SEPTAL LESIONS IMPAIR RATS'
MORRIS-TEST PERFORMANCE BUT FACILITATE LEFT-RIGHT RESPONSE
Michael Noonan, Michelle Penque and Seymour
Canisius College and The State University of
New York at Buffalo
As published in Physiology & Behavior,
1996, 60, 895-900.
Lesions in the septum impaired performance on the Morris
test, a task in which the rat locates a hidden escape platform by use of fixed
landmarks, but facilitated a water-maze-based left-right response
differentiation, a task in which the rat finds a hidden escape ramp by means of
its internal sense of direction. These results are interpreted as supporting an
allocentric/egocentric dichotomy with respect to navigation, and supporting the
notion that rats approach spatial problems with a hierarchy of potential
solutions in which allocentric solutions take precedence over egocentric ones.
The septal lesions are inferred to disrupt the allocentric mapping system.
It is now well established that lesions of the
septal-hippocampal axis disrupt an animal's ability to master spatial navigation
tasks, particularly those which are approached with what O'Keefe and Nadel (22)
call a "place hypothesis". Lesions to the lateral septum (11), medial septum (2,
3, 5), fornix (16, 23) and hippocampus (15, 27), and/or chemical disruptions of
the interconnections among these structures (9, 17, 24), are particularly
disruptive to animals that attempt to solve a spatial problem by forming an
allocentric, "cognitive map" of their surroundings.
By contrast, the distinction between left and right should
not, indeed cannot, depend on a place hypothesis. The left/right difference is
an egocentric one which changes its relationship to the surroundings as
the animal moves about. That is, the directions left and right orient an animal
towards different places in its environment depending on which direction the
animal is facing at any given moment. One might expect therefore that an
animal's ability to distinguish left from right would be independent of its
ability to form a cognitive map, and so would be unimpaired by lesions in the
allocentric mapping system.
An animal's ability to distinguish left and right can be
tested directly in what Corballis and Beale (1) call a "left-right response
differentiation" task. Here an animal is obliged to differentially associate
mirror-image responses (such as turning left and turning right) with arbitrary
stimuli which do not contain any inherent directional mirror-image information
(e.g., lights on/lights off). O'Keefe and Nadel (22) reviewed some experimental
tasks which would appear to fit these criteria in their discussion of
"successive discriminations" (p. 284). Although recognizing that such tasks do
not depend on cognitive mapping, they nevertheless reviewed experimental
findings that performance on such tasks has, in some instances, been impaired
following damage to the putative mapping system. To account for this, they
speculated that animals with impaired mapping abilities might be compelled to
adopt maladaptive orientations on such tasks (pp. 278-286). In their discussion,
O'Keefe and Nadel cited studies in which hippocampus-lesioned rats were
deficient at food-motivated, successive-discrimination tasks requiring them to
turn in one direction when the maze walls were black and the opposite direction
when the maze walls were white (4, 7). In these studies the hippocampal rats had
adopted persistent habits in which they turned in only one direction for long
strings of trials. The more recent work of Marston, Everitt and Robbins (10) may
also be relevant here since they too employed a task which might have been
approached by their subjects as a left-right problem. They found that septal-lesions
resulted in deficiencies on a "conditional visual discrimination" in which rats
in operant chambers were obliged to press the left lever when lights flickered
at one frequency and the right lever in response to a different frequency.
However, none of these studies were designed to focus
specifically on the allocentric/egocentric distinction vis-à-vis spatial
navigation. Accordingly their left-right tasks were not designed to minimize
allocentric cues, nor were any efforts included to confirm that their subjects
solved their tasks by critically distinguishing left and right. In the
hippocampal studies (4, 7), the rats were tested in mazes which were fixed in
place within well-lit rooms possessing salient extra-maze landmarks, and operant
chambers like the ones used in the Marston et al. study (10) likewise typically
contain observable stationary features. As O'Keefe and Nadel themselves argue,
rats appear to try to solve spatial tasks preferentially using place-based,
allocentric mapping, particularly when salient fixed landmarks are available. It
is at least possible that the rats in these studies were influenced by the fixed
features of their testing environments, and made inappropriate attempts to
associate the location of reward with these features.
Unfortunately, this has left us without a clear
experimental demonstration of the effects of lesions of the septal-hippocampal
axis on an animal's ability to make the distinction between left and right, and,
more generally, without an unequivocal test of the dissociability of egocentric
left-right response differentiation from the allocentric mapping system. We are
left with the unsatisfying speculation (22) that lesioning the allocentric
mapping system impairs not only performance on tasks demanding navigation to
fixed places by means of extra-maze cues, but also performance on tasks
demanding egocentric orientations independent of fixed cues because the
orientation system becomes maladaptively engaged. Our goal in this project was
to try to resolve this situation by testing the effects of septal lesions on a
task specifically designed to test the animal's ability to make the left-right
In our laboratory, we have been investigating the behavior
of rats in a left-right response differentiation (LRRD) task using a
water-escape variation on the theme (18, 19, 20, 21). We test our animals in a
pair of M-shaped tanks oriented in opposite directions in different dimly-lit
rooms, which we have endeavored to keep as symmetrical and featureless as
possible. Over successive trials, the rats learn to swim to the right under one
non-directional stimulus condition and to the left under another such condition.
By testing the performance of rats under different probe conditions after they
have mastered this task, we have shown that our subjects continue to show
reliable left/right response differentiation when their testing is carried out
in the alternative maze oriented in the opposite direction. That is, we have a
test in which the salience of allocentric mapping cues is minimized, and on
which we have earlier demonstrated that rats solve the problem posed by means of
egocentric navigational reference.
Our goal was to examine the effects of lesions in the
septum on the ability of rats to distinguish left and right in our paradigm, and
to contrast the results with the effects of the lesions on the most common
behavioral test of allocentric cognitive mapping--the Morris test (13, 14). In
this task, the rat swims repeated trials in a tank of water in search of a
submerged refuge platform. From trial to trial, the rat is placed into the tank
at varying locations, and comes over time to efficiently locate the platform in
its fixed location by means of noting its position relative to salient landmarks
outside of the tank.
Subjects. Ninety-eight adult male and female hooded
(Long-Evans) rats were maintained on an alternating 12:12 white:red light cycle.
Room temperature was kept at 26°C.
Surgery. The rats were randomly assigned to one of
three surgical treatments. The Septal group (N = 33) sustained bilateral
electrolytic septal lesions. Animals in the Sham group (N = 34) experienced
electrode placement but no current. Animals in the Intact group (N = 31) were
anesthetized, positioned in the stereotaxic head holder, and subjected to scalp
preparation, but no skull or brain defects were created. Because the septal
electrodes of the first two groups passed through the corpus callosum, and we
have shown in earlier studies (20, 21) that callosal damage can itself
facilitate LRRD, we included the Intact group as a basis for comparison with our
Sham group in order to assess the degree to which the electrode passage itself
contributed to our findings.
Anesthesia was accomplished through IP administration of
ketamine (Ketaset, 52 mg/kg) combined with xylazine (Rompun, 2.6 mg/kg). The
subject was mounted in the flat-skull position, i.e., nose-clamp at -3.3 mm
(25), and the tip (uninsulated for 1 mm) of a monopolar electrode (0.8 mm
diameter) was lowered under stereotaxic guidance through 2 mm bore holes to
points 0.5 mm anterior and 0.6 mm lateral to bregma, and 6.6 mm ventral from the
surface of the skull. For the Septal subjects, 2.0 mA of current were passed
into the septum on each side for 7.5 seconds. The reference (negative) was a
clip attached to the edge of the open scalp.
For logistical reasons, the rats were divided into three
cohorts, counterbalanced with surgical groups, which commenced behavioral
testing six, eight, and ten weeks postsurgically. In the week preceding testing,
the rats were handled twice daily in order to habituate them to human contact.
Each rat underwent LRRD testing first and the Morris test one week later. All
animal handling and data collection were carried out by observers blind to the
animals' surgical-group assignment, and recorded on videotapes which were then
reviewed by a second blind observer.
LRRD Test. We employed two M-shaped Plexiglas
water-mazes, 46 cm deep (cf. 20). Water entered continuously (6.3 liter/min at
24° C) at the floor of the starting box, and flowed out at the floor at the ends
of both arms, being maintained at a depth of 25 cm. Each maze arm was 15 cm wide
and extended for 30 cm laterally. The arms then turned 90° back, so that an
escape ramp, extending down into the water at the end of the appropriate arm,
was out of sight to the rat at the choice point. The reinforcement was escape
from the water, accomplished by climbing up the ramp.
Testing took place under red light. The walls of the maze
were white and could be back-illuminated. When not illuminated, the walls as
viewed from within the maze appeared to the human observer as uniform and dark.
When back-illuminated, alternating dark and light 3 cm-wide vertical stripes
appeared. On trials in which the maze walls were illuminated, the escape ramp
was always placed in the right arm; when the walls were unilluminated, the
escape ramp was in the left arm. A "dummy" ramp, which extended down only to 15
cm above the water surface and could therefore not be used for escape, was
always placed in the opposite arm so that the escape-ramp location could not be
determined by a view from outside the tank.
Pseudorandomly sequenced trials (maze-illuminated/maze-unilluminated)
were presented at 4-min inter-trial intervals. On each trial the rat was placed
in the starting box and allowed to swim until it found the ramp; it was then
returned to its home cage until the next trial. Each rat was tested for 25
trials per day until it reached the criterion of 10 successive correct first
turns at the choice point, or for a maximum of five successive days. The number
of trials taken to reach criterion served as the index of difficulty in making
the left-right response differentiation (cf. 18, 19, 20, 21).
Seven rats (0 Septal, 3 Sham, 4 Intact) failed to reach
criterion after completing the five days of testing (125 trials); they were
assigned trials-to-criterion scores equivalent to the lowest score possible
given their ending performance. As examples, if the response on the 125th trial
was the last of 5 consecutive correct responses, the rat was given a score of
130. If the 125th trial was incorrect, the rat was given a score of 135.
In this as in related projects, we conducted ten
additional trials to confirm that our subjects' scores were not functions of
confounding variables. After initially reaching criterion, each rat was moved
temporarily into an adjacent hallway and then moved either into a
different room to be tested by different experimenters in a maze oriented
differently with respect to compass heading; or back into their original
testing room for ten additional trials under conditions identical to their
initial training. The rats in the latter condition served to provide a basis of
comparison to allow us to assess the influence on the rats of being moved about.
Morris Test: For this test, the rats were moved to
a room illuminated by white lights. We employed a cylindrical polyethylene tank
140 cm in diameter and 45 cm deep. It was filled with 26° C tap water to a depth
of 21 cm. An inverted clear-glass jar (11 cm diam, 20 cm high) served as a
hidden refuge platform just under the surface of the water. For any given rat,
the platform was always located centrally in a particular quadrant of the tank,
with this escape-quadrant being varied from rat to rat, counterbalanced across
groups. For eight trials per day over three successive days, the rat was placed
into the tank facing the near tank wall, with the entry quadrant varying
randomly within the provision that each quadrant was included in each block of
four trials. The latency for the rat to reach the refuge platform was recorded
for each trial. If on any trial the rat had not reached the platform after 120
sec, it was placed on the platform by hand. In either case, the rat was left to
stand on the platform for 20 sec after reaching it.
In other laboratories which employ the Morris test, a
white powder is commonly added to the tank water in order to reduce the
visibility of the platform (e.g., 2, 15, 27). We satisfied ourselves that such a
procedure to hide the location of our glass platform was unnecessary for the
following reasons: (a) a human observer has difficulty finding the transparent
platform when viewing from any angle; (b) the platform becomes visually
unavailable as the point of view approaches the surface of the water (that is,
because of the viewing angle, the "rat's-eye view" of the water's surface
reveals only reflections of above-water stimuli); (c) the rats often swam within
a centimeter of the platform without detecting it; (d) on the day following the
three standard days of formal testing described above, we conducted trials on
some rats in which no platform was present, and found that the latency to swim
to the previously trained quadrant was not different from the latency on trials
in which the platform was present; and (e) on day-4 test trials on other rats,
we placed the platform in "incorrect" (i.e., not previously reinforced)
quadrants and found that the rats swam with unchanged latency to the previously
reinforced quadrant, and thence initiated search patterns which were as often
directed toward either of the other empty quadrants as toward the one with the
Histology. Following behavioral testing, the rats
were perfused intracardially with saline followed by formalin. Serial 8-micron
coronal sections were made, and every 20th slice was stained with cresyl violet.
The performances of the Sham and Intact rats were very
similar and not significantly different on either behavioral test; these groups
were therefore combined into a single control group for subsequent analyses.
Similarly, there were no cohort differences on either task, nor were there any
significant statistical interactions between cohort and surgical groups.
Accordingly, in the analyses presented below the cohorts are combined.
As expected, the Septal subjects were substantially
impaired in mastering the Morris test (see Figs 1 and 2). The mean latency of
the lesioned group to reach the platform (Mean = 15.4 sec) was 58.8% higher than
that of the controls (Mean = 9.7), F (1,94) = 37.6, p
< .0001. When examined separately by four-trial block, this impairment of the
Septal group was statistically significant (p < .01) for
each of the blocks except the last. The sexes did not differ in overall mean
latency (F (1,94) = 0.0, ns). There was however a marginally
significant interaction between surgical treatment and sex (F
(1,94) = 3.9, p = .053), reflecting the fact that the magnitude of
the impairment of the septal animals compared to controls was greater for males
than for females.
By contrast, on the Left-Right Response Differentiation
Task, the Septal subjects were dramatically superior to the Controls (Fig
2, left panel). The trials-to-criterion scores for the lesioned subjects (Mean =
43.1) averaged 38.4% lower than those of the controls (Mean = 70.0), F
(1,94) = 22.0, p < .0001. The sexes also differed significantly (F
(1,94) = 7.9, p = .006), females overall having lower scores than
males. The statistical interaction between sex and surgical group was not
significant. In the ten post-criterion trials conducted after the rats were
moved, rats from both surgical groups and in both post-criterion testing
conditions continued to demonstrate reliable left-right response
In an effort to assess whether the lesioned rats were more
prone to adopting maladaptively persistent orientations on this task, we
tabulated for each subject the total number of trials spent in a string of
consistently directed first responses at the maze choice point. That is, we
counted the number of consecutive trials on which the rat turned left, and
similarly the number of consecutive trials on which it turned right. For this
purpose, we included in a string any trial whose first response was in the same
direction as the one before and/or after it, so long as at least one of the
responses in the string was incorrect. We also tabulated the number of times
there was a break in such behavior, and the number of times the rat switched
from a left-going string to a right-going string or vice versa. We then
expressed these totals as proportions of the total number of trials. Overall,
the Septal subjects averaged fewer of their trials in such unilateral
strings than did the Controls (54% vs 64% respectively), and this difference
proved statistically reliable, F(1,96) = 9.68, p = .002. The groups did not
differ in the number of breaks in their strings nor in the number of switches in
direction from string to string.
Microscopic examination of the brain sections of the
Septal group revealed lesions confined to the septal region with the corpus
callosum, caudate/putamen, hippocampus and thalamus essentially normal in
appearance in each subject. Across subjects there was some variation in the
anterior/posterior extent of the lesion. In 14 subjects, the lesions were
largely confined to the lateral and medial septal subdivisions with little or no
involvement of visible fimbrial fibers or the triangular septal nucleus. In the
other 19 Septal subjects, the lesions extended posteriorly to include much of
the anterior fimbria and triangular nucleus. Brain sections from a
representative subject of this latter type are presented in Figure 3. For each
subject, in a process blind to the behavioral results, we visually estimated the
percentage of tissue in each septal subdivision which remained, and we
subsequently assessed the relationship between these estimates and the rats'
behavioral scores. There was a significant positive correlation (r =
0.55, p < .01) between the proportion of fimbria and triangular nucleus
damage and overall mean latency to reach the refuge platform in the Morris
test--the more posterior the lesion, the worse the performance in the Morris
test. However, direct fimbrial involvement appeared not to be critical in
explaining the Septal group's collective impairment on the Morris test. An
analysis of variance comparing the mean escape latency of the 14 subjects in
which the fimbria was largely spared with that of the combined Control subjects
showed that lesions confined to the lateral and medial septum were alone
sufficient to significantly impair Morris Test performance (F
(1,77) = 12.9; p = .001). No statistically reliable relationships
were obtained between LRRD scores and any of these post-hoc assessments of
damage to septal subdivisions.
The impairment shown by our septal-lesioned rats on the
Morris test replicates similar findings and confirms a role for the septum (2,
5, 10, 12, 17), along with that shown by others for the hippocampus (10, 15, 22,
28), in the conduct of landmark-guided spatial navigation. The marginal sex by
surgical group interaction we found is compatible with the notion that male and
female rats may engage the spatial-mapping neural substrate differently (29).
It remains to be asked whether the septal-hippocampal axis
comprises a single functional system with respect to spatial navigation, such
that lesions to any one critical component is as debilitating as would be a
lesion of the whole. Alternatively, each sub-component might make its own
contribution in a way which remains somewhat functional in the absence of the
others. Our findings appear to be compatible with the latter view: lesions which
appeared to be restricted to the lateral and medial subdivisions of the septum
were alone sufficient to produce a significant impairment on the Morris test,
and even greater deficits were shown as the extent of lesion in the fimbria
Regarding our left-right task, the sex differences we
found in mean trials-to-criterion scores do not correspond to results from our
earlier studies (18, 19, 20, 21) in which the sexes were essentially equal in
performance. We are therefore inclined to caution in attributing this finding to
the population at large.
The possibility that the improvement in LRRD we are
attributing to septal lesions might be due to incidental callosal damage must be
considered. In other work we have shown that severing the corpus callosum leads
to an improvement in LRRD scores (20, 21), presumably by eliminating the
inter-mixing of lateralized information. Nevertheless, three reasons make us
inclined to rule out callosal damage in explaining our present results: (a)
microscopic examination of the stained sections from the Septal brains showed no
evidence of electrolytic damage in the callosum; (b) the Sham subjects which
also experienced electrode penetration through the callosum did not differ
significantly from the Intact subjects; and (c) although the possibility cannot
be ruled out that the functioning of the adjacent callosal area was impaired in
ways not evident upon microscopic examination, we have shown in other work (21)
that when the entire anterior third of the corpus callosum (the area adjacent to
the septum) is severed, the magnitude of the LRRD improvement is only 16.3%
compared to sham operates, an effect much smaller than the magnitude of the
improvement found here following septal lesions (38.4% improvement compared to
controls). Indeed the improvement shown by the Septal subjects is greater than
that shown even by completely callosotomized subjects in the earlier study
(30.5%). We therefore consider it unlikely that the facilitation of LRRD in the
present study derives primarily, if at all, from impaired functioning of the
That the Septal subjects were not deficient on the LRRD
task is compatible with the view that the role of the septal-hippocampal axis in
spatial processing is specific to allocentric cognitive mapping by means of
external landmarks. Clearly, since our lesioned subjects were not impaired at
our LRRD task, the integrity of the septal/fimbrial region is not a necessary
precondition for all types of spatial learning.
That the septal animals in this study were actually
substantially superior at the LRRD task contrasts with the normal
expectation that brain damage would result in behavioral deficits. However, this
finding is not without precedent. For example, septal lesions in rats also
facilitate learning of shuttlebox active avoidance (e.g., 6, 8, 26). Such
results are compatible with the notion advanced by O'Keefe and Nadel (22) that
animals follow a hierarchy of hypotheses when approaching a spatial problem, and
ordinarily first approach problems containing spatial elements by attempting to
map relevant stimuli relative to fixed landmarks. Thus, rats in a shuttlebox by
natural inclination first try to learn the location of the safe place. It
is only after they have exhausted this spatial mapping strategy as a potential
solution that an approach lower in the hierarchy is adopted. On this view, when
intact rats encounter our LRRD task they ordinarily expend some initial trials
attempting to map the new environment and trying to remember where in a fixed
spatial framework the escape ladder is reliably located. Only after this process
is determined to be futile -- a step facilitated by the unavailability of fixed
landmarks -- do the subjects entertain the (correct) possibility that the ladder
moves about and that its location can be predicted by the luminance of the
walls. O'Keefe and Nadel (22) argue that when an animal's cognitive mapping
system is impaired due to lesions in the underlying neural substrate, it more
readily abandons the allocentric mapping strategy and shifts more quickly to
If the rats' adoption, in the initial stages of our LRRD
task, of persistent tendencies to turn in one direction at the maze choice point
is viewed as consequent to an attempt by the rats to identify one
spatially-fixed arm of the maze as the location for escape, then the fact that
our normal rats characteristically adopt such position habits, and that our
septal-lesioned rats were less likely to do so, is also compatible with the
notion that animals approach such tasks initially with a cognitive mapping
strategy, and that this strategy is either unavailable or less firmly exhibited
at the top of the hierarchy when its neural substrate is impaired. According to
this view, it is precisely because our septal animals were deficient at
allocentric cognitive mapping that they were facilitated at egocentric
left-right response associations.
This work was supported in part by a grant to Canisius
College from the Charles A. Dana Foundation, and by a grant to MP from Sigma Xi.
The authors thank and praise Jill Krakowiak and Debra Lipczynski, who served as
research assistants, and Sandra Thamer who provided histological processing.
Corballis, M.; Beale, I. The Psychology of Left and
Right. Hillsdale, NJ: Lawrence Erlbaum Associates; 1976.
Hagan, J.J.; Salamone, J.D.; Simpson, J.; Iversen,
S.D.; Morris, R.G.M. Place navigation in rats is impaired by lesions of medial
septum and diagonal band but not nucleus basalis magnocellularis. Behavioral
Brain Research 27: 9-20; 1988.
Hodges, H.; Allen, Y.; Kershaw, T.; Lantos, P.L.; Gray,
J.A.; Sinden, J. Effects of cholinergic-rich neural grafts on radial maze
performance of rats after excitotixic lesions of the forebrain cholinergic
projection system-1: Amelioration of cognitive deficts by transplants into
cortex and hippocampus but not into basal forebrain. Neuroscience, 45,
Isaacson, R.L.; Schmaltz, L.W.; Douglas, R.J. Retention
of a successive discrimination problem by hippocampectomized and neocorticate
rats. Psychological Reports, 19, 991-1002, 1966.
Kelsey, J.E.; Landry, B.A. Medial septal lesions
disrupt spatial mapping ability in rats. Behavioral Neuroscience, 102,
Kessler, J.; Markowitsch, H.J.; Sigg, G. Memory related
role of the posterior cholinergic system. International Journal of
Neuroscience, 30, 101-119, 1986.
Kimble, D.P. The effects of bilateral hippocampal
lesions in rats. Journal of Comparative and Physiological Psychology, 56,
King, F.A. Effects of septal and amygdaloid lesions on
emotional behavior and conditioned avoidance responses in the rat. Journal of
Nervous and Mental Disease 126: 57-63; 1958.
Leranth, C., Frotscher, M. Organization of the septal
region of the rat brain: cholinergic-GABAergic interconnections and the
termination of hippocampal-septal fibers. Journal of Comparative Neurology,
289, 304-314, 1989.
Marston, H.M.; Everitt, B.J.; Robbins, T.W. Comparative
effects of excitotoxic lesions of the hippocamus and septum/diagonal band on
conditional visual discrimination and spatial learning. Neuropsychologia, 31,
M'Harzi, M.; Jarrard, L.E. Effects of medial and
lateral septal lesions on acquisition of a place and cue radial maze task.
Behavioral Brain Research, 49, 159-165, 1992.
Miyamoto, M.; Kato, J.; Narumi, S.; Nagaoka, A.
Characteristics of memory impairment following lesioning of the basal
forebrain and medial septal nucleus in rats. Brain Research 419: 19-31; 1987.
Morris, R.G.M. Spatial localization does not require
the presence of local cues. Learning & Motivation 12: 239-249; 1981.
Morris, R.G.M. Development of a water-maze procedure
for studying spatial learning in the rat. Journal of Neuroscience Methods, 11,
Morris, R.; Garrud, P.; Rawlins, J.; O'Keefe, J. Place
navigation impaired in rats with hippocampal lesions. Nature 297: 681-683;
Myhrer, T.; Kaada, B. Locomotor avoidance and maze
behavior in rats with the dorsal fornix transected. Physiology & Behavior, 14,
Nagahara, A.H.; McGaugh, J.L. Muscimol infused into the
medial septal area impairs long-term memory but not short-term memory in
inhibitory avoidance, water maze place learning and rewarded alternation
tasks. Brain Research, 591, 54-61, 1992.
Noonan, M.; Axelrod, S. Behavioral bias and left-right
response differentiation in the rat. Behavioral and Neural Biology 52:
Noonan, M.; Axelrod, S. Failure of induced asymmetries
to improve left-right response differentiation in the rat. Journal of General
Psychology 117: 197-202; 1990.
Noonan, M.; Axelrod, S. Improved acquisition of
left-right response differentiation in the rat following section of the corpus
callosum. Behavioural Brain Research: 46, 135-142, 1991.
Noonan, M.; Axelrod, S. Partial callosotomy and
left-right response differentiation in the rat: Separate anterior and
posterior facilitatory effects. Behavioral Neuroscience, 106, 433-436, 1992.
O'Keefe, J., Nadel, L. The Hippocampus as a Cognitive
Map. Oxford: Claredon Press, 1978.
O'Keefe, J., Nadel, L., Keightley, S., Kill, D. Fornix
lesions selectively abolish place learning in the rat. Experimental Neurology,
48: 152-166, 1975.
Onteniente, B, Tago, H., Kimura, H., Maeda, T.
Distribution of gamma-aminobutyric acid-immunoreactive neurons in the septal
region of the rat brain. Journal of Comparative Neurology, 248, 422-430,
Paxinos, G; Watson, C. The Rat Brain in Stereotaxic
Coordinates (2nd Edition). New York: Academic Press; 1986.
Schwartzbaum, J.S.; Green, R.H.; Beatty, W.W.;
Thompson, J.B. Acquisition of avoidance behavior following septal lesions in
the rat. Journal of Comparative and Physiological Psychology 63: 95-104; 1967.
Sutherland, R.; Kolb, B.; Whishaw, I. Spatial mapping:
Definitive disruption by hippocampal or medial frontal cortical damage in the
rat. Neuroscience Letters 31: 271-276; 1982.
Whishaw, I.Q.; Rod, M.R.; Auer, R.N. Behavioral
deficits revealed by multiple tests in rats with ischemic damage limited to
half of the CA1 sector of the hippocampus. Brain Research Bulletin, 283-289,
Williams, C.L.; Meck, W.H. The organizational effects
of gonadal steroids on sexually dimorphic spatial ability.
Psychoneuroendocrinology, 16, 155-176, 1991.
Figure 1. Mean escape latency in four-trial blocks on the
Morris Test, by group.
Figure 2. Performance on the Left-Right Response
Differentiation (left) and Morris (right) tests.
Figure 3. Brain sections from a representative subject.
The entire septal complex is destroyed (including the lateral, medial, and
triangular subdivisions) with consequent ventriculomegaly. Secondary atrophy of
hippocampal-fimbrial fibers is also evident.