C .J. Maclean et al. Brain Research 888 2001 34 –50
37
maintain motivation, the monkeys were fed their normal i.p., the monkeys were deeply anaesthetised with 1.0 ml
daily diet of bread, fruit and monkey pellets after testing sodium pentobarbitone 200 mg ml, i.p. and perfused
each day. Three types of task were used: coloured object transcardially with 250 ml ice-cold phosphate-buffered
Object discrimination either as single discriminations or saline PBS, pH 7.4, followed by 300 ml ice-cold 4
as 10 concurrent discriminations, black object Shape paraformaldehyde in 0.1 M phosphate buffer, pH 7.4. The
discrimination, and spatial discrimination. brains were removed and postfixed for 2 h in ice-cold 4
For Object discrimination, two small plastic coloured paraformaldehyde in phosphate buffer, after which they
junk objects were presented over two food-wells in the were inspected visually. Diagrammatic drawings were
WGTA and the monkey had to learn to displace the made of the cortical damage in monkeys in Groups L1 and
appropriate object to retrieve a small food reward usually L2 and the brains of monkeys in Group L2 were also
a piece of marshmallow. The left–right position of the photographed. The brains were then cut coronally into
two objects varied pseudorandomly but the reward was blocks that were transferred to 30 sucrose–PBS at 48C
always found under the same object. For Shape discrimina- for 2 to 3 days. The blocks were transferred to fresh 30
tion, two small junk objects painted black all over were sucrose–PBS after 24 h. Using a freezing stage microtome,
used as stimuli. These two tasks differ in the type of sections were cut throughout the brain. Sections 40 mm
perceptual analysis needed for task solution. While were stained for acetylcholinesterase AChE activity
coloured objects can be distinguished by overall appear- [34,51] or with Cresyl Violet.
ance or by identifying differences in individual features e.g., differently coloured parts, the black objects can only
be distinguished by perceiving differences in the shape of
3. Results
the whole object. For spatial discrimination tasks, a four-hole test board
3.1. Postoperative behaviour was used in which there were two food-wells 4.5 cm apart
centre to centre on the left side of the test tray and two 3.1.1. Experiment 1
food-wells 4.5 cm apart on the right side of the test tray. Following surgery, the monkeys were transferred to
The distance between the inner food-wells was 10 cm. The large incubators maintained at |288C. All monkeys were
left side pair of food-wells, or the right side pair of given 0.2 ml paracetamol syrup if judged necessary. There
food-wells, was covered with two identical stimuli accord- was some fitting in three monkeys, which was controlled
ing to a pseudorandom schedule and the other two food- by one or two doses of benzodiazepine 0.1 ml of 2
wells were open and empty. For spatial learning, reward mg ml, i.m.. The monkeys were hand-fed and -watered as
was to be found under the left stimulus of the pair on every required and their physiological recovery over the next 2 to
trial, i.e., irrespective of the left right position of the pair 3 days was uneventful. Their capacity for self-care was,
of stimuli. This task could not be solved by the monkey however, compromised for a further 3 to 4 days by a
maintaining a particular bodily position within the WGTA. disinclination to drink and, to some extent, eat without
For spatial reversal, the reward was now to be found under assistance. Although they had good appetites, they ignored
the right stimulus of the pair irrespective of the left right the waterspout and most of the food, only eating food
position of the pair of stimuli on each trial. which they encountered accidentally. Some monkeys had
For each task, trials were presented until the monkey to be taught to use the waterspout by smearing the spout
had reached a predetermined criterion e.g., 27 correct with sugar syrup. Sometimes, when offered a piece of
responses in 30 consecutive trials, 27 30. If the criterion banana, they would not distinguish between the banana
was not reached within a predetermined number of trials and the hand of the person holding it, tending to nibble
e.g., 300 the monkey was deemed to have failed the task. both. They spent much time rooting about in the fleece that
In all these tasks the monkey learns to associate one of the lined the bottom of the incubator or cage. The monkeys
two stimuli or positions in the case of spatial discrimina- were uncharacteristically tame, even after making allow-
tion with reward i.e., one object or position acquires ance for their physiological recovery from surgery see
secondary reinforcing properties. In concurrent coloured Fig. 1. When left alone they lacked initiative and showed
object discrimination 10 pairs of coloured objects were little interest in their surroundings. On occasions this
presented to the monkey, one pair at a time over the amounted to ‘time out’, i.e., blank staring with or without
food-wells and in the same order pair 1, pair 2 . . . pair 10; a drifting head movement. Sometimes they orientated to a
pair 1, pair 2 . . . etc for each monkey until the monkey non-event. This gave the appearance of hallucinatory
reached criterion or performed a set number of trials. behaviour but obviously this cannot be proved. Thus, the
monkeys exhibited the ‘psychic blindness’, ‘paradoxical 2.4. Histology
tameness’, and ‘paresis of attention’ which form part of the ¨
Kluver–Bucy syndrome [33]. Their behaviour was in- Monkeys in Group L1 and L2 were perfused for
distinguishable from that exhibited by other marmosets histology 18–20 weeks after surgery for each experiment.
with bilateral suction ablations confined to the inferotem- After premedication with 0.05 ml ketamine 100 mg ml,
poral cortex which were studied contemporaneously [53].
38 C
surgery the four lesioned monkeys were assessed with a checklist twice each day see Table 1.
3.2. Cognitive testing 3.2.1. Experiment 1
For clarity, the design and results of each stage of Experiment 1 are described together. The mean learning
scores number of trials to criterion6S.E.M. for each group on each task are shown in Table 2. Data were
analysed for within- and between-group effects by analysis of variance ANOVA. Groups of tasks of the same type or
related tasks e.g., postoperative retention were analysed in a repeated measures general linear model design,
followed by post hoc comparisons between groups using t-tests. Where appropriate, the degrees of freedom were
reduced to take account of non-homogeneity of variances.
3.2.1.1. Preoperative testing. Before surgery, monkeys were tested on a number of tasks. The first was a simple
coloured object discrimination Object 1 presented until the monkeys had reached a criterion of 90 correct re-
sponses in 100 consecutive trials 90 100. This task provided the necessary training in the basic requirements
of task performance in the WGTA. This was followed by
¨ Fig. 1. Photograph of marmoset with Kluver–Bucy syndrome taken 6
two further simple coloured object discriminations, Object
weeks after bilateral transections of the temporal stem, amygdala and
2 to 27 30 and Object 3 to 9 10. This provided further
fornix. The marmoset is gently nibbling a gloved finger at an open cage
practice and prepared the monkeys for acquisition of
door. The aggressive bite of a normal marmoset is extremely painful, and most marmosets would attempt to escape through an open cage door.
different discriminations to a low criterion during concur- rent testing. The monkeys were then tested on a concurrent
By about 6 days after surgery most of the monkeys were coloured object discrimination task Conc 1 in which 10
capable of self-care and were returned to their home cages. pairs of coloured objects were presented, one pair on each
Testing was resumed 7 to 10 days after surgery. Per- trial in the same order, until an overall criterion of 90 100
formance in the WGTA was not compromised by the consecutive trials was reached see Fig. 2. This task was
behaviour described above. intended to place a burden on memory for objects. The
monkeys were then rested for about 30 days after which they were tested on retention of this concurrent discrimina-
3.1.2. Experiment 2 tion Ret Conc 1 to 90 100 see Fig. 2. This allowed us
Following surgery for Experiment 2, monkeys showed to assess whether this species was capable of retaining a
the same behavioural syndrome as described above. A concurrent discrimination over a period of time and
¨ more formal assessment of the Kluver–Bucy syndrome
ensured that these discriminations were well learnt. was made in these monkeys, in addition to the postopera-
Repeated-measures ANOVA on the preoperative tasks tive welfare charts kept for all monkeys. During the time
showed no group effect and no group3task interaction. that they were in incubators at least one week after
The two groups were, therefore, well matched for learning
Table 1 ¨
Signs of Kluver–Bucy Syndrome in monkeys in group L2 n54 Needing to be hand-fed and -watered beyond normal post-op care
4 4 monkeys Then only eating food that was accidentally encountered
4 4 monkeys Then rooting for food by smell, and plunging the face into the fleece
3 4 monkeys Unaggressively nibbling observers’ fingers
4 4 monkeys Nibbling faeces
3 4 monkeys Being extra tame relative to postoperative condition
4 4 monkeys Lacking behavioural initiative
4 4 monkeys Tolerating being touched on the nose, ears and body
4 4 monkeys Ignoring on-going events but ‘attending’ to non-existent events
4 4 monkeys
C .J. Maclean et al. Brain Research 888 2001 34 –50
39 Table 2
Mean learning scores 6S.E.M. for tasks used in Experiment 1 Tasks
Control group Lesion group
Post hoc tests ANOVA
Preoperative: Object 1 90 100
145645 215667
ns Group F
50.197 ns
1,8
Object 2 27 30 35615
24617 ns
Task F 513.5
P,0.001
4,32
Object 3 9 10 763
362 ns
Group3task F 50.76
ns
4,32
Conc 1 90 100 4096129
288668 ns
Ret Conc 1 90 100 46621
43627 ns
Postoperative: Ret Object 1 27 30
1865 20060
P,0.001 Group F
5492.18 P,0.001
1,8
2nd Ret Conc 1 90 100 663
471629 P,0.001
Task F 577.95
P,0.001
1,8
Group3task F 593.87
P,0.001
1,8
Easiest Conc 1 task 27 30 060
1769 ns
Group F 55.32
p,0.05
1,8
2nd easiest Conc 1 task 90 100 060
69638 ns
Task F 51.56
ns
1,8
Group3task F 51.56
ns
1,8
Object 4 27 30 1069
50618 P50.08
Group F 511.19
P,0.01
1,8
Object 5 90 100 060
38617 P50.06
Task F 50.59
ns
1,8
Group3task F 50.004
ns
1,8
Spatial left 27 30 85631
104644 ns
Group F 50.05
ns
1,8
Spatial right 90 100 60612
145631 P,0.05
Task F 54.40
P50.069
1,8
Group3task F 50.78
ns
1,8
Conc 2 90 100 99615
3356102 P50.08
Shape 1 27 30 1666
94635 P50.09
Group F 59.32
P,0.05
1,8
Shape 2 90 100 16612
141636 P,0.05
Task F 52.09
ns
1,8
Group3task F 52.12
ns
1,8
ability before surgery. Following a 30 day rest period, Object 1 to 27 30. They were deemed to have failed the
there was no difference between the groups on retention of task if criterion was not reached within 200 trials. They
the concurrent discrimination. All monkeys showed a were then tested on retention of the concurrent discrimina-
substantial reduction in learning score on retention testing tion 2nd Ret Conc 1 to 90 100 see Fig. 2. In this case
indicating that these discriminations were held within long- they were deemed to have failed the task if they did not
term memory reach criterion in 500 trials. Repeated-measures ANOVA
on these tasks showed a highly significant group effect 3.2.1.2. Postoperative testing. Retention of tasks learned
[F 5492.18, P,0.001], task effect [F
577.95, P,
1,8 1,8
preoperatively: Behavioural testing resumed 7–10 days 0.001], and group3task interaction [F
593.87, P,
1,8
after surgery. The monkeys were tested first on retention of 0.001].
Post hoc comparisons showed that the lesioned group was impaired relative to the control group on both re-
tentions. All lesioned monkeys failed to reach criterion in 200 trials of retention of Object 1. Four of five lesioned
monkeys failed to reach criterion on the concurrent re- tention task in 500 trials see Fig. 2. Since the original
learning scores for concurrent discrimination task had been below 500 trials for four of these five monkeys, this failure
represents an impairment in relearning as well as in retention.
The learning score to 9 10 for retention of each component discrimination of the concurrent discrimination
task was also calculated Fig. 3A. Where a monkey did not reach a criterion of 9 10 on a component discrimina-
tion, the total number of trials on that task for that monkey was used. Repeated measures ANOVA across the com-
Fig. 2. The effect of the lesion on learning and retention of concurrent
ponent discriminations revealed that there was a highly
discriminations before and after surgery Expt. 1. Histogram shows mean
significant group effect [F 523.04, P,0.001], a signifi-
1,8
trials to criterion 1S.E.M.. Conc 1 is first set of 10 concurrent
cant component effect [F 52.48, P,0.05] and a
9,72
discriminations learnt preoperatively, retained preoperatively and retained
group3component interaction [F 52.01, P,0.05]. Post
9,72
again postoperatively. Conc 2 is a new set of 10 concurrent discrimina-
hoc examination revealed that the lesioned group was
tions learnt postoperatively. See also Table 2. P,0.001, comparing lesioned and control groups.
significantly impaired on all but one of the component
40 C
0.001]. Post hoc analysis revealed a significant group difference at all levels of difficulty except the easiest.
3.2.1.3. Further testing
of tasks
relearnt postoper
- atively. Since the lesioned monkeys had failed to reach
criterion on both postoperative retention tasks and on all but one of the components of the retention of the concur-
rent discrimination task, it was important to consider the extent to which these monkeys were capable of maintain-
ing sustained performance in the WGTA. All monkeys were therefore retested to 27 30 on retention of the
component they had each found easiest to relearn in the concurrent discrimination task. All monkeys were then
retested to 90 100 on the component which they had each found second easiest to relearn in the concurrent discrimi-
nation task. Repeated-measures ANOVA on the relearning scores for these two tasks showed a significant group
difference over both tasks [F
55.32, P,0.05]. Post hoc
1,8
comparisons did not reach significance on either task; all control monkeys scored zero on both these tasks whereas,
for the lesioned group, scores ranged from 0–50 on the first task and 0–200fail on the second task. Thus some
lesioned monkeys who had been able to master a task to a criterion of 9 10 had further difficulty carrying perform-
ance through to a criterion of 27 30 or 90 100. This could be interpreted as a mnemonic impairment which is evident
after the visual analysis of objects has been sufficient to produce discrimination performance to a low criterion.
Acquisition of visual discriminations: After retention testing, the marmosets were tested on acquisition of a new
simple coloured object discrimination Object 4 to a criterion of 27 30 and a second new simple coloured
Fig. 3. A Postoperative retention of a concurrent discrimination set first
object discrimination Object 5 to a criterion of 90 100.
learnt prior to surgery 2nd Ret Conc 1 in Table 2. B Postoperative learning of a new set of 10 concurrent discriminations Conc 2 in Table
Repeated measures ANOVA revealed a significant group
2. Histogram shows mean trials to criterion 1S.E.M. for each
effect [F 511.19, P,0.01], but no task effect and no
1,8
component discrimination which are ordered according to increased task
group3task interaction. Post hoc comparisons approached
difficulty for the control group.
significance for both tasks. Scores for these two tasks were zero or near zero for control monkeys. Thus lesioned
monkeys were impaired on acquisition of visual discrimi- nations even where the tasks were extremely easy for
discriminations of this concurrent task. Retention scores control monkeys.
for the control group were near zero for all tasks so it was Spatial discrimination tasks: In a further attempt to
not possible to correlate impairment in lesioned monkeys dissociate visual discrimination impairments from other
with difficulty for unoperated monkeys across component difficulties of sustained performance, the monkeys were
discriminations. tested on simple spatial learning to 27 30 followed by
The scores for each component discrimination of the spatial reversal to 90 100.
retention of the concurrent task were also ordered accord- Repeated measures ANOVA revealed no group effect, a
ing to difficulty for each monkey and then averaged at small task effect [F
54.40, P50.069] and no group3task
1,8
each level of difficulty. This allowed, for example, com- interaction. Post hoc comparisons, however, revealed a
parison of performance between the groups on the com- small difference between groups on the spatial reversal
ponent discrimination which each monkey found easiest, task P,0.05. Thus overall there was only minimal
or hardest, etc. Repeated measures ANOVA on these impairment on these spatial tasks, which contrasts with the
scores revealed a significant group effect [F 523.04,
major impairment seen on visual discrimination tasks.
1,8
P,0.001], a significant difficulty effect necessarily and a Further acquisition of visual discriminations: Monkeys
significant group3difficulty interaction [F 513.40, P,
were then tested on new concurrent learning Conc 2 of a
9,72
C .J. Maclean et al. Brain Research 888 2001 34 –50
41
further 10 component discriminations, using wholly novel and in some cases may only be discriminable on the basis
objects, to 90 100. Three lesioned monkeys failed this task of overall shape. Repeated ANOVA across these two tasks
in 500 trials but the other two monkeys learnt the task with revealed a significant group effect [F
59.32, P,0.05],
91,80
scores within the range of the control monkeys see Fig. but no task effect and no group3task interaction. Post hoc
2. The difference between groups approached significance analysis indicated that the difference between the two
P50.08. groups approached significance on the first task, which was
Repeated measures ANOVA of the scores to 9 10 for tested to a lower criterion 27 30 and attained signifi-
each component discrimination of this concurrent task cance on the second task, which was tested to a higher
revealed a significant group effect [F 56.05, P,0.05]
criterion 90 100. The impairment on black object dis-
1,8
and a significant component effect [F 53.85, P,0.001]
crimination especially when tested to a higher criterion
9,72
but no group3component interaction. Post hoc compari- suggests that defects in visual analysis and in mnemonic
sons for each individual component revealed no com- processing are involved in producing the learning impair-
ponents for which the two groups differed significantly ment.
although the score for the lesioned group was above that of the control group for all components except one, where the
3.2.2. Experiment 2 scores were nearly equal see Fig. 3B. There was a
significant correlation between component difficulties ac- 3.2.2.1. Preoperative testing. Monkeys in Experiment 2
ross the two groups r50.7962, P,0.01. In other words, were tested on retention of the first object discrimination
both the lesioned and control monkeys found the same that they had ever learnt 2nd Ret Object 1 for monkeys
component discriminations harder than some other com- from both sources, followed by acquisition of a new
ponent discriminations. Since learning difficulty for control object discrimination Object 6 and two new shape
monkeys probably reflects differences in discriminability discriminations Shape 3 and Shape 4. Repeated measures
between the two objects used in each component, this ANOVA showed no group difference over these tasks
correlation indicates that the learning impairment shown indicating that the groups were well matched for learning
by lesioned monkeys was also influenced by the same ability prior to surgery. Table 3
differences in discriminability between objects. The scores for each component discrimination were also
3.2.2.2. Postoperative testing. Monkeys were retested on ordered according to difficulty for each monkey and then
retention of the first object discrimination which they had averaged for each level of difficulty. Repeated measures
ever learnt 3rd Ret Object 1, followed by acquisition of a ANOVA on these scores revealed a significant group effect
new object discrimination Object 7, retention of the [F
56.05, P,0.05], a significant difficulty effect neces- shape discrimination first learnt prior to surgery Ret
1,8
sarily and a significant group3difficulty interaction Shape 3, and acquisition of a new shape discrimination
[F 55.06, P,0.001]. Post hoc analysis revealed a
Shape 5. Repeated measures ANOVA across these tasks
9,72
significant group difference only on the three tasks that revealed a significant group difference F
530.25, P,
1,6
each monkey found most difficult. This suggests that the 0.01 and a significant group3task interaction F
5
3,18
impairment, which had ameliorated considerably from the 10.42, P,0.001. Post hoc t-tests showed a significant
time of the postoperative retention of the other concurrent group difference on the first object retention task t5
discrimination task, was now confined to learning about 5.336, P,0.01 and on acquisition of the shape discrimi-
objects which the monkeys found most difficult to dis- nation t55.189, P,0.01.
criminate. Ten pairs of pseudorandomly chosen objects are Since the largest impairment was seen on acquisition of
likely to include some that are less readily discriminable the shape discrimination, this type of task was used to
than others. Thus the overall impairment by lesioned assess the effect of pilocarpine. The monkeys were pre-
monkeys on concurrent learning may reflect their dis- sented with a series of shape discriminations and were
proportionate difficulty in dealing with the visual aspects pretreated with saline or pilocarpine vol. 0.1–0.2 ml, i.m.
of some of the discriminations, i.e., that the lesioned |20 min before testing each day. Testing was repeated
monkeys had a form of visual agnosia. across days for each drug task combination until a criter-
In order to investigate this further we next tested the ion of 27 30 was achieved. Each monkey was tested
monkeys on two visual discriminations the first to 27 30 initially with a dose of 1 mg kg pilocarpine. One monkey
and the second to 90 100 using objects which were in Group L2 and two monkeys in Group C2 would not
painted black all over Shape 1 and Shape 2. Multi- perform trials in the WGTA under this dose because of
coloured junk objects differ in many component features side effects vomiting and or excess salivation and were
because the colours break the object up into many separ- therefore tested at a dose of 0.5 mg kg pilocarpine. The
ately identifiable parts, each of which may form the basis scores to criterion were summed for the two shape
of a comparison with the other object of the stimulus pair. discriminations learnt under saline and for the two shape
Black junk objects differ from each other in far fewer ways discriminations learnt under pilocarpine. Repeated mea-
42 C
Table 3 Mean learning scores 6S.E.M. for tasks used in Experiment 2
Tasks Control group
Lesion group Post hoc tests
ANOVA
Preoperative: 2nd Ret Object 1 27 30
26622 1568
ns Group F
50.004 ns
1,6
Object 6 27 30 2169
12612 ns
Task F 51.79
ns
3,18
Shape 3 27 30 262
664 ns
Group3task F 50.882
ns
3,18
Shape 4 27 30 15614
27610 ns
Postoperative: 3rd Ret Object 1 27 30
1269 216637
P,0.01 Group F
530.25 P,0.01
1,6
Object 7 27 30 1768
54635 ns
Task F 514.28
P,0.001
3,18
Ret Shape 3 27 30 060
2069 P50.067
Group3task F 510.42
P,0.001
3,18
Shape 5 27 30 34618
179621 P,0.01
Shape–Saline 27 30 26613
67623 ns
Group F 531.71
P,0.001
1,6
Shape–Pilocarpine 27 30 41620
90630 ns
Drug F 51.79
ns
3,18
Group3drug F 50.02
ns
3,18
sures ANOVA showed a significant group effect F 5
cortex. In the other three monkeys in Group L1, the
1,6
31.713, P,0.001 but no drug effect and no group3drug perirhinal cortex, like the inferotemporal cortex was lateral
interaction. Thus although these monkeys showed a learn- to the incision. In two monkeys in Group L1, the amygdala
ing impairment as a result of surgery, this impairment was was cut neatly so that half was medial to the cut while the
not ameliorated by treatment with a cholinergic agonist. other half was lateral to the cut. In the other three monkeys
in Group L1, the amygdala lesion was larger. In one 3.3. Histology
monkey in Group L1, there was a very small amount of bilateral damage in the hippocampus and in another
3.3.1. Experiments 1 and 2 monkey in Group L1 there was substantial unilateral
On gross inspection of the brains of monkeys in Group damage to the hippocampus. The tail of the caudate
L1 and Group L2, very little damage was visible on the nucleus was damaged unilaterally in two monkeys but was
cortical surface see Figs. 4 and 5. The incision on the intact bilaterally in the other three monkeys in Group L1.
lateral surface was confined to cortex above the superior The tail of caudate nucleus was damaged bilaterally in all
temporal dimple and was, therefore, in auditory rather than monkeys in Group L2. In Group L1, the fornix was
visual association cortex. In one monkey in Group L1 transected bilaterally in three monkeys; a thread of tissue,
shown on the far right in Fig. 5A, there was some which appeared to consist only of ependymal lining,
damage to the superior temporal cortex in the left hemi- bridged the lesion site in one monkey and in another
sphere only. One monkey in Group L2 also shown on the monkey, a very small amount of fornical tissue remained
far right in Fig. 5B sustained a large infarct in the left intact on one side. In Group L2, the fornix was transected
temporal lobe although the incision did not reach the in all monkeys. The lateral geniculate nuclei were intact
medial ventral surface of the cortex, such that the temporal bilaterally in all monkeys.
stem was not completely sectioned. This monkey also had a large medial temporal lobe lesion in the right hemisphere
3.3.3. Acetylcholinesterase histochemistry Figs. 8 and and was excluded from experimental analysis.
9 In all monkeys in Group L1 and Group L2, there was
3.3.2. Cresyl Violet staining substantial loss of AChE staining throughout the medial
In the temporal lobes in all monkeys, an incision could and inferior temporal lobe. AChE staining was severely
be seen parallel to, but starting about 2 mm below, the reduced throughout the hippocampus and entorhinal cortex
lateral sulcus in the anterior half of the temporal lobe. bilaterally except in the one monkey in Group L1 in which
Examples of this incision are illustrated in AChE stained a small amount of fornical tissue remained, where AChE
sections in Figs. 6 and 7. This incision descended staining was not so greatly reduced in the hippocampus in
diagonally from the lateral cortical surface to the medial that hemisphere. Some AChE staining remained in these
ventral cortical surface. The incision extended from at least areas probably as a consequence of cholinergic inputs to
3 mm behind the temporal pole i.e., at the level of the the posterior areas via the supracallosal stria, which were
amygdala posteriorly for |5 mm i.e., to the anterior part only partially transected by the incision in the corpus
of the hippocampus and traversed the temporal stem in all callosum.
monkeys. There was severe gliosis in the anterior commis- There was near total loss of AChE staining in the
sure in all monkeys indicating substantial loss of subcorti- perirhinal and inferotemporal cortex lateral to the surgical
cal temporal lobe efferents. In two monkeys in Group L1, incision and for several millimetres caudal to the incision,
the incision ended between the entorhinal and perirhinal adjacent to the hippocampus, and in the foveal prestriate
C .J. Maclean et al. Brain Research 888 2001 34 –50
43
Fig. 4. Photographs of lateral, frontal, and ventral views of the brain from a lesioned monkey from Expt 2. There was no visible damage on the dorsal surface. On the lateral surfaces the arrows indicate a slit in the dorsal temporal cortex between the lateral sulcus and the superior temporal dimple. Viewed
from the front and below, arrows indicate the extension of the slit. The monkey illustrated is the second from the left in Fig. 5B.
cortex. There was a loss of AChE staining in that part of and had presumably cut the temporal lobe efferents to the
the amygdala which was lateral to the surgical incision. frontal lobe and dorsomedial thalamus via the temporal
There was also a loss of AChE staining in the most stem amygdala see [23] and to the mammillary bodies
anterior part of the hippocampus. This part of the hip- and anterior thalamic nuclei via the fornix. This lesion
pocampus receives its cholinergic input from the NBM via would, however, have left intact the visual inputs from the
a ventral pathway and staining in this area is usually occipital lobe to the temporal lobe and their reciprocal
spared by fornix transection. The loss of this staining is connections. The lesions in the two experiments had been
therefore probably a consequence of the temporal stem intended to be the same although, in practice, the temporal
lesion. lobe incision in the second experiment had extended very
slightly further back than in the first experiment such that 3.3.4. Summary of histological findings
the tail of the caudate nucleus was damaged bilaterally in Transection of the temporal stem and amygdala had cut
the monkeys in Experiment 2 but not in those in Experi- the cholinergic input to that part of the amygdala and
ment 1. temporal cortex which was lateral to the incision and to a
substantial proportion of the temporal cortex caudal to the incision. The fornix transection had cut the greater part of
4. Discussion
