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The Journal of Neuroscience, January 1, 1999, 19(1):495-502
Functionally Dissociating Aspects of Event Memory: the Effects of
Combined Perirhinal and Postrhinal Cortex Lesions on Object and Place
Memory in the Rat
Timothy J.
Bussey,
Janice L.
Muir, and
John P.
Aggleton
School of Psychology, Cardiff University, Cardiff CF1 3YG Wales,
United Kingdom
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ABSTRACT |
Reciprocal interactions between the hippocampus and the perirhinal
and parahippocampal cortices form core components of a proposed
temporal lobe memory system. For this reason, the involvement of the
hippocampus in event memory is thought to depend on its connections
with these cortical areas. Contrary to these predictions, we found that
NMDA-induced lesions of the putative rat homologs of these cortical
areas (perirhinal plus postrhinal cortices) did not impair performance
on two allocentric spatial tasks highly sensitive to hippocampal
dysfunction. Remarkably, for one of the tasks there was evidence of a
facilitation of performance. The same cortical lesions did, however,
disrupt spontaneous object recognition and object discrimination
reversal learning but spared initial acquisition of the discrimination.
This pattern of results reveals important dissociations between
different aspects of memory within the temporal lobe. Furthermore, it
shows that the perirhinal-postrhinal cortex is not a necessary
route for spatial information reaching the hippocampus and that object
familiarity-novelty detection depends on different neural substrates
than do other aspects of event memory.
Key words:
episodic memory; event memory; spatial memory; object
recognition; perirhinal cortex; postrhinal cortex; temporal lobe; rat
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INTRODUCTION |
Processing of a complex event memory
likely involves the association of information from multiple brain
regions. One such contributing region may be the
perirhinal-parahippocampal cortex (Brown, 1990 ; Squire and
Zola-Morgan, 1991; Eichenbaum et al., 1994; Gaffan and Parker, 1996),
which has dense, reciprocal connections with the hippocampus (Deacon et
al., 1983; Suzuki and Amaral, 1994). Indeed, it has been proposed that
the involvement of the hippocampus in event memory depends on its
connections with this cortical area (Squire and Zola-Morgan, 1991;
Eichenbaum et al., 1994). A direct prediction is that
perirhinal-parahippocampal cortex damage should lead to hippocampal
dysfunction and that it should not be possible to obtain functional
double dissociations between these two regions.
Contrary to these predictions, some studies have revealed dissociations
between fornix and perirhinal cortex lesions (Gaffan, 1994a; Ennaceur
et al., 1996). This is noteworthy, because fornix lesions partially
disconnect the hippocampus and mimic many of the effects of
hippocampectomy. In such studies, lesions of perirhinal or perirhinal
plus postrhinal cortex (thought to be the homolog of parahippocampal
cortex in the monkey; Burwell et al., 1995) impaired spontaneous object
recognition but spared certain tests of spatial memory (Ennaceur et
al., 1996; Aggleton et al., 1997; Ennaceur and Aggleton, 1997). The
opposite pattern of results was obtained after fornix lesions (Ennaceur
et al., 1996, 1997). These findings raise the question of whether the
visual information required by the hippocampus in spatial memory tasks
must necessarily come from the perirhinal and postrhinal cortices.
Resolving this issue is important for understanding the neurobiology of
event memory; although spatial memory is not directly equivalent to event memory, it is an important attribute that is likely to depend on
hippocampal function (Gaffan, 1994b). The foregoing results thus
suggest important dissociations between aspects of event memory, namely
of visual object processing in temporal cortex and spatial processing
in the hippocampal system (O'Keefe and Nadel, 1978). To test this
possibility, however, it is vital to use spatial tasks that
unambiguously test allocentric spatial memory, because it is this form
of spatial processing that is thought to depend critically on the hippocampus.
Accordingly, rats with excitotoxic lesions of the
perirhinal-postrhinal (PPRH) cortex were tested with two well
characterized tests of allocentric spatial memory using the Morris
water maze and the radial arm maze. To confirm the functional efficacy
of the lesions, the same animals were tested on a spontaneous object recognition task. Finally, to extend our investigations into the involvement of these areas in visual processing, the rats were also
tested on rewarded one-pair object discriminations and reversal.
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MATERIALS AND METHODS |
Surgical and histological methods
Fifteen adult male rats (DA strain; Bantin-Kingman, Hull, UK)
received bilateral injections of NMDA in five sites in the PPRH cortex. This PPRH group was compared with 13 control (CONT) rats that
received sham surgeries. All animals were deeply anesthetized by
intraperitoneal injection (60 mg/kg) of pentobarbitone sodium (Sagatal,
Rhône Mérieux) and then placed in a stereotaxic head holder
(David Kopf Instruments, Tujunga, CA) with the nose bar at +5.0. The
scalp was then cut and retracted to expose the skull. For the PPRH
lesion, injections of 0.2 µl of 0.09 M NMDA (Sigma, Poole, UK) dissolved in phosphate buffer, pH 7.2, were made
through a 1 µl Hamilton syringe into five sites in each hemisphere.
Each injection was made gradually over a 5 min period, and the needle was left in situ for an additional 4 min before being
withdrawn. The stereotaxic coordinates relative to ear-bar zero were as
follows: anteroposterior (AP) +3.9, lateral (L) ±5.9,
dorsoventral (DV) +2.0; AP +2.4, L ±6.1, DV +1.6; AP +0.6, L ±6.2, DV
+2.5; AP  0.8, L ±6.2, DV +2.7; and AP 0.8, L ±6.2, DV +4.3. The
CONT animals received exactly the same initial surgery, i.e.,
craniotomy, but no injections were made. At the completion of all
surgeries, the skin was sutured, and an antibiotic powder
(Acramide; Dales Pharmaceuticals, Skipton, UK) was applied.
On completion of the experiment, all animals were killed with an
overdose of Euthatal (Rhône Mérieux) and perfused
intracardially with saline, followed by 10% formol saline. The brains
were then removed and placed in 10% formol saline for a minimum of 2 hr. After fixation, the brain was transferred to 20% sucrose in 0.2 M phosphate buffer and left overnight. The brain was then
cut on a freezing microtome into 60 µm coronal sections, and sections were mounted and then stained with cresyl violet, a Nissl stain.
Behavioral methods
Testing began ~30 d after surgery. For some of the
postoperative test period (radial arm maze task; see below), the
animals were placed on a restricted diet, but they were weighed
regularly and their food was adjusted to ensure that they did not fall
below 85% of normal body weight. Throughout the study, all animals had access to water ad libitum. All animals were tested on
the various tasks in the order in which they are described below.
Morris swim task. Eight equidistant start locations [north
(N), south (S), east (E), west (W), NE, SE, NW, and SW] were
allocated, thus delineating four quadrants (NE, SE, NW, SW) of the
pool. In each trial, a rat was placed in the pool facing the wall at one of the eight start locations. To escape the cool (25°C) water, the rat swam to an invisible platform, which was positioned in the same
place in the same quadrant throughout the acquisition sessions. The
position of the platform and the starting positions for each trial were
counterbalanced between rats. Animals (PPRH, n = 15;
CONT, n = 13) received four trials per session, one
session per day, for ten d. Each acquisition trial was terminated
either when the animal located the hidden escape platform or after 120 sec had elapsed. If the rat located the platform, it was allowed to
remain there for 30 sec. If the rat failed to find the platform after
120 sec, it was placed on the platform and allowed to remain on it for
60 sec. In the next trial, the rat was placed in the pool at the second
start location, and so on for four trials. On the eleventh day, a probe
trial was given in which the platform was removed from the pool. Each
rat was placed at a start position opposite to where the platform had
been located.
Radial arm maze task. The rats were tested next in a
standard eight-arm radial maze in which two reward pellets were placed at the end of each arm at the start of each test session (one session
per day). Normal rats learn the most effective strategy, which is to
enter each arm only once. The requirement to update the memory of those
arms already entered ensures that the task taxes spatial working
memory. Testing was performed in an eight-arm radial maze made of wood.
This apparatus was of a standard design, with the exception that the
arms had walls made of clear Perspex to ensure that the rats
could not cross directly from one arm to another. Each arm was 87 cm
long and 10 cm wide; the side walls were 24 cm high. At the end of each
arm was a food well 2 cm in diameter and 0.5 cm deep. Each arm led
through a clear Perspex guillotine door, which was 14 cm high to the
central octagonal arena and 34 cm in diameter. Each of these guillotine
doors had strings attached, enabling the experimenter to open the doors either individually or simultaneously. The arms of the maze were mounted on a turntable so that they stood 62 cm off the ground. The
turntable enabled the arms, but not the central platform, to be rotated
through 360°. The floor of the testing room was marked so that the
position of the maze could be standardized in relation to the room
cues. Lighting was provided by two fluorescent lights mounted 180 cm
above the maze.
After habituation to the maze, training consisted of 12 trials, one per
day. (One PPRH and three CONT animals would not explore the maze; these
animals were therefore excluded from this phase of the study. The
numbers of subjects in each group for this phase of the study were
therefore PPRH, n = 14 and CONT, n = 10.) At the start of each trial, all eight arms were baited with two 45 mg reward pellets (Sandown Instruments). The animal was placed in the
central arena and was allowed to explore the maze and collect pellets
until all eight arms had been visited. The number of arm entries taken
to retrieve all pellets and the number of correct choices (visits to
baited arms) were recorded. After the 12 acquisition days, rats were
given five trials, one per day, designed to control for the possible
use of nonallocentric strategies. The rat was placed in the maze as
usual and allowed to collect pellets from any four arms. It was then
removed from the apparatus and placed in a carrying cage for 30 min.
During this period, the maze was rotated 45° either clockwise or
counterclockwise, and the four unvisited positions were baited. Now the
unvisited baited arms were in the same location relative to the room
cues as they would have been had the maze not been rotated but the
actual arms had changed. After the delay, the rat was placed back in
the central arena and was allowed to revisit the four remaining baited
arms. The experimenter recorded the number of errors (entries into
unbaited arms) made after the delay.
Spontaneous object recognition test. The apparatus consisted
of an open arena (100 × 100 × 46 cm) made of wood, the
inside of which was painted gray. The floor was covered with sawdust. The arena was situated in a room containing features such as a door,
light fixtures, and a video camera. Triplicate copies were obtained of
the objects to be discriminated, which were made of glass, plastic, or
metal. For any given test, the pairs of objects to be discriminated
were typically composed of the same material so that they could not
readily be distinguished by olfactory cues. All rats (PPRH,
n = 15; CONT, n = 13) received a series
of habituation sessions before the first test.
Each test session consisted of two phases. In the initial sample phase,
two identical objects (A1 and A2) were placed in the far corners of the
arena, each 10 cm from the side wall. A rat was then placed in the
middle of the arena, and the total time spent exploring the two objects
was determined from video-taped recordings. Exploration of an object
was defined as directing the nose to the object at a distance of <2 cm
and/or touching it with the nose. This "sample phase" ended when
the rat had explored the two identical objects for a total of 25 sec.
The rats' behavior was assessed from video recordings, and all
assessments were blind.
After a delay of 15 min, the rat was reintroduced to the arena
("choice phase"), which now contained a third identical copy of the
familiar object (A3) and a new object (B). These were placed in the
same locations as the sample stimuli. The location of the two choice
objects was counterbalanced between rats and across sessions. All rats
were tested with two sets of objects and received a total of four
tests. Thus, in test 1, object A was the sample and object B was
the novel alternative. For test 2 (48 hr later), their roles were
reversed, i.e., object B was the sample and object A was the
"novel" alternative. For tests 3 and 4, new pairs of objects were
used (C and D) in a similar counterbalanced order. The time spent
exploring the novel and familiar objects was recorded for the all 3 min
of the choice session, but attention was focused on the first minute,
during which object discrimination is typically greatest (Dix and
Aggleton, 1998). From these results, we calculated d1, the difference
in time spent exploring the novel and familiar objects for each of the
two sets of objects, and d2, the proportion of total exploration time
spent exploring the novel objects for each pair of objects (i.e., d1
divided by the total time spent exploring the objects). This latter
measure takes into account individual differences in the total amount
of exploration time.
Object discriminations and reversal. The apparatus, a Grice
box, consisted of a small rectangular start box (13 × 18 cm)
separated from a triangular test area by a guillotine door. The far
wall of the test area was 43 cm long and 43 cm from the guillotine door. The walls of the apparatus, which were made of aluminum, were 24 cm high. The floor contained two food wells, 2.5 cm in diameter,
positioned 35 cm from the start box. An aluminum partition, which
protruded 16 cm from the far wall, ensured that the rats could not run
directly between the two food wells, which were 21 cm apart. During
pretraining, the rats were trained to run from the start box to find
food pellets in either food well by pushing aside a circular wooden
disk (4.5 cm diameter, 1.5 cm high). This was followed by two object
discriminations. The objects were comparable to those used in the
object recognition task. For half of the animals in a group, one of the
two objects (S+) was rewarded with two food pellets, and for the other
half, the other object was rewarded. For each trial, the guillotine
door was raised, and the rat were allowed to select one object. A
choice occurred when the rat had displaced the object sufficiently to reveal the edge of the food well. The left-right positions of the
objects were varied according to a pseudorandom schedule, and there was
no correction procedure.
All rats (PPRH, n = 15; CONT, n = 13)
were tested on the first object discrimination for 6 d, followed
by the second object discrimination for 4 d. Each session
consisted of 20 trials. Next, the rats were given a 1 week retention
period, after which the second object discrimination was
re- tested for one session, followed by a 2 week retention
period, after which this same discrimination was retested for three
sessions. (One PPRH animal suddenly became ill during this test and was
therefore excluded from the remainder of the study; the numbers of
subjects in each group for this phase of the study were therefore
PPRH, n = 14 and CONT, n = 13.)
Finally, animals were tested on a reversal of this discrimination in
which reward contingencies were reversed (i.e., the S+ became the S and vice versa). (One PPRH animal would not work under the reversal condition and was therefore excluded; the numbers of subjects in each
group for this phase of the study were therefore PPRH, n = 13 and CONT, n = 13). Reversal
testing continued for 12 sessions, one session per day. All data from
discriminations and reversal were analyzed across sessions with two-way
ANOVA. Reversal data were further analyzed in terms of errors required
to progress between three learning stages: "perseveration" (<6 of
20 correct, during which animals are responding to the previously
rewarded stimulus); "chance performance" (6-13 of 20); and "new
learning" (>14 of 20, during which animals are responding to the
currently rewarded stimulus) (for review, see Jones and Mishkin, 1972;
Dias et al., 1996; Bussey et al., 1997).
Activity. After completion of the above tests, all rats
(PPRH, n = 13; CONT, n = 13) were
placed in novel test cages (56 × 39 × 19 cm) in a novel
room. Activity was measured using pairs of photobeams situated 20 cm
apart and 18 cm from the end of the cage (Paul Fray Ltd.,
Cambridge, UK). The total number of beam breaks was recorded.
Data were gathered in 12 intervals of 10 min each.
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RESULTS |
Histological results
Histological analysis showed that PPRH animals had very extensive
cellular loss throughout the perirhinal and postrhinal cortices, as
well as area TE (Figs. 1,
2). The lesions started close to the
rostral border of the perirhinal cortex and continued caudally throughout the postrhinal cortex. Within this region, all neurons had
disappeared. In two animals, there was some unilateral sparing of the
most rostral perirhinal cortex. The lesions consistently extended
ventrally to include adjacent parts of the pyriform cortex and lateral
entorhinal cortex. The cellular damage also extended dorsally so that
in 13 cases it reached the ventral border of the primary auditory
cortex. In eight cases, there was unilateral cell loss in a very
restricted portion of the hippocampal CA1 field, and in a further three
cases, this damage was bilateral.
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Figure 1.
Coronal sections illustrating the extent of the
largest (gray) and smallest
(black) lesions of the PPRH cortex. The
numbers correspond to the approximate position from
bregma (Paxinos and Watson, 1997).
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Figure 2.
Photomicrographs showing the extent of a typical
PPRH lesion. Left, The lesion in the left and right
hemispheres at approximately bregma 4.0 and 4.8 (Paxinos and
Watson, 1997). Right, The lesion in the left and right
hemispheres at approximately bregma 6.8 and 8.0 (Paxinos and
Watson, 1997). Note the very small amount of CA1 damage in the
left section in the right panel. This is
a typical amount of CA1 damage in cases in which hippocampal damage
occurred.
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Behavioral results
Morris water maze
Performance, as measured by latency to reach the platform, showed
that the PPRH and CONT animals acquired the task at very similar rates
(main effect of group, F < 1; group × session
interaction, F(9,234) = 1.2) (Fig.
3a). Analysis of swim path
lengths similarly did not reveal any group differences (main effect of
group, F < 1; group × session interaction,
F < 1) (Fig. 3b). A probe trial in session
11 in which the hidden platform was removed showed that both groups
favored the quadrant where the platform had been and that there was no
group difference (F < 1) (Fig. 3c).
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Figure 3.
Performance of PPRH and CONT animals on the
Morris swim task. a, Mean escape latencies during
acquisition. b, Mean swim path lengths during
acquisition. c, Percentage of time spent in the four
quadrants during a probe test conducted after the tenth acquisition
session. There were no differences between the groups during either
test.
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Radial arm maze
Both groups rapidly acquired the radial maze task over 12 sessions
(main effect of group: number of arms visited,
F(1,22) = 2.2; number correct in first eight
choices, F(1,22) = 2.9) (Fig. 4a,b), but
paradoxically the PPRH animals showed the better level of performance
on some accuracy measures [group × trial interaction: number
correct in first eight choices, F(11,242) = 1.98; p < 0.05; analysis of simple effects revealed
superior performance of PPRH group in trials 3 (p < 0.05), 11 (p < 0.001), and 12 (p < 0.05)] (Fig.
4b). Acquisition was immediately followed by five sessions in which each rat was removed from the maze as soon as the first four
arms had been selected. During a retention interval of 30 min, the maze
was rotated 45° (clockwise or counterclockwise), and the arms were
rebaited so that the unvisited arms were still in the same spatial
position with respect to the room cues. The rat was then placed
back in the central arena and monitored until all four baited arms had
been visited. Both PPRH and CONT animals performed accurately after
the delay (F < 1) (Fig. 4c), showing that
both groups relied on allocentric cues to solve the task.
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Figure 4.
Performance of PPRH and CONT animals on the
radial arm maze task. a, Mean number of arms visited to
obtain reward from all eight arms. b, Number correct in
the first eight choices. c, Total number of errors
committed across five sessions in which the maze was rotated during a
30 min delay period.
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Spontaneous object recognition
The effectiveness of the cortical lesion was confirmed with a
spontaneous test of object recognition. Normal rats demonstrate object
recognition by showing a spontaneous preference for a novel object
versus a familiar one. Unlike the CONT group, the PPRH rats showed
abnormally low preference levels for the novel object, as measured by
the difference in time spent exploring the novel and familiar objects
(d1, F(1,26) = 10.1; p = 0.004)
(Fig. 5a) and by the ratio of
total exploration time spent with the novel object (d2,
F(1,26) = 8.1; p = 0.008) (Fig.
5b).
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Figure 5.
Performance of PPRH and CONT animals on the
spontaneous recognition test. a, Difference in time
spent exploring the novel and familiar objects (d1).
b, Ratio of time spent exploring the novel object
(d2). **p < 0.01, significantly
poorer performance of PPRH animals relative to controls.
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Object discrimination and reversal
Despite the recognition deficit, the PPRH rats were able to
perform a pair of object discriminations, confirming their ability to
distinguish between objects. Both the PPRH and CONT rats rapidly learned to select the rewarded object (main effect of group,
F(1,26) = 3.0; group × session
interaction, F(5,130) = 1.2). The first discrimination was immediately followed by a second, with a new pair of
objects. Again, there were no group differences (main effect of group,
F(1,26) = 2.1; group × session
interaction, F < 1). After the second object
discrimination, a 1 week retention interval was interposed, and the
rats were retested. There were no group differences in performance
after the 1 week interval (F(1,26) = 1.5). After
a subsequent 2 week interval, rats were retested over a 3 d
period, and PPRH animals were significantly impaired (main effect of
group, F(1,25) = 5.1; p < 0.05), but analysis of simple effects revealed that by the third day of
testing PPRH animals had attained the same performance level as
controls. Finally, when the reward contingencies of this second
discrimination were reversed, the previously rewarded object now being
nonrewarded and vice versa, PPRH animals were significantly impaired
relative to controls (main effect of group,
F(1,24) = 5.8; p = 0.02;
group × session interaction F(11,264) = 3.3; p < 0.001). Reversal data were further analyzed
in terms of errors required to progress between three criteria
delineating three learning stages: perseveration, chance performance,
and new learning (Jones and Mishkin, 1972; Dias et al., 1996; Bussey et
al., 1997). The lack of a significant group × stage interaction
(F < 1) suggests that errors were distributed approximately evenly across the three stages. However, PPRH rats tended
to make more errors during the perseverative and chance performance
stages than did controls.
Activity
Finally, the rats were given one 2 hr session in novel activity
cages fitted with photocells to measure spontaneous locomotor activity.
Data were analyzed in 12 intervals of 10 min each. The spontaneous
activity and habituation to the cages was very similar for the PPRH and
CONT groups (beam breaks during the first 10 min bin: PPRH, 151.13;
CONT, 154.3; beam breaks during final 10 min bin: PPRH, 30.6; CONT,
24.5; main effect of group, F < 1; group × interval interaction, F < 1). Thus, the selective
effects of the lesion reported above are unlikely to be attributable
to gross changes in arousal or motoric function.
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DISCUSSION |
This study provides the first comprehensive test of combined PPRH
cortex removal on allocentric spatial memory. The striking finding is
that this lesion can impair object recognition yet completely spare
spatial memory. Furthermore, the sparing of spatial memory was
independent of whether the task taxed spatial "working" or spatial
"reference" memory. These results are contrary to several influential theories of event memory that emphasize obligatory interactions between the hippocampus and the perirhinal and
parahippocampal cortices (Squire and Zola-Morgan, 1991; Eichenbaum et
al., 1994). Instead, they demonstrate a degree of independence between
different aspects of memory within the temporal lobe. This feature
needs to be accommodated in future models of a temporal lobe memory system.
Although spatial memory is not directly equivalent to event memory, it
is an important attribute that is likely to depend on hippocampal
function. Recall of an event includes the context or setting in which
the event took place, and this contextual information can have a
spatial component that is dependent on the hippocampus (Nadel and
Willner, 1980; Gaffan, 1994b). Object recognition, in contrast, does
not appear to depend on the hippocampus or fornix (Ennaceur et al.,
1996, 1997; Murray and Mishkin, 1998) but instead depends on the
perirhinal cortex (Meunier et al., 1993; Ennaceur et al., 1996). These
results show that the perirhinal cortex and hippocampus can operate
independently from one another, in a manner not predicted by current
influential models (Squire and Zola-Morgan, 1991; Eichenbaum et al.,
1994).
This is not the first study to indicate that perirhinal cortex lesions
can spare spatial memory (Ennaceur et al., 1996; Aggleton et al., 1997;
Ennaceur and Aggleton, 1997), but previous studies failed to include
the postrhinal cortex and/or failed to use tasks that are unambiguously
allocentric. The present findings show that the hippocampus does not
require visual information from either the perirhinal or postrhinal
cortices to mediate the performance of allocentric spatial tasks. This
inevitably raises the question of how spatial information reaches the
hippocampus. One possible clue comes from studies reporting that
electrolytic lesions of perirhinal cortex can disrupt performance of
spatial tasks in the water maze and radial arm maze (Wiig and Bilkey,
1994; Liu and Bilkey, 1998a,b). Comparison with the present study using axon-sparing excitotoxic lesions implicates fibers coursing through or
adjacent to the perirhinal and postrhinal cortices. These fibers now
require identification.
Whereas PPRH lesions had no effect on tests of spatial memory, these
same lesions significantly disrupted spontaneous object recognition,
thus confirming the efficacy of the lesions and replicating previous
studies (Ennaceur et al., 1996; Aggleton et al., 1997; Ennaceur and
Aggleton, 1997). Importantly, these lesions left intact the acquisition
of simple object discriminations (Aggleton et al., 1997), showing that
the object recognition deficit was not attributable to a general
inability to discriminate objects. Furthermore, this sparing of object
discrimination learning shows that the PPRH cortex is not necessary for
all forms of visual discrimination. This is in agreement with recent
reports showing that monkeys with lesions of perirhinal cortex are
impaired on object discrimination only under certain circumstances
(e.g., when the stimulus set size is large; Buckley and Gaffan, 1997). These results and the discrimination reversal deficit reported in the
present study also show that deficits after perirhinal cortex lesions
are not limited to recognition paradigms, consistent with the view that
this region may have a more general role in "object identification"
(Buckley and Gaffan, 1998; Murray et al., 1998).
In summary, the present dissociation not only shows that the perirhinal
and postrhinal cortices are not necessary routes for visual information
reaching the hippocampus but also that object familiarity-novelty
detection depends on different neural substrates than do other aspects
of event memory. This pattern of results cannot be accommodated within
the notion of a unitary medial temporal lobe memory system and reveals
the existence of important dissociations between different aspects of
memory within the temporal lobe. Combined with other studies, these
data support a dissociation between visual object processing in
temporal cortex and spatial processing in the hippocampal system. At
the same time, it must be acknowledged that these two forms of
information will often be integrated so that specific objects can be
situated within their spatial context. It is this integration for which
connections between temporal cortex and hippocampus are most likely
required. Indeed, in most situations, the encoding of complex event
memories will require such integration. Thus, these regions are
typically not independent of one another; rather, there is a continuum
of situations along which they interact to varying degrees. The present study investigates phenomena at both ends of this continuum.
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FOOTNOTES |
Received Sept. 14, 1998; revised Oct. 19, 1998; accepted Oct. 21, 1998.
This research was supported by a project grant from the Wellcome Trust.
We thank Alison Baird, Angie Morgan, and Charlotte Price for invaluable
assistance with behavioral testing and histology.
Correspondence should be addressed to Dr. Timothy J. Bussey, Laboratory
of Neuropsychology, National Institute of Mental Health, National
Institutes of Health, Building 49 Room 1B80, Bethesda, MD 20892.
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Top
Abstract
Introduction
