Previous Article | Next Article 
The Journal of Neuroscience, September 1, 1998, 18(17):7027-7032
Differential Effects of Dorsal and Ventral Hippocampal
Lesions
Brian J.
Hock Jr. and
Michael D.
Bunsey
Kent State University, Kent, Ohio, 44242
 |
ABSTRACT |
Several studies have demonstrated that dorsal, but not ventral,
hippocampus is critical for spatial memory. The mnemonic role of the
ventral hippocampus remains unclear. The existence of relatively direct
connections between hypothalamic nuclei and ventral hippocampus suggests that the ventral hippocampus may be involved in acquisition of
information regarding internal cues (e.g., hunger).
Male Long-Evans rats received ibotenic acid-induced lesions of either
dorsal or ventral hippocampus or underwent sham surgeries. After a 3 week recovery, subjects were tested on delayed alternation in a T-maze
and on a task in which food-deprivation state was used as a contextual
cue (Davidson and Jarrard, 1993
). Rats with dorsal, but not ventral,
lesions were impaired in delayed alternation, consistent with previous
findings, but both groups were impaired in the learning of the internal
state-shock association task.
Key words:
ventral hippocampus; dorsal hippocampus; ibotenic
lesions; T-maze; food deprivation; spatial memory
| |
INTRODUCTION |
Several recent studies have examined
functional dissociations between dorsal and ventral hippocampus. Moser
et al. (1993, 1995) reported that lesions of dorsal hippocampus (DH),
but not ventral hippocampus (VH), caused spatial memory impairments in rats. These results are broadly consistent with electrophysiological data which have indicated that, in comparison with VH, DH contains both
a greater proportion of and more sharply tuned place cells (Jung et
al., 1994). Together, these results suggest a functional dissociation
along the septotemporal extent of the hippocampus, with the dorsal
hippocampus being more important than ventral hippocampus for spatial
memory processes.
However, the above lesion studies are limited, because they did not
demonstrate a double dissociation between DH and VH. Demonstration of a
double dissociation is critical to confidently conclude that the
spatial deficit that follows a DH lesion reflects a preferential role
of DH in spatial memory; based on the above results, we cannot rule out
the possibility that DH lesions are merely more disruptive than VH
lesions. According to this latter framework, DH lesions would be more
likely to disrupt any form of hippocampal-dependent memory. Notably,
demonstration of a double dissociation between DH and VH would also
provide insight into the functional role of VH, about which little is
presently known.
The present study tested for a double dissociation between DH and VH
lesions using two tasks: (1) a spatial delayed alternation task, and
(2) a conditional learning task that used internal state as a
contextual cue. DH rats, but not VH rats, were expected to demonstrate
an impairment in the spatial task, as in previous studies, whereas VH
rats were expected to demonstrate an impairment in the internal state
task. Davidson and Jarrard (1993) have shown previously that specific
hippocampal lesions (encompassing both DH and VH) cause impairments in
the internal state-conditional task. A preferential role for the VH in
this type of task was hypothesized based on neuroanatomical
considerations. VH receives a relatively dense input from the
tuberomammillary nucleus in the posterior hypothalamus (Kohler et al.,
1985), which presumably carries information regarding internal states,
including hunger (Risold and Swanson, 1996).
| |
MATERIALS AND METHODS |
Subjects. Thirty-six naive male Long-Evans rats
(Charles River Laboratories, Wilmington, MA) were kept on a 15/9 hr
light/dark cycle. Animals were housed in Plexiglas home cages and given
water ad libitum. Food, however, was limited according to
task (see below).
Surgery and histology. The surgical procedure was the same
technique developed by Jarrard (1989), using multiple microinjections of ibotenic acid (Sigma, St. Louis, MO). Rats were anesthetized with
pentobarbital (50 mg/kg) and placed into a stereotaxic frame. A midline
incision was made on the scalp, the skin was reflected, and the skull
overlying the targeted region was removed. Injections of ibotenic acid,
dissolved in PBS, pH 7.4, at 10 mg/ml, were given using a 2 µl
Hamilton syringe with a fine pipette attachment to minimize mechanical
damage mounted on the stereotaxic frame. Injections of 0.05-0.1 µl
were given over a 30-60 sec delivery period at various points,
depending on the type of lesion (Table 1). Rats in the sham group underwent all
of the surgical procedures, except that neurotoxin was not released and
the pipette did not enter the hippocampal region. Rats were given 3 weeks to recover before training began.
After testing, rats were given an overdose of pentobarbital and
perfused with physiological saline and 10% formal saline. The brains
were placed in a formal saline solution, followed by a
sucrose-formalin solution for at least 24 hr each. The brains were
then sectioned (40 µm) in the coronal plane and stained with cresyl
violet. Lesion extent was calculated by using a point-counting technique (Gunderson and Jensen, 1987). For each of three evenly spaced
sections through the dorsal half of the hippocampus, an array of dots
was placed directly over the section, and the number of points falling
on hippocampal tissue was counted. The volume of intact tissue for each
region was calculated by multiplying the sum of the areas among
the sections by the distance between the sections. The values for each
subject were subtracted from the value of control values to
estimate percent of damage. This procedure was repeated for VH.
Apparatus and procedure. During the last week of the 3 week
recovery period, each rat was handled. Most of the subjects (see below)
were then tested in the two tasks. Half of the subjects from each group
were tested in the spatial task before the conditional task, and half
of the animals received testing in the opposite order. Because of a
mechanical failure in the shock generator, two to three animals in each
group received fewer foot shocks than intended in the fear task. Their
data were dropped, and nine additional animals (three per group) were
run in this task alone.
T-maze experiments. Rats were first food-deprived to 80% of
their original body weight. Five days before training, rats were handled for 1-2 min each day and given four whole Froot Loops (FLs) per day for 2 d in their home cages to accustom them to eating FLs. On the third day, rats were brought to the training room
one at a time and placed in the start box (24.7 × 10.8 × 13.3 cm) of the T-maze without the guillotine door. The T-maze was made
of 5 mm black Plexiglas, and the roof was covered with clear Plexiglas
over the start and goal boxes, whereas the rest of the maze was covered
with 5 mm wire mesh squares. Each arm of the T-maze was 50.8 cm long.
FLs were located along the floor of the T-maze and in the reward cups
of each goal box. Each rat was allowed to roam freely in the T-maze for
20 min before the next rat was run. The maze and floor were cleaned
after each rat's session.
On day 4, five or six FLs were placed in the goal boxes, and three FLs
were placed in the reward cups. Each rat was placed in the start box
with the guillotine door closed, and after 4 sec, the door was opened
and the rat was allowed to roam until reaching a goal box, at which
point the door was closed. The rat was removed from the goal box after
eating an FL and placed back into the start box, and the procedure was
repeated. The procedure was repeated until 20 min had elapsed.
Training began on day 5. Each rat was run on a reinforced alternation
schedule according to the procedure described by Thomas (1978). Each
rat was rewarded with one FL for entering the arm opposite to the one
just visited. The criterion for an arm choice was that all four paws
passed the point where the guillotine door would close. The rats were
run for six trials a day until they reached a criterion of one or fewer
errors on 2 consecutive days. To control for the possibility that the
rats were smelling the reward at the end of the arm, the last two
trials of each day were not rewarded until the rat reached the correct
goal box. This was done by dropping the FL in the reward cup after
closing the guillotine door. Performance on these trials did not differ from that on the standard trials.
Once the criterion was reached, the reinforced delayed alternation task
began. During this phase, a 5 min delay was added between trials,
during which the rat was placed back in its home cage. Subjects were
run for six trials per day using this procedure until the criterion of
one or fewer errors on 2 consecutive days was reached.
Internal state-shock association task. While half of the
rats were being tested in the T-maze, the other half were being trained in the conditioning chamber (81302; Lafayette Instrument Co.). The
conditioning chamber (29 × 21.5 × 27 cm) had two side
stainless steel walls and two Plexiglas walls comprising the front and
back. On the top was a Plexiglas door through which animals were placed into the chamber. The floor consisted of 18 stainless steel bars measuring 5 mm in diameter with a 1 cm gap between each bar. A 0.9 mA
electric shock could be administered through the grid floor for 0.5 sec. A white Styrofoam cooler (61 × 35.6 × 36.8 cm) with the bottom cut out was placed over the conditioning chamber. A video
camera (CC547; RCA) was mounted on a tripod to record freezing behavior
through the Plexiglas door.
In this task, a brief foot shock was delivered in the chamber,
conditional on the subject's internal state, i.e., food deprivation level. Rats were placed on a food deprivation schedule such that 24 hr
periods of ad libitum food alternated with 24 hr periods of
food deprivation. At the end of a 24 hr period, rats were brought down
to the well lit training room one at a time and placed in the
conditioning chamber for 4 min. Rats in the deprivation-shock (DS)
group were given a brief foot shock at the end of 4 min only on those
days when they were food-deprived; on nondeprived days they received no
foot shock. Animals in the fed-shock (FS) group received foot shock
only on those days when they were not deprived. The rats were trained
for a total of eight sessions, spaced across 11 d. This schedule
prevented foot shocks from alternating across days. The remaining
19 d were extinction trials in which the rats were maintained on
the deprivation schedule and were brought down to the same training
room and placed in the chamber but received no shock.
After this experiment, subjects were trained in an olfactory
discrimination task not reported here (Hock and Bunsey, 1997).
| |
RESULTS |
T-maze experiments
DH (n = 8), VH (n = 8), and
sham-lesioned (n = 9) rats did not differ in the zero
delay training (p > 0.1) (Fig.
1A). For the 5 min
delayed alternation task, the dependent measure of errors to criterion
was evaluated using a one-way ANOVA. For the
errors-to-criterion-dependent variable, there was a significant
effect of lesion (F(2,24) = 4.93;
p = 0.017), and further a priori tests using
a Fisher's least significant difference test found DH [mean (M) = 23.37] made significantly (p < 0.05)
more errors than both VH (M = 10.5) and controls (M = 13.33).
VH and controls were not significantly different from each other
(p > 0.1) (Fig. 1B).
View larger version (23K):
[in this window]
[in a new window]
|
Figure 1.
A, The effects of DH, VH, and sham
lesions on the zero delay alternation in the T-maze.
Bars represent mean + SEM errors to criterion.
B, The effects of DH, VH, and sham lesions on delayed
alternation in the T-maze. Bars represent mean + SEM
errors to criterion.
|
|
Internal state-conditional task
For DH (n = 9), VH (n = 9), and
sham-lesioned (n = 8) rats, learning was indexed by
preferential freezing when in the internal state associated with shock.
Freezing behavior was classified as skeletal muscle immobility as
defined by Fanselow and Bolles (1979).
Behavior was videotaped and scored by tabulating freezing once every 10 sec during the entire 4 min interval, with a maximum possible score of
24 for a session. The dependent measure used in subsequent analyses was
a d' score for a pair of days calculated by subtracting the
amount of freezing on the nonshocked day from the amount of freezing on
the shocked day, divided by the total freezing score for both days.
This was done for each of two pairs of days chosen a priori.
Based on the data of Davidson and Jarrard (1993) and our pilot
data, we chose for analysis the last 2 d of training and the third
and fourth days of extinction. The first 2 d of extinction were
dropped because of a videotape failure. It was during this block of
trials, at the end of training and beginning of extinction, that
controls have shown maximal learning, whereas hippocampals have
demonstrated clear impairment (Davidson and Jarrard, 1993).
A repeated measures analysis revealed a significant effect of treatment
(F(2,22) = 3.89; p = 0.036) but
no interaction between treatment and session (p > 0.1). Further analysis between DH and controls yielded a significant
treatment effect (F(1,14) = 8.65; p = 0.011), as did an analysis comparing VH and
controls (F(1,14) = 4.82; p = 0.046) (Fig. 2).
View larger version (13K):
[in this window]
[in a new window]
|
Figure 2.
The effect of DH and VH lesions in the internal
state-shock association task. Freezing d' scores are plotted with SEs.
A score of 0 represents chance performance (i.e., equal freezing in
both conditions), whereas scores >0 represent greater freezing in the
shock-associated state, and scores <0 represent less freezing in the
shock-associated state.
|
|
In all groups, there was little to no freezing at any point before the
first shock. Groups also did not differ in terms of absolute amount of
freezing (p > 0.1), nor was there an
interaction between treatment and session (p > 0.1), although numerically VH froze less than the other two groups
(Table 2).
Histology
Three subjects, two DH and one VH, had little or no apparent
damage to the target structure, likely because of blockage of the
syringe during surgery, and were dropped before analysis. The remaining
subjects in the DH group had substantial DH ablation bilaterally, with
minimal damage to overlying cortex and to VH (Fig.
3). DH rats had an average loss of 60%
of dorsal tissue (SEM = 7.29), comparable with previous studies
(Bunsey and Eichenbaum, 1995) with much of the sparing at the rostral
and caudal extremes of DH. The volume of VH in these subjects was 90%
of controls (SEM = 5.34), with most of this VH loss reflecting
shrinkage rather than direct damage. In two of the DH rats, there was
substantial bilateral cortical damage over some of the lesion (Fig. 3),
and in two subjects there was unilateral damage. Most VH subjects had
substantial ablation of VH with little or no apparent damage to DH
(Fig. 4). These rats had an average loss
of 43% of VH tissue (SEM = 6.04). This is somewhat less than the
ablation in DH subjects, consistent with previous reports of sparing of
some VH tissue, especially at the ventral tip of VH (Jarrard, 1989;
Bunsey and Eichenbaum, 1995). These subjects also had a shrinkage
(15%) of DH (SEM = 5.46), again with no apparent disruption of
cell layers.
View larger version (52K):
[in this window]
[in a new window]
|
Figure 3.
Coronal sections of six slides of DH lesions
showing minimal (dark areas) and maximal (shaded
areas) damage.
|
|
View larger version (48K):
[in this window]
[in a new window]
|
Figure 4.
Coronal sections of five slides of VH lesions
showing minimal (dark areas) and maximal (shaded
areas) damage.
|
|
| |
DISCUSSION |
The present results revealed an impairment after DH, but not VH,
lesions in reinforced delayed alternation, as was expected based on
previous studies (Hughes, 1965; Stevens and Cowey, 1973; Sinnamon et
al., 1978; Moser et al., 1993, 1995), and impairments after either
lesion in an internal state-conditional task. This latter result
provides the first evidence for a learning impairment after specific VH
lesions. Together, these findings provide further, but still limited,
evidence for functional dissociations along the septotemporal extent of
the hippocampus. The impairment in delayed reinforced alternation in
the T-maze in rats with DH, but not VH, lesions is consistent with past
research using other spatial memory tasks (Hughes, 1965; Stevens and
Cowey, 1973; Sinnamon et al., 1978; Moser et al., 1993, 1995) and
extends the result to a task different from those used in previous
studies. An important advantage of the use of the present delayed
alternation task is that hippocampals perform normally at short delays,
making it is possible to demonstrate a delay-dependent impairment
(O'Keefe and Nadel, 1978) and thus allowing us to attribute any
deficit to impaired memory rather than deficits in other nonspecific
processes. It is not always possible to demonstrate delay dependence in
other spatial tasks, because hippocampals are impaired at even the
shortest delays. The normal performance of hippocampals with short
delays in the T-maze may be attributable to the constraints on
responding in this task; subjects can only turn left or right on
any trial. In many other tasks, such as the Morris water maze, there
are fewer choice constraints. A second important feature regarding the
present spatial deficit is that it was observed after a specific neurotoxin-induced lesion (Moser et al., 1995). Specific lesions are
especially important in this type of study, because traditional lesions
(e.g., electrolytic lesions), in destroying fibers of passage, cannot
reliably restrict disruption to one-half of the hippocampus.
Nonspecificity of lesion may be responsible for the fact that in
earlier studies VH subjects were somewhat impaired in spatial learning,
albeit less than DHs (Hughes, 1965; Sinnamon et al., 1978). Although
the DH lesions were larger than the VH on average, lesion size was not
likely responsible for the group differences in light of the existing
literature (Moser, et al., 1995). These results thus add to the growing
body of evidence suggesting a preferential role for DH over VH in
spatial memory. As noted above, electrophysiological data provide
converging evidence for this framework, showing that place cells are
more numerous and spatially selective in the DH than in the VH (Jung et
al., 1994; Poucet et al., 1994). Anatomical data are also consistent with this view, indicating that spatial information (i.e., visual and
other sensory information) seems to be directed predominantly to DH in
rats (Deacon et al., 1983).
In contrast to the delayed alternation data, the present results
revealed impairments after either DH or VH lesions in the internal
state-conditional task. Earlier studies had demonstrated impairment in
VH rats in "probability discrimination" (Stevens and Cowey, 1973)
and in extinction in a drink suppression task (Nadel, 1968). These
deficits are difficult to interpret given the use of electrolytic
lesions and the potential role of hyperactivity in hippocampal subjects
as a mechanism for the observed results. The deficits in the present
study were consequent to relatively small neurotoxic lesions. It is
hypothesized that the present impairment after VH lesions was
attributable to impaired ability to form associations with the internal
state-conditional cues. Davidson and Jarrard (1993) provided strong
evidence that impaired learning of this task in rats with full
hippocampal lesions was critically dependent on the use of internal
state as a conditional cue. Hippocampal rats were unimpaired under
training conditions that were very similar, with the exception that
subjects were tested with an auditory cue-predicting shock (Davidson
and Jarrard, 1993). Subjects with specific hippocampal lesions have
also been shown to be unimpaired in conditional tasks using olfactory
or visual conditional cues (Murray et al., 1993; Bunsey and Eichenbaum, 1996). The use of internal state cues thus seems critical in observing a hippocampal impairment in this type of conditional learning. That
this same deficit would be seen in animals with specific VH lesions was
predicted given the hypothalamic projections to this region of
hippocampus (Kohler et al., 1986). Although speculative, it is
possible that this same mechanism may be responsible for the other
impairments seen in VH rats (Nadel, 1968; Stevens and Cowey, 1973). For
example, Stevens and Cowey (1973) found VH subjects to be impaired in a
situation in which they were required to learn relative rates of
reinforcement in two arms of a T-maze in which one arm was rewarded
70% of the time, and the other was rewarded 30% of the time.
Performance in this task would require a comparison of memories of
reinforcement histories in the two arms. Internal states would
constitute a large component of these memories.
It is unclear why conditional tasks using internal states as cues would
be more vulnerable to hippocampal damage than conditional tasks using
other sensory modalities. This difference is most likely attributable
to neuroanatomical differences among the various sensory modalities.
Specifically, information from most sensory modalities converges in
perirhinal and entorhinal cortices before reaching the hippocampus
(Deacon et al., 1983). These parahippocampal areas may be sufficient as
a substrate for conditional learning, either within or across sensory
modalities, after hippocampal damage (Eichenbaum and Bunsey, 1995;
Gluck and Myers, 1995). It is possible that the critical information
about internal states does not first go through perirhinal and
entorhinal cortex but rather is carried within the projection from
hypothalamus to VH; VH lesions would thus prevent this information from
converging with other sensory information and cause a conditional
learning impairment.
Finally, it is unclear why DH lesions caused an impairment in the
internal state-conditional task. One possibility is that both DH and VH
are critical for the processing of internal states. A second
possibility is that acquisition of the internal state-conditional task
used here requires processing of both internal and external contextual
cues. Davidson and Benoit (1996) have recently reported that external
context does play an important role in learning this task.
Specifically, subjects learn not merely that a particular internal
state predicts shock but rather that an internal state experienced in a
particular external context (i.e., the conditioning chamber) predicts
shock. This spatial-contextual component may account for the
impairment after DH lesions. Notably, these data do not show a double
dissociation between DH and VH, and as such it remains possible that DH
lesions are simply more disruptive than VH lesions. Performance in the
internal state-conditional task may be impaired after either lesion
merely because it is more vulnerable to hippocampal damage than to
performance in spatial tasks and thus "requires" less total
hippocampal disruption. Nonetheless, in conjunction with
electrophysiological and anatomical data, the present results seem to
strengthen the case that functional dissociations do exist along the
septotemporal extent of the hippocampus.
| |
FOOTNOTES |
Received March 5, 1998; revised June 15, 1998; accepted June 18, 1998.
This work was supported by National Institutes of Health FIRST
Award R29 N536962-01 (M.D.B.). We thank Dr. Doug Kline for assistance
with photography.
Correspondence should be addressed to Michael Bunsey or Brian Hock, 118 Kent Hall, Kent State University, Kent, OH 44242.
| |
REFERENCES |
-
Bunsey MD,
Eichenbaum H
(1995)
Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulus-stimulus association.
Hippocampus
5:546-556[Web of Science][Medline].
-
Bunsey MD,
Eichenbaum H
(1996)
Conservation of hippocampal memory function in rats and humans.
Nature
379:255-257[Medline].
-
Davidson TL,
Benoit SC
(1996)
The learned function of food-deprivation cues: a role for conditioned modulation.
Anim Learn Behav
24:46-56.
-
Davidson TL,
Jarrard LE
(1993)
A role for hippocampus in the utilization of hunger signals.
Behav Neural Biol
59:167-171[Medline].
-
Deacon TW,
Eichenbaum HE,
Rosenberg P,
Eckman KW
(1983)
Afferent connections of the perirhinal cortex in the rat.
J Comp Neurol
220:168-190[Web of Science][Medline].
-
Eichenbaum H,
Bunsey M
(1995)
On the binding of associations in memory: clues from studies on the role of the hippocampal region in paired-associate learning.
Curr Direct Psychol Sci
4:19-23.
-
Fanselow MS,
Bolles RC
(1979)
Naloxone and shock-elicited feeding in the rat.
J Comp Physiol Psychol
93:236-244.
-
Gluck MA,
Myers CE
(1995)
Representation and association in memory: a neurocomputational view of hippocampal function.
Curr Direct Psychol Sci
4:23-29.
-
Gunderson HJG,
Jensen ER
(1987)
The efficiency of systematic sampling in sterology and its prediction.
J Microsc
147:229-263[Medline].
-
Hock Jr BJ,
Bunsey MD
(1997)
Differential effects of dorsal and ventral hippocampal lesions.
Soc Neurosci Abstr
23:1958.
-
Hughes KR
(1965)
Dorsal and ventral hippocampal lesions and maze learning: influence of preoperative environment.
Can J Psychol
19:325-332[Web of Science][Medline].
-
Jarrard LE
(1989)
On the use of ibotenic acid to lesion selectively different components of the hippocampal system.
J Neurosci Methods
29:251-259[Web of Science][Medline].
-
Jung MW,
Weiner SI,
McNaughton BL
(1994)
Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat.
J Neurosci
14:7347-7356[Abstract].
-
Kohler C,
Swanson LW,
Haglund L,
Wus J
(1985)
The cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat.
Neuroscience
16:85-110[Web of Science][Medline].
-
Kohler C,
Ericson H,
Watanabe T,
Polak J,
Palay SL,
Palay V,
Chan-Palay V
(1986)
Galanin immunoreactivity in hypothalamic histamine neurons: further evidence for multiple chemical messengers in the tuberomammillary nucleus.
J Comp Neurol
250:58-64[Medline].
-
Moser E,
Moser M,
Andersen P
(1993)
Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions but is hardly present following ventral lesions.
J Neurosci
13:3916-3925[Abstract].
-
Moser M,
Moser E,
Forrest E,
Andersen P,
Morris RG
(1995)
Spatial learning with the minislab in the dorsal hippocampus.
Proc Natl Acad Sci USA
92:9697-9701[Abstract/Free Full Text].
-
Murray EA,
Gaffan D,
Mishkin M
(1993)
Neural substrates of visual stimulus-stimulus association in rhesus monkeys.
J Neurosci
13:4549-4561[Abstract].
-
Nadel L
(1968)
Dorsal and ventral hippocampus lesions and behavior.
Physiol Behav
3:891-900.
-
O'Keefe J,
Nadel L
(1978)
In: The hippocampus as a cognitive map. Oxford: Oxford UP.
-
Poucet B,
Thinus-Blanc C,
Muller RU
(1994)
Place cells in the ventral hippocampus of rats.
NeuroReport
5:2045-2048[Web of Science][Medline].
-
Risold PY,
Swanson LW
(1996)
Structural evidence for functional domains in the rat hippocampus.
Science
272:1484-1486[Abstract].
-
Sinnamon HM,
Freniere S,
Kootz J
(1978)
Rat hippocampus and memory for places of changing significance.
J Comp Physiol Psychol
92:142-155[Medline].
-
Stevens R,
Cowey A
(1973)
Effects of dorsal and ventral hippocampal lesions on spontaneous alternation, learned alternation, and probability learning in rats.
Brain Res
52:203-224[Medline].
-
Thomas G
(1978)
Delayed alternation in rats after pre- or postcommissural fornicotomy.
J Comp Physiol Psychol
92:1128-1136[Medline].
Copyright © 1998 Society for Neuroscience 0270-6474/98/18177027-06$05.00/0
This article has been cited by other articles:
|
|
|
|
 
K. Woollett, H. J. Spiers, and E. A. Maguire
Talent in the taxi: a model system for exploring expertise
Phil Trans R Soc B,
May 27, 2009;
364(1522):
1407 - 1416.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Ainge, M. Tamosiunaite, F. Woergoetter, and P. A. Dudchenko
Hippocampal CA1 Place Cells Encode Intended Destination on a Maze with Multiple Choice Points
J. Neurosci.,
September 5, 2007;
27(36):
9769 - 9779.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Rekart, C. J. Sandoval, F. Bermudez-Rattoni, and A. Routtenberg
Remodeling of hippocampal mossy fibers is selectively induced seven days after the acquisition of a spatial but not a cued reference memory task
Learn. Mem.,
June 6, 2007;
14(6):
416 - 421.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Otto and P. Poon
Dorsal hippocampal contributions to unimodal contextual conditioning.
J. Neurosci.,
June 14, 2006;
26(24):
6603 - 6609.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. J. Kennedy and M. L. Shapiro
Retrieving Memories via Internal Context Requires the Hippocampus
J. Neurosci.,
August 4, 2004;
24(31):
6979 - 6985.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. guzman-marin, N. Suntsova, D. R Stewart, H. Gong, R. Szymusiak, and D. McGinty
Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats
J. Physiol.,
June 1, 2003;
549(2):
563 - 571.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. R. Stefani and P. E. Gold
Intrahippocampal Infusions of K-ATP Channel Modulators Influence Spontaneous Alternation Performance: Relationships to Acetylcholine Release in the Hippocampus
J. Neurosci.,
January 15, 2001;
21(2):
609 - 614.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. D. Vann, M. W. Brown, J. T. Erichsen, and J. P. Aggleton
Fos Imaging Reveals Differential Patterns of Hippocampal and Parahippocampal Subfield Activation in Rats in Response to Different Spatial Memory Tests
J. Neurosci.,
April 1, 2000;
20(7):
2711 - 2718.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Maguire, D. G. Gadian, I. S. Johnsrude, C. D. Good, J. Ashburner, R. S. J. Frackowiak, and C. D. Frith
Navigation-related structural change in the hippocampi of taxi drivers
PNAS,
April 11, 2000;
97(8):
4398 - 4403.
[Abstract]
[Full Text]
[PDF]
|
|
|
Top
Abstract
Introduction
