0.9% saline solution). The
brains were blocked in the coronal stereotaxic plane posterior to the
lunate sulcus, removed from the skull, allowed to sink in sucrose
formalin solution (30% sucrose, 10% formalin), and sectioned
coronally at 50 µm on a freezing microtome. Every tenth section
through the temporal lobe was stained with cresyl violet and mounted.
Figure 1 shows, for each monkey, five of
these sections spaced 4 mm apart through the lesioned area. Figure
2 shows the extent of the intended lesion
on a labeled ventral illustration of a standard monkey brain with an
illustration of the actual extents of the lesions in two representative
subjects. Further detailed drawings of reconstructions of these lesions have also been published elsewhere (Buckley et al., 1997). The extent
of the perirhinal lesions in all three cases was essentially as
intended, except for some inadvertent damage caused by slight involvement of the laterally adjacent area TE (on the left in PRh1 and
PRh3 and bilaterally in PRh2), for an anteroposterior extent of 2 and 4 mm on the left and right sides, respectively. There was slight
involvement of the most lateral part of the entorhinal cortex in PRh2
and PRh3 and slight involvement of the anterior parahippocampal cortex
in all three cases.
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Figure 1.
Five 50 µm sections of the brain are shown for
each animal in the perirhinal groups (PRh1, PRh2, PRh3).
From top to bottom the sections are spaced 4 mm apart running anterior
to posterior through the area of the bilateral perirhinal cortex
ablation. L, Lateral sulcus; S, superior
temporal sulcus; A, anterior middle temporal sulcus;
P, posterior middle temporal sulcus; O,
occipital sulcus.
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Figure 2.
A, Shaded regions
show the intended location and extent of the ablation of the perirhinal
cortex on a schematic diagram of the ventral view of the brain with
sulci and gyri in labeled regions; B, shaded regions
show the extent of the actual perirhinal cortex lesions in two
representative subjects (PRh1,
PRh3).
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Apparatus and stimuli
The present tasks were performed in an automated test apparatus.
The subject sat in a wheeled transport cage fixed in position in front
of a touch-sensitive screen (380 × 280 mm) on which the stimuli
could be displayed. The subject could reach out between the horizontal
or vertical bars (150 mm apart) at the front of the transport cage to
touch the screen. An automated pellet delivery system, controlled by
the computer, delivered reward pellets into a food well that was 80 mm
in diameter and was positioned in front of and to the right of the
subject. Reward pellets (190 mg) were only delivered in response to a
correct choice made by the subject to the touch screen. Pellet delivery
was accompanied by an audible click. An automated lunchbox (length 200 mm, width 100 mm, height 100 mm) was positioned in front of and to the
left of the subject. The lunchbox was spring-loaded and opened
immediately with a loud crack on completion of the whole task. The
lunchbox contained the subject's daily diet of cereals, seeds,
proprietary primate pellets, nuts, raisins, and half an apple or
banana. An infrared camera was positioned looking down into the
transport cage from above to allow the subject to be observed while it
was engaged in the task. The whole apparatus was housed in an
experimental cubicle that was dark except for a 25 W incandescent lamp.
This lamp was positioned on the floor, below the level of the touch screen, to avoid any reflection onto the screen but to allow the subject to see into the cup and lunchbox when the screen was dark. The
presentation of the visual stimuli on the touchscreen was controlled by
a computer. The computer also recorded the responses that subjects made
to the touchscreen and controlled the delivery of reward pellets after
correct responses, and it controlled the opening of the lunchbox after
completion of the session.
The stimulus material for task 1 was composed of digitized images of
real objects presented on a touchscreen. To create these digitized
images, each object was photographed in front of a plain white or black
background using an electronic camera (Canon ION, model RC-260). Six
different views of each object were taken. For each of two elevations
(~30 and 60°) looking down on the object, three different rotations
were photographed (face on, 45° rotated left, and 45° rotated
right). The images were then saved as 8 bit, 256 color, bitmap (BMP)
files with a spatial resolution of 368 × 272 pixels. Each image
was then reduced to 64 colors using a Stuki dither color reduction
algorithm. A computer program analyzed each of these files and
converted the background of each image into a homogenous plain gray
color. The BMP files were finally converted into a format that could be
used by a separate program that was designed to display two of these
images on the screen instantaneously, side by side, on a plain gray
background. The resolution of the display was 1024 × 768 pixels.
The stimulus material for task 2 was composed of digitized images of
scenes containing varying numbers of foreground and background objects.
To create these digitized images, each scene was photographed using the
Canon ION electronic camera. A total of 10 different scenes were
selected. In addition to the other foreground and background objects
contained in the scene, each scene also contained a pair of foreground
objects; one was positioned on the right and the other on the left of
the scene. Each scene was photographed with this pair of objects placed
in their respective foreground positions, with their positions
reversed, and with both objects on the same side. This latter
contingency allowed a section of the scene containing the object to be
alternated with the same section of the photograph of the scene with
the object absent, at the same time maintaining full color balance in
the scene as a whole, thus allowing objects to be flashed on and off
within the scene as visual feedback, as required during the task. The images were then saved as 8 bit, 256 color, BMP files with a spatial resolution of 736 × 544 pixels. Each image was then reduced to 128 colors using a Stuki dither color reduction algorithm. The BMP
files were finally converted into a format that could be used by a
separate program that was designed to display one of these scenes on
the screen instantaneously. The same program also allowed sections of
photographs of the same scene to be rapidly and instantaneously alternated, as described above, to give the impression of a flashing stimulus object as required. The resolution of the display was 800 × 600 pixels.
Behavioral testing
Experiment 1: identification of familiar objects
presented in new views. Experiment 1 consisted of two stages. In
stage A the subjects learned to criterion a concurrent discrimination learning task consisting of 40 pairs of digitized images of objects, with each object presented on the touchscreen in one of three different
views in each trial. In stage B the subjects were retested in the same
manner using one of three similar but previously unseen views of the
same objects. No preliminary training was given in the automated
apparatus because the subjects were experienced in touching stimuli on
the touchscreen to obtain food reward.
Stage A. The subjects were required to learn concurrently a
set of 40 pairs of object discriminations between pairs of digitized images of objects presented on a plain gray background on a
touchscreen. These 40 pairs of objects were familiar to the subjects
because they had already learned concurrent discrimination learning
tasks to criterion with these stimuli in a previous study in which only three out of the six different views of each object were used (Buckley
and Gaffan, 1998a). These three digitized images of different views
were chosen at random with respect to the two levels of elevation but
included one image with the object face on, one image with the object
rotated 45° to the left, and one image with the object rotated 45°
to the right. The object-reward associations that were used in the
last stage of this previous study were maintained in stage A of the
present study, and only the same three views of each object that were
used in this previous study were used in stage A of the present study.
The left-right position of the correct choice (S+) and incorrect
choice (S ) on the touchscreen was randomized from trial to trial.
Which of the three different views of each object that would be
presented in each trial was determined pseudorandomly before the
session began. Figure 3 illustrates three
representative problems between pairs of digitized images as they would
appear on the touchscreen (top row) and shows how the view
of each object may change in a subsequent presentation of the same
problem (bottom row). If the subject touched the S+, then a
reward pellet was delivered, the S disappeared, and the S+ remained
on the screen for a further 1.5 sec before the intertrial interval of
10 sec commenced. If the subject touched the S, both the S+ and S
disappeared and the intertrial interval of 10 sec commenced. There were
no correction trials. If the subject touched elsewhere on the screen,
both images remained until one of them was touched. If the subject
touched the screen during the 10 sec intertrial interval, then the 10 sec intertrial interval was restarted from that time. In each session
the set of 40 problems was repeated three times and in the same
sequence. After all 120 trials within the session had been completed,
the automated lunchbox opened immediately to make available the
subject's daily meal, as described above. The subjects performed one
session of this task every day until they attained a criterion of
 90% correct responses made within a single session. On the next day
after attaining criterion, they proceeded to stage B of experiment 1 .
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Figure 3.
Examples of how three different discrimination
problems from experiment 1 appear to subjects (reproduced in gray
scale) when stimuli are presented as digitized images of objects on the
touchscreen. For each of three different problems the figure
illustrates how the appearance of the objects changes with presentation
of the objects in different views.
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Stage B. In stage B the subjects continued testing on the
same problems in the same order and in the same manner as in stage A. The only difference was that instead of using the views of the objects
that had been used in stage A, in each trial of stage B the objects
were presented in one of the three remaining views that until this
stage of this experiment had never been seen before by the subjects.
The subjects performed one session of this task every day until they
attained a criterion of 90% correct responses made within a single
session
Experiment 2: identification of familiar objects presented
in scenes. In experiment 2 the subjects learned to criterion a concurrent discrimination learning task consisting of 10 problems. Each
of these problems consisted of a unique scene that contained two
objects that were designated as the S+ and S in addition to various
other foreground and background objects. Each of the 10 S+ and S
object pairs were a pair of objects that had been used in experiment 1 and also in a previous study (Buckley and Gaffan, 1998a). The
object-reward contingencies remained unchanged for each of these 10 pairs of objects. The subjects therefore were highly familiar with
these objects and with the object-reward contingencies; however, they
had not experienced previously the objects in the context of a scene.
Each pair of objects was always presented within the same scene but the
left/right position of the objects in the foreground of the scene was
chosen pseudorandomly before the trial began. The top row of Figure
4 illustrates three representative
problems between pairs of objects presented in their scenes as they
would appear on the touchscreen; the bottom row of Figure 4 shows
the same problem with the S+ and S positions reversed. If the subject
touched the S+, then a reward pellet was delivered and the S+ flashed
on and off within the scene five times, providing visual feedback for a
correct response before the intertrial interval of 15 sec commenced. If
the subject touched the S, then the screen blanked and the intertrial
interval of 15 sec commenced. There were no correction trials. If the
subject touched elsewhere on the screen than the S+ or S, then the
scene remained on the screen until either the S+ or S was touched. If
the subject touched the screen during the 15 sec intertrial interval,
then the 15 sec intertrial interval was restarted from that time. The
subjects were first required to learn problems one to five
concurrently. The subjects performed one session of this task every day
until they attained criterion of 90% correct responses made within a
single session. In each of these sessions the set of five problems was
repeated in the same sequence until the subject had made 100 correct
responses. On the next day after attaining criterion on problems one to
five, the subjects were required to learn problems 6 to 10 concurrently. The subjects performed one session of this task every day
until they attained criterion of 90% correct responses made within a
single session. In each of these sessions the set of five problems was
repeated in the same sequence until the subject had made 100 correct
responses. On the next day after attaining criterion on problems 6 to
10, the subjects were required to learn problems 1 to 10 concurrently. The subjects performed one session of this task every day until they
attained criterion of 90% correct responses made within a single
session. In each of these sessions, the set of 10 problems was repeated
in the same sequence until the subject had made 100 correct responses.
In all of these sessions, when the 100th correct response was made the
automated lunchbox opened immediately to make available the subject's
daily meal, as described above.
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Figure 4.
Examples of how three different discrimination
problems from experiment 2 appear to subjects (reproduced in gray
scale) when stimuli are presented in the context of digitized images of
unique complex scenes. For each of three different problems the figure illustrates how the scene appears with the positions of the S+ and S
reversed.
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RESULTS |
Experiment 1: identification of familiar objects presented in
new views
In stage A the subjects were required to learn 40 concurrent discrimination problems to criterion with digitized images
of objects presented in one of three different views. The CON group made a mean of 120 errors before attaining criterion in stage A,
whereas the PRh group made a mean of 214 errors. After attaining criterion in stage A the subjects were tested on the same problems in
stage B but with the objects presented in similar but previously unseen
views. Errors to criterion from stage B in which the subjects had to
identify familiar objects in new views are illustrated in Figure
5. The CON group made a mean of 11 errors
before attaining criterion on stage B, whereas the PRh group made a
mean of 41 errors, which was significantly greater than the number of
errors made by the CON group (Wilcoxon rank sum W test: W = 15;
p = 0.05; one-tailed test). Thus the PRh group was
significantly impaired relative to the CON group at performing a set of
well learned concurrent discrimination problems when the objects were
presented in new views.
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Figure 5.
Mean errors to criterion made by each group in
stage B of experiment 1 in which the 40 concurrent discrimination
learning problems that were learned to criterion in stage A were
retested using new views of each of the objects in stage B. Individual scores for each subject are also plotted (triangles).
CON, n = 3; PRh,
n = 3.
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Experiment 2: identification of familiar objects presented
in scenes
In experiment 2 the subjects were required to learn a set 10 concurrent discriminations problems to criterion between pairs of
objects presented in scenes. The subjects were familiar with the
objects and with the object-reward contingencies, but they had not
experienced these objects presented in the context of digitized images
of complex scenes before. Errors to criterion from experiment 2 in
which the subjects had to identify familiar objects presented within
scenes are illustrated in Figure 6. The CON group made a mean total of 123 errors before attaining criterion on
this task, whereas the PRh group made a mean of 246 errors, which was
significantly greater than the number of errors made by the CON group
(Wilcoxon rank sum W test: W = 15; p = 0.05; one-tailed test). Thus the PRh group was significantly impaired relative to the CON group at performing a set of well learned concurrent discrimination problems when each of the pairs of objects was presented in the unfamiliar context of a unique complex scene.
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Figure 6.
Mean total errors to criterion made by each group
in experiment 2 in which 10 well learned concurrent discrimination
problems were retested with each of the 10 pairs of objects presented
in a context not experienced before, that is, with each pair of objects embedded within a digitized image of an unique scene. Individual scores
of each subject are also plotted (triangles).
CON, n = 3; PRh,
n = 3.
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DISCUSSION |
The perirhinal cortex ablations in all three cases were
essentially as intended, with only slight and largely unilateral damage to laterally adjacent TE. This inadvertant cortical damage is therefore
unlikely to be the cause of the large behavioral effects we report. The
behavioral effects of the ablation are also unlikely to be attributable
to inadvertent white matter damage. The histological slides show
degeneration in the white matter underlying the perirhinal cortex, an
expected consequence of the cortical ablation; however, little or no
damage to the white matter occurred as a result of direct mechanical
damage to the white matter during surgery. In previous studies in which
perirhinal cortex ablation was combined with ablation of the
parahippocampal gyrus or hippocampus (Zola-Morgan et al., 1989, 1993),
branches of the posterior cerebral artery that cross the
parahippocampal gyrus to supply the inferior temporal gyrus would
necessarily have been severed in the course of making the combined
ablations, and it remains unclear to what extent the behavioral effects
reported in these studies may be attributable to interruption of the
blood supply to TE. Indeed, Gaffan and Lim (1991) demonstrated that
pial section along the medial boundary of TE, thereby interupting the
blood flow in the posterior cerebral artery en route to TE, can affect
visual discrimination learning even without producing large infarcts in
TE. In contrast, in the course of making perirhinal cortex ablation
alone, as in the present study, the blood supply to TE is not
interrupted because the perirhinal cortex receives its blood supply
principally from the middle cerebral artery. Thus we attribute the
behavioral impairments reported in this study to the loss of function
of the perirhinal cortex.
Current behavioral evidence is consistent with the hypothesis that
there is a deficit in object identification after perirhinal cortex
damage. The present experiments test this hypothesis more directly. In
experiment 1 subjects learned a concurrent discrimination learning task
between 40 pairs of familiar digitized images of objects to criterion.
The subjects were then tested on the same problems using similar but
previously unseen views of the objects. The subjects with perirhinal
cortex ablation were found to be impaired relative to normal controls
when tested with the new views (Fig. 5). This provides evidence that
perirhinal cortex ablation produces an impairment in object
identification and not just in memory. In experiment 2 subjects were
required to relearn 10 of the above problems but with each of the 10 pairs of objects presented in the unfamiliar context of a digitized
image of a unique complex scene. The subjects with perirhinal cortex
ablation were found to be impaired relative to normal controls in
learning this task to criterion (Fig. 6). This experiment similarly
provides evidence that perirhinal cortex ablation impairs object
identification and not just memory. We conclude that perirhinal cortex
ablation impairs the ability of subjects to identify familiar objects
presented in unfamiliar views and the ability of subjects to identify
familiar objects presented in the unfamiliar context of complex scenes. These results give considerable support to the hypothesis that the
perirhinal cortex has a role in object identification.
We further suggest that the nature of the impairment after perirhinal
cortex ablation is a deficit in the ability to process coherent
concepts of multiple individual objects, because monkeys with
perirhinal or combined perirhinal and entorhinal cortex damage have
been shown to be specifically impaired on tasks that require a
relatively high level of ability to process coherent concepts of
multiple individual objects. The pattern of impairments found in both
recognition memory and concurrent discrimination learning after these
lesions supports this hypothesis. DMS and DNMS with large stimulus set
sizes are impaired, whereas DMS with severely restricted set sizes is
unimpaired (Murray et al., 1989; Gaffan and Murray, 1992; Meunier et
al., 1993; Eacott et al., 1994; Gaffan, 1994b). Likewise, new
postoperative concurrent discrimination learning with small set sizes
is unimpaired (Gaffan and Murray, 1992; Eacott et al., 1994; Buckley
and Gaffan, 1997), whereas concurrent discrimination learning with
larger set sizes is impaired (Buckley and Gaffan, 1997). Other tasks
that require relatively high levels of ability to process coherent
concepts of multiple individual objects have been found to be
selectively impaired after perirhinal cortex ablation. These include
concurrent discrimination learning with multiple foils (Buckley and
Gaffan, 1997), concurrent discrimination learning with objects
presented in different views in each trial (Buckley and Gaffan, 1998a),
identification of new views of familiar objects (see experiment 1),
identification of familiar objects subsequently presented in the
context of unfamiliar scenes (see experiment 2), visual
stimulus-stimulus association learning (Murray et al., 1993; Buckley
and Gaffan, 1998b), and configural learning (Buckley and Gaffan,
1998b). In marked contrast, tasks that do not require a relatively high
level of ability to process coherent concepts of multiple individual
objects, such as color discrimination (Buckley et al., 1997) and simple
spatial discrimination learning (Gaffan, 1994b), are unimpaired.
Reassessment of the role of the perirhinal cortex in light of the
recent behavioral data therefore provides strong support for the
hypothesis that perirhinal cortex damage impairs object identification
and is consistent with our suggestion that the deficit lies in the
subject's ability to process coherent concepts of multiple individual
objects.
This hypothesis is also supported by electrophysiological and
anatomical evidence. Saleem and Tanaka (1996) indicated that the
perirhinal cortex may receive convergent inputs from multiple widely
distributed sites in the ventral part of anterior TE. This suggests
that different moderately complex features of objects represented by
distant columns in TE (Fujita et al., 1992; Kobatake and Tanaka,
1994; Tanaka, 1996) could be associated together in the perirhinal
cortex to represent whole objects. In addition to the prominent inputs
from the laterally adjacent unimodal visual areas TE and TEO, the
perirhinal cortex also receives projections from diverse unimodal and
polymodal areas of association cortex (Suzuki and Amaral, 1994a). The
perirhinal cortex is therefore in a position to associate information
about stimuli from different modalities, which is consistent with the
proposal that the perirhinal cortex has a role in processing coherent
concepts of individual objects. Also consistent with this scheme, cells
in the perirhinal cortex and some parts of TE (subdivisions TE1 and
TE2) (Seltzer and Pandya, 1978), but not in other areas in the inferior
temporal cortex, have a higher concentration of cells that show
recognition-related responses for specific stimuli in that they respond
more strongly to the first than to subsequent presentations of
unfamiliar stimuli (Fahy et al., 1993). Furthermore, the perirhinal
cortex has recently been functionally doubly dissociated from the
middle temporal gyrus (MTG), part of TE (Buckley et al., 1997). Monkeys
with MTG ablations were impaired at color discrimination but unimpaired at object recognition memory, whereas monkeys with perirhinal cortex
ablation showed the reverse pattern of impairments. This further
supports the idea that whereas TE and TEO process information about
features of objects, the perirhinal cortex processes knowledge about
specific individual objects.
A major defining feature of the perirhinal cortex is its robust
interconnections with the hippocampal formation via the entorhinal cortex (Van Hoesen and Pandya, 1975; Insausti et al., 1987; Suzuki and
Amaral, 1994b; Suzuki, 1996a,b). In both monkeys and humans the
hippocampal system has been implicated in scene memory. Monkeys with
fornix transection were severely impaired in a nonspatial scene memory
task (Gaffan, 1994c). Such impairment in memory for a discrete event
involving a particular object in a particular background may be
analogous to the memory impairment for discrete personally experienced
events that follows fornix damage in humans (for review, see Gaffan and
Gaffan, 1991). Scene memory requires information about object identity
to be combined with information about visuospatial relationships
between objects; consistent with this, a recent disconnection study
showed that interaction between the perirhinal cortex and the fornix is
important for scene memory (Gaffan and Parker, 1996). The role of the
perirhinal cortex has been differentiated from that of the fornix
(Gaffan, 1994b), and in light of such dissociations it has been
suggested that there is a loosely hierarchical arrangement of function
in the temporal lobe in which the specialization of memory systems is
conferred by specialization of their anatomical connections to other
structures (Gaffan, 1996; Gaffan and Hornak, 1997a; Buckley and Gaffan,
1998b); for instance, information about isolated features can be
associated together and combined with nonvisual object qualities in the
perirhinal cortex, and information about individual objects can be
combined in the hippocampus with spatial information to represent a
spatially organized scene. The present study provides further evidence
that the role of the perirhinal cortex can no longer be considered to
be restricted to object memory but that it is also involved in object
identification. This evidence further erodes the distinction as to
whether certain cortical areas should be ascribed as largely perceptual
or mnemonic in function. Indeed, it has been suggested that the
cortical plasticity that underlies perceptual learning and memory is
not fundamentally different (Gaffan, 1996). Evidence that memory
retrieval is retinotopically organized (Gaffan and Hornak, 1997b)
implies that the function of retinotopic cortical areas, usually
thought of as being perceptual in function, may be to maintain a
representation of the visual world based on both retinal input and
memory. Conversely, it remains to be seen to what extent perceptual
impairments toward scenes, in addition to impairments in memory, may
follow damage to the hippocampal system.
To conclude, the present experiments have shown that perirhinal cortex
ablation impairs the ability of monkeys to identify familiar objects
presented in new views and impairs the ability of monkeys to identify
familiar objects presented in the unfamiliar context of complex scenes.
These results demonstrate that the perirhinal cortex has a broader role
in visual object memory than was previously known, and along with
recent behavioral, antatomical, and electrophysiological data they
support the hypothesis that the perirhinal cortex has a role in the
visual identification of objects. We suggest that the perirhinal cortex
is crucially involved in processing coherent concepts of individual
objects. An impairment in this process could underlie the pattern of
deficits that follow perirhinal cortex ablation in both visual object
recognition memory and visual associative memory.
| |
FOOTNOTES |
Received Aug. 14, 1997; revised Dec. 22, 1997; accepted Jan. 6, 1998.
This research was supported by the Medical Research Council (UK).
Correspondence should be addressed to Mark J. Buckley, Department of
Experimental Psychology, Oxford University, South Parks Road, Oxford,
OX1 3UD, UK.
| |
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Top
Abstract
Introduction
