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The Journal of Neuroscience, June 15, 1999, 19(12):5119-5123
Basolateral Amygdala Noradrenergic Influences on Memory Storage
Are Mediated by an Interaction between  - and
 1-Adrenoceptors
Barbara
Ferry,
Benno
Roozendaal, and
James L.
McGaugh
Center for the Neurobiology of Learning and Memory and Department
of Neurobiology and Behavior, University of California, Irvine,
California 92697-3800
 |
ABSTRACT |
Extensive evidence indicates that norepinephrine modulates memory
storage through an activation of  -adrenoceptors in the basolateral
nucleus of the amygdala (BLA). Recent findings suggest that the effects
of -adrenergic activation on memory storage are influenced by
 1-adrenoceptor stimulation. Pharmacological findings
indicate that activation of postsynaptic 1-adrenoceptors potentiates -adrenoceptor-mediated activation of cAMP
formation. The present study examined whether inactivation of
1-adrenoceptors in the BLA would alter the
dose-response effects on memory storage of intra-BLA infusions of a
-adrenoceptor agonist, as well as that of a synthetic cAMP analog.
Male Sprague Dawley rats received bilateral microinfusions into the BLA
of either the -adrenoceptor agonist clenbuterol (3-3000 pmol in 0.2 µl) or 8-bromoadenosine 3':5'-cyclic monophosphate
(8-bromo-cAMP) (0.2-7 nmol in 0.2 µl) alone or together with
the 1-adrenoceptor antagonist prazosin (0.2 nmol)
immediately after training in an inhibitory avoidance task. Retention
was tested 48 hr later. Clenbuterol induced a dose-dependent
enhancement of retention, and prazosin attenuated the dose-response
effects of clenbuterol. Posttraining intra-BLA infusions of
8-bromo-cAMP also induced a dose-dependent enhancement of retention
latencies. However, concurrent infusion of prazosin did not alter the
dose-response effects of 8-bromo-cAMP. These findings are consistent
with the view that 1-adrenoceptors affect memory storage
by modulating -adrenoceptor activation in the BLA. Moreover, these
findings are consistent with those of pharmacological studies
indicating that -adrenoceptors modulate memory storage by a direct
coupling to adenylate cyclase, whereas 1-receptors act
indirectly by influencing the -adrenoceptor-mediated influence on
cAMP formation.
Key words:
basolateral amygdala; 1-adrenoceptor; -adrenoceptor; norepinephrine; memory storage; cAMP
| |
INTRODUCTION |
Several lines of evidence suggest
that the storage of information for inhibitory avoidance training is
regulated by -adrenergic influences within the amygdaloid complex
(McGaugh et al., 1993 ). Posttraining infusions of norepinephrine or the
-adrenoceptor agonist clenbuterol into the amygdala enhance memory
storage (Liang et al., 1990; Introini-Collison et al., 1991). More
recent findings from our laboratory suggest that the memory-modulatory
effects of the -adrenoceptor system of the amygdala are mediated
selectively by the basolateral nucleus of the amygdala (BLA). Infusions
of -adrenoceptor antagonists administered into the BLA, and not the
central nucleus (CN), block the memory-enhancing effects of posttraining systemic injections of glucocorticoids (Quirarte et al.,
1997). Posttraining infusions of norepinephrine or the -adrenoceptor
agonist clenbuterol into the BLA enhance retention of inhibitory
avoidance and water-maze training (Ferry and McGaugh, 1999; Hatfield
and McGaugh, 1999).
Other recent findings from our laboratory indicate that the
noradrenergic influence on memory storage also involves activation of
1-adrenoceptors. Posttraining infusions of the selective
1-adrenoceptor antagonist prazosin administered into the
BLA impair inhibitory avoidance retention, whereas selective activation
of 1-adrenoceptors enhances retention (Ferry et al.,
1999). Furthermore, the memory-modulatory effects of norepinephrine in
the BLA appear to be mediated by an interaction between
1- and -adrenoceptors. Posttraining infusions of the -adrenoceptor antagonist atenolol into the BLA block
the memory enhancement induced by selective
1-adrenoceptor activation (Ferry et al., 1999). These
results suggest that the role of the 1-adrenoceptor
system in regulating memory storage involves modulation of
-adrenergic activity. These findings are consistent with evidence that 1- and -adrenoceptors interact in modulating
catecholamine-induced physiological responses in the rat brain (Perkins
and Moore, 1973; Schultz and Daly, 1973; Stone et al., 1987).
It is known that the generation of second messengers, such as cAMP,
permits the distribution of cell-surface regulatory input within the
cell interior, amplification of the initial signal, and enables
synergistic or antagonistic regulation of other signaling pathways.
Norepinephrine has been shown to increase cAMP levels in brain tissue
(Burkard, 1972), an effect involving an interaction between - and
1-adrenoceptors (Rall and Sattin, 1970; Huang and Daly,
1972; Schultz and Daly, 1973). The -adrenoceptor is coupled directly
to adenylate cyclase via the guanine-nucleotide-binding regulatory Gs
protein (Pfeuffer, 1977; Ross et al., 1978), whereas the
1-adrenoceptor site appears to be indirectly coupled to
the cAMP-generating system by potentiating the response induced by -adrenoceptor activation (Perkins and Moore, 1973; Daly et al., 1980).
The present study examined further the interaction of - and
1-adrenoceptor activation in the BLA and the coupling to
the cAMP system in memory storage. A first experiment examined the functional interaction between the two receptor types in regulating memory storage. Rats received microinfusions of clenbuterol, a -adrenoceptor agonist, alone or together with the
1-adrenoceptor antagonist prazosin into the BLA
immediately after training in an inhibitory avoidance task. A second
experiment investigated whether the influence of
1-adrenoceptors on memory occurs before or after the
-adrenoceptor-mediated cAMP formation. To address this issue, the
effects of posttraining intra-BLA infusions of 8-bromoadenosine
3':5'-cyclic monophosphate (8-bromo-cAMP) (an analog of cAMP
that passes the cell membrane) were examined when administered alone or
together with prazosin.
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MATERIALS AND METHODS |
Subjects. Male Sprague Dawley rats (n = 254; body weight, 270-300 gm at the time of surgery) from Charles
River Laboratories (Wilmington, MA) were used. After arrival,
they were individually housed in a temperature-controlled (22°C)
colony room and maintained on a standard 12 hr light/dark cycle (lights
on from 7:00 A.M. to 7:00 P.M.) with access to food and water
ad libitum. All experiments were performed
during the light phase of the cycle between 10:00 A.M. and 2:00
P.M..
Surgery. One week after arrival, the animals were
anesthetized with sodium pentobarbital (50 mg/kg body weight, i.p.) and given atropine sulfate (0.4 mg/kg, i.p.) to suppress salivation. The
skull was fixed in a flat position to a stereotaxic frame (Kopf
Instruments, Tujunga, CA), and stainless steel cannulas (23 gauge, 15 mm long) were implanted bilaterally 2 mm dorsal to the BLA
(coordinates: anteroposterior,  2.8 mm from bregma; mediolateral,
±5.0 mm from midline; dorsoventral, 6.7 mm from skull surface)
according to the atlas of Paxinos and Watson (1986). The cannulas and
two anchoring screws were affixed to the skull with
dental cement. Stylets (15-mm-long 00 insect dissection pins) were
inserted into each cannula to maintain patency and were removed only
for the infusion of drugs. The rats were allowed to recover a minimum
of 7 d and were handled 1 min each day for 3 consecutive days
before training was initiated.
Drugs and infusion procedures. Clenbuterol
(4-amino-a-[t-butylaminomethyl]-3,5-dichlorobenzyl alcohol
hydrochloride; Sigma, St. Louis, MO), a selective
1-adrenoceptor agonist, prazosin (1-[4-amino-6,7-dimethoxy-2-quinazolinyl]-4-[2-furanylcarbonyl] piperazine; Sigma), a selective 1-adrenoceptor
antagonist, and 8-bromo-cAMP (Sigma) were used. The compounds were
dissolved in 0.9% saline. Control animals received saline only.
Clenbuterol (3, 30, 300, or 3000 pmol/side) and 8-bromo-cAMP (0.2, 0.7, 2, or 7 nmol/side) were infused alone or in combination with prazosin (0.2 nmol) into the BLA immediately after the training session. The
doses of clenbuterol and prazosin were selected on the basis of
previous experiments (Liang et al., 1995; Ferry and McGaugh, 1999),
whereas the doses of 8-bromo-cAMP were selected from a recent study by
Bernabeu and colleagues (1997). Solutions of all drugs were prepared
freshly before each experiment. Bilateral intra-BLA infusions of saline
or drug were made using 30 gauge injection needles connected to a 10 µl Hamilton microsyringe by polyethylene (PE 20) tubing. The
injection needles protruded 2 mm beyond the tips of the cannulas to
reach the BLA. A 0.2 µl injection volume per side was infused for 23 sec by an automated syringe pump (Sage Instruments, Boston, MA). To
allow diffusion of the drug, the injection needles were retained within
the cannulas for an additional 50 sec after drug infusion. The infusion
volume was based on our findings that selective neurotoxically induced lesions of the BLA are produced with an infusion volume of 0.2 µl
(Roozendaal and McGaugh, 1996). Furthermore, drug infusions of this
volume into either the BLA or the adjacent CN induce markedly differential effects on memory storage (Parent and McGaugh, 1994; Roozendaal and McGaugh, 1997). After infusion, the animal was returned
to its home cage.
Inhibitory avoidance apparatus and procedures. The
inhibitory avoidance apparatus consisted of a trough-shaped alley (91 cm long, 15 cm deep, 20 cm wide at the top, 6.4 cm wide at the floor) divided into two compartments separated by a sliding door that opened
by retracting into the floor. The starting compartment (31 cm long) was
illuminated, and the shock compartment (60 cm long) was dark (McGaugh
et al., 1988). The apparatus was located in a light- and
sound-attenuated room.
The rat was placed in the starting compartment, with the door opened,
and was allowed to enter the dark compartment. After the rat stepped
completely into the dark compartment, the door was closed, and a mild
inescapable foot shock (0.40 mA, 1.0 sec) was administered. Animals
with entrance latencies longer than 30 sec were eliminated from the
study. The rat was removed from the dark alley 15 sec after termination
of the foot shock and immediately given bilateral microinfusions of
either saline or drug into the BLA. On the 48 hr retention test, the
rat was placed in the starting compartment, as in the training session,
and the latency to enter the dark compartment (maximum latency of 600 sec) was recorded and used as the measure of retention. Shock was not
administered on the retention test trial.
Histology. After completion of behavioral testing, the rats
were anesthetized with an overdose of sodium pentobarbital (100 mg/kg)
and perfused intracardially with a 0.9% saline (w/v) solution, followed by 4% formaldehyde (w/v). After decapitation, the brains were
removed and placed in 4% formaldehyde. At least 24 hr before sectioning, the brains were placed in a 15% sucrose (w/v) solution for
cryoprotection. Sections of 40 µm were made (using a freezing microtome) and stained with cresyl violet. The sections were examined under a light microscope, and determination of the location of cannula
tips in the BLA was made according to the standardized atlas plates of
Paxinos and Watson (1986).
Statistics. Retention data were analyzed with two-way ANOVAs
with clenbuterol (five levels) or 8-bromo-cAMP (five levels) and
prazosin (two levels), both as between-subject variables. Further
analysis used Fisher's post hoc tests to determine
the source of the detected significances in the ANOVAs. A probability level of < 0.05 was accepted as statistically significant. The number
of animals per group is indicated in the figure legends.
| |
RESULTS |
Figure 1 shows a representative
location of the infusion needle tip in the BLA. Behavioral data from
228 animals were included in the analysis. Histological analysis
revealed that 26 animals had incorrect cannula placements. The results
of these animals were not included in the analyses.
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Figure 1.
a, Schematic representation of the
amygdaloid complex. The solid lines indicate the
position of the photomicrograph (b) representing
the cannula (top arrow) and the injection tip
(bottom arrow) placement. L, Lateral
nucleus of the amygdala.
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|
The retention test latencies of rats given posttraining infusions of
one of several doses of clenbuterol alone or in combination with
prazosin into the BLA are shown in Figure
2. A two-way ANOVA revealed a significant
clenbuterol effect (F(4,99) = 8.71;
p < 0.001) and a significant interaction between
clenbuterol and prazosin (F(4,99) = 11.21;
p < 0.001). Clenbuterol enhanced retention latencies when infused in the lowest dose only (3 pmol; p < 0.001) compared with the saline controls. Infusion of higher doses of
clenbuterol (30, 300, and 3000 pmol) had no significant effect on
retention. Concurrent infusions of prazosin into the BLA shifted the
dose-response effects of clenbuterol to the right. The
retention-enhancing effect observed with the infusion of 3 pmol of
clenbuterol was blocked by prazosin (p < 0.001). In prazosin-treated animals, significant increases in retention
latencies were found with infusions of higher doses of clenbuterol (300 and 3000 pmol; both, p < 0.001).
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Figure 2.
Inhibitory avoidance retention latencies of
animals that received posttraining infusion of several doses of the
selective -adrenoceptor agonist clenbuterol alone or in combination
with the selective 1-adrenoceptor antagonist prazosin
into the BLA. Error bars represent mean ± SEM latency (in
seconds) to enter the dark compartment on the retention test.
**p < 0.01; ***p < 0.001 compared with vehicle-infused group;  p < 0.001 compared with the corresponding groups infused with clenbuterol
alone. n = 9-12 per group.
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The retention test latencies of rats given posttraining intra-BLA
infusions of various doses of 8-bromo-cAMP alone or in combination with
prazosin are shown in Figure 3. A two-way
ANOVA revealed a significant 8-bromo-cAMP effect
(F(4,109) = 11.46; p < 0.001) but no prazosin effect (F(1,109) = 0.70;
NS) or interaction between the two factors
(F(4,109) = 0.66; NS). 8-Bromo-cAMP enhanced
retention latencies when infused in the lowest dose only (0.2 nmol;
p < 0.001) compared with the controls. Infusion of the
higher doses of 8-bromo-cAMP (0.7, 2, and 7 nmol) were ineffective.
Concurrent infusions of prazosin into the BLA did not alter the
dose-response effects of 8-bromo-cAMP on memory storage. The same low
dose of 8-bromo-cAMP (0.2 nmol) enhanced retention latencies when
infused either alone or together with prazosin
(p < 0.001).
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Figure 3.
Inhibitory avoidance retention latencies of
animals that received posttraining infusion of several doses of
8-bromo-cAMP, an analog of cAMP that passes the cell membrane, alone or
in combination with the selective 1-adrenoceptor
antagonist prazosin into the BLA. Error bars represent mean ± SEM
latency (in seconds) to enter the dark compartment on the retention
test. ***p < 0.001 compared with vehicle-infused
group. n = 10-13 per group.
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| |
DISCUSSION |
There are two main findings of these experiments. First, they
provide further evidence that and 1 components of
the adrenoceptor system in the BLA are involved in modulating memory
storage. Second, infusions of the second messenger cAMP analog
8-bromo-cAMP into the BLA enhanced inhibitory avoidance retention
performance, and the effect of infusions of 8-bromo-cAMP on memory does
not depend on 1-adrenoceptor activity. These findings
clearly suggest that the effect of 1-adrenoceptors on
memory occurs at the level of the -adrenoceptor-mediated cAMP generation.
The results of the first experiment indicate that the memory-modulatory
effects of -adrenoceptors in the BLA are mediated by an interaction
with 1-adrenoceptors. The finding that prazosin blocked
the memory-enhancing effect induced by a low dose of clenbuterol and
attenuated its dose-response effects clearly suggests that 1-adrenoceptors in the BLA influence the effect of
-adrenoceptor activation on memory storage. These findings are in
agreement with extensive evidence indicating that activation of
-adrenergic mechanisms in the amygdala (in particular in the BLA)
induces dose-dependent memory enhancement (Liang et al., 1986, 1990;
Introini-Collison et al., 1989, 1991; Ferry and McGaugh, 1999; Hatfield
and McGaugh, 1999). These findings are also in agreement with evidence
implicating 1-adrenergic mechanisms in memory
consolidation processes. Sternberg et al. (1986) reported that
pretraining systemic injections of the nonselective -adrenoceptor
antagonist phentolamine attenuated the memory-enhancing effect of
peripherally administered epinephrine. Puumala et al. (1998) found that
pretraining stimulation of 1-adrenoceptors facilitates
acquisition of the water-maze task. Furthermore, our results are
consistent with evidence suggesting an involvement of amygdala
-adrenoceptors in the influence of norepinephrine on memory storage.
Gallagher and Kapp (1981) found that posttraining infusions of various
doses of the nonselective -adrenoceptor antagonist phentolamine into
the amygdala induced a dose-dependent enhancement of retention
latencies in an inhibitory avoidance task. The inverted U-shaped curve
of retention latencies suggests that 2- and
1-adrenoceptors (both present in the amygdala;
U'Prichard et al., 1980) may be differentially involved in modulating
memory storage. At low doses, phentolamine enhances norepinephrine
activity by facilitating its release through blockade of presynaptic
2-adrenoceptors (Starke, 1979). At higher doses,
phentolamine also acts on postsynaptic 1-adrenoceptors.
More recently, we reported that the memory-enhancing effects induced by
selective activation of 1-adrenoceptors in the BLA were
blocked by a concomitant infusion of the -adrenoceptor antagonist
atenolol (Ferry et al., 1999). These results suggest that
1-adrenoceptor-induced retention enhancement involves
-adrenoceptor activation. Our present findings, considered together
with previous results, thus suggest that 1-adrenoceptors
are indirectly involved in modulating memory storage by influencing
-adrenoceptor activation.
Several pharmacological findings suggest that - and
-adrenoceptors are present on the same neurons (Szabadi and
Bradshaw, 1974; Bevan et al., 1977; Szabadi, 1978). In addition,
-adrenoceptor stimulation increases intracellular cAMP levels via a
direct activation of adenylate cyclase (Schultz and Daly, 1973; Taussig
and Gilman, 1995). 1-Adrenoceptors are not coupled to
adenylate cyclase but modulate cAMP release indirectly by potentiating
-adrenoceptor-cAMP responsiveness (Perkins and Moore, 1973; Daly et
al., 1980, 1981; Leblanc and Ciaranello, 1984; Johnson and Minneman,
1986; Pilc and Enna, 1986). In view of these findings, the second
experiment addressed the locus of interaction between the - and
1-adrenoceptors in the BLA. Posttraining infusions of
8-bromo-cAMP into the BLA dose-dependently enhanced retention,
suggesting that the second messenger cAMP in the BLA is involved in
inhibitory avoidance memory storage. This finding is in general
agreement with previous results showing that posttraining infusions of
8-bromo-cAMP into the hippocampus or the amygdala enhanced retention in
the inhibitory avoidance task (Liang et al., 1995; Bernabeu et al.,
1996, 1997). In addition, concurrent administration of prazosin did not
alter the memory-enhancing effect of 8-bromo-cAMP. This finding
provides evidence concerning the interaction between - and
1-adrenoceptors and rules out the possibility that the
1-adrenoceptor modulates memory storage by acting
downstream from cAMP synthesis in the BLA. If that were the case,
infusions of prazosin should have attenuated the dose-response effects
of 8-bromo-cAMP. The lack of effect induced by prazosin suggests that
1-adrenoceptors influence -adrenoceptor-mediated
effects on memory by acting upstream from cAMP formation.
Although these findings are consistent with pharmacological evidence
indicating a direct interaction between postsynaptic 1-
and -adrenoceptors in cAMP synthesis, the lack of effect of prazosin
on the dose-response curve of 8-bromo-cAMP might also reflect an
indirect participation of the 1-adrenoceptors in the -mediated memory storage modulation. It is possible that the role of
the 1-adrenoceptors in memory storage is independent of
the -mediated cAMP generation and might interact with
-adrenoceptors via another intracellular route (Hardman et al.,
1997). Furthermore, although findings of several experiments have
reported colocalization of - and 1-adrenoceptors in
brain neurons (for review, see Szabadi, 1979), it cannot be excluded
that the effects induced by clenbuterol and prazosin are mediated by an
interaction between - and 1-adrenoceptors located on
different cells in the BLA. The presence of - and 1-adrenoceptors on astroglial cells (McCarty and De
Vellis, 1979; Hosli et al., 1982) may be of significance in the
regulation of the response to norepinephrine released from neurons (for
review, see Salm and McCarthy, 1992). Although the role of these
receptors is likely to induce differentiation leading to
morphological changes of the cell (Shain et al., 1987; Bicknell et al.,
1989), it is reasonable to think that these receptors might also
participate in the effects observed in our study. These alternative
explanations of the present findings are highly speculative but cannot
be excluded as yet.
In conclusion, our results indicate that memory storage of inhibitory
avoidance training is modulated by an interaction between - and
1-adrenoceptors in the BLA. Moreover, the present
findings suggest that the memory enhancement induced by -receptor
activation in the BLA is mediated by cAMP generation and that this
process is modulated by 1-adrenoceptor stimulation.
| |
FOOTNOTES |
Received Dec. 17, 1998; revised March 24, 1999; accepted March 30, 1999.
This research was supported by a FYSSEN Foundation grant and a
fellowship from the Ralph and Leona Gerard Family Trust (B.F. and B.R.)
and United States Public Health Service Grant MH12526 from National
Institute of Mental Health (J.L.M.). We thank Jimmy Nong for technical
assistance and Nancy Collett for assistance in the preparation of this manuscript.
Correspondence should be addressed to Dr. Barbara Ferry, Center for the
Neurobiology of Learning and Memory, University of California, Irvine,
CA 92697-3800.
| |
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TOP
ABSTRACT
INTRODUCTION
