 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 9, Issue of May 1, 1997 pp. 3254-3261
Copyright ©1997 Society for NeuroscienceRepeated Cocaine Modifies the Mechanism by which Amphetamine Releases Dopamine
R. Christopher Pierce and Peter W. Kalivas Alcohol and Drug Abuse Program, Washington State University, Pullman, Washington 99164-6520
ABSTRACT
This study determined whether daily cocaine administration initiates a calcium requirement for the increase in extracellular dopamine produced by psychostimulants. The increase in extracellular dopamine induced by perfusion of amphetamine through a microdialysis probe in the nucleus accumbens shell was enhanced in cocaine- relative to saline-pretreated rats. The augmented portion of the amphetamine-induced increase in nucleus accumbens dopamine was abolished by the coperfusion of L- or N-type calcium channel blockers. Inhibition of calcium/calmodulin-dependent protein kinase II (CaM-KII) also prevented the augmented increase in dopamine by amphetamine, whereas inhibition of vesicular exocytosis by botulinum toxin B was ineffective. When the concentration of extracellular dopamine in the nucleus accumbens was elevated by blocking the plasmallemal dopamine transporter with GBR-12909, the augmented increase in extracellular dopamine in rats sensitized to repeated cocaine was blocked by a CaM-KII inhibitor. Pretreatment with botulinum toxin B prevented the increase in extracellular dopamine by GBR-12909 in both cocaine-pretreated and control rats. Taken together, these results demonstrate that the psychostimulant-induced enhanced increase in extracellular dopamine in the nucleus accumbens shell of cocaine-pretreated rats arises from the induction of calcium- and CaM-KII-dependent mechanisms.
Key words: behavioral sensitization; cocaine; amphetamine; GBR-12909; verapamil; conotoxin; diltiazem; KN-93; botulinum toxin; calcium; calmodulin
INTRODUCTION
The abuse of amphetamine-like psychostimulants is a medical and social problem throughout the world. The behavioral stimulant and reinforcing properties of amphetamine-like stimulants are linked to the capacity of these drugs to increase extracellular concentrations of dopamine in the forebrain, notably in the nucleus accumbens (Wise and Bozarth, 1987
; Koob and Bloom, 1988
Recent findings indicate that calcium-dependent protein kinases are critically involved in activity-dependent synaptic modifications (Calabresi et al., 1994
To appraise potential mechanisms underlying the calcium requirement for the augmented increase in extracellular dopamine in cocaine-sensitized animals, the present study estimated the effects of various compounds that block calcium channels or inhibit calcium-calmodulin-stimulated kinases on the increase in extracellular dopamine in the nucleus accumbens shell produced by psychostimulants. Two psychostimulants were used: GBR-12909, which blocks the dopamine transporter in a manner similar to cocaine (Van der Zee et al., 1980
MATERIALS AND METHODS
Subjects. All of the experiments described in this report were performed in accordance with the specifications of the Washington State University Animal Care and Use Committee. Male Sprague Dawley rats (Simmonsen Laboratories, Gilroy, CA) were individually housed with food and water available ad libitum. A 12 hr light/dark cycle was used with the lights on at 6:30 A.M. All cocaine injections, behavioral testing, and microdialysis were performed during the light cycle.
Repeated cocaine or saline treatment. Equal numbers of subjects were assigned to the cocaine and saline groups. The day before the start of the experiment, all animals were habituated to the photocell boxes (Omnitech Electronics, Columbus, OH) for 3 hr. On the first treatment day, all animals were habituated to the photocell boxes for 1 hr. After habituation, animals received either cocaine (15 mg/kg, i.p.; donated by the National Institute of Drug Abuse) or saline (1.0 ml/kg, i.p.), and behavior subsequently was monitored for 2 hr. On days 2-6, rats received daily injections of cocaine (30 mg/kg, i.p.) or saline in the home cage. On the seventh day, all animals were again habituated to the photocell boxes for 1 hr. Cocaine (15 mg/kg) or saline then was administered i.p., and behavior was monitored for 2 hr.
Surgery. Stereotaxic implantation of a dialysis guide cannula was conducted 2 weeks after the last injection of cocaine or saline. Rats weighing 300 to 350 gm were anesthetized with Equithesin (3.0 ml/kg) and mounted in a stereotaxic apparatus. A unilateral microdialysis guide cannula (12 mm, 20 gauge stainless steel) was implanted 2 mm dorsal to the nucleus accumbens shell (1.0 mm anterior; 0.8 mm lateral relative to bregma; Paxinos and Watson, 1986
Microdialysis and measurement of extracellular dopamine. The dialysis probes were constructed as described by Robinson and Whishaw (1988) -conotoxin (1 µM; Research Biochemicals). After baseline and 100 min of one of the calcium channel antagonists alone, increasing concentrations of amphetamine (0.1, 1.0, and 10.0 µM) or GBR-12909 (1.0, 10.0, and 100.0 µM) were incorporated into the dialysis buffer for 100 min each. The effect of the CaM-KII inhibitor KN-93 also was assessed. After baseline and 100 min of KN-93 (10 µM; Calbiochem, San Diego, CA) alone, increasing concentrations of amphetamine (0.1, 1.0, and 10.0 µM) or GBR-12909 (1.0, 10.0, and 100.0 µM) were incorporated into the dialysis buffer for 100 min each. The effect of the negative control compound for KN-93, KN-92, also was assessed. After baseline and 100 min of KN-92 (10 µM; Calbiochem, San Diego, CA) alone, increasing concentrations of amphetamine (0.1, 1.0, and 10.0 µM) were incorporated into the dialysis buffer for 100 min each. In the final experiments, the rats were pretreated with a microinfusion of botulinum toxin B (1.0 ng/µl, 0.3 µl; Sigma, St. Louis, MO) or saline (0.3 µl) into the nucleus accumbens 15 min before inserting the microdialysis probe. The next day, after 100 min of baseline, increasing concentrations of amphetamine (0.1, 1.0, and 10.0 µM) or GBR-12909 (1.0, 10.0, and 100.0 µM) were incorporated into the dialysis buffer for 100 min each. In all cases microdialysis samples were taken every 20 min.
For the measurement of extracellular dopamine, samples were collected into microfuge tubes containing 20 µl of mobile phase (0.1 M citric acid, 75 mM Na2HPO4, 1.5 mM heptanosulfonic acid, 0.1 mM EDTA, 15% methanol, v/v, pH 4.2) plus 2.0 pmol of dihydroxybenzylamine as an internal standard. After collection, all samples were frozen at 80°C until analyzed. The samples were subsequently thawed and placed in an autosampler (Gilson Medical Supplies, Middleton, WI) connected to an HPLC system with electrochemical detection. The dopamine was separated using a 25 cm C18 reversed phase column (Bioanalytical Systems, West LaFayette, IN) and oxidized/reduced using coulometric detection (ESA, Bedford, MA). Three electrodes were used: a preinjection port guard cell (+0.4 V) to oxidize the mobile phase, an oxidation analytical electrode (+0.3 V), and a reduction analytical electrode (
Histology. After the dialysis experiment, the rats were given an overdose of pentobarbital (>100 mg/kg, i.p.) and perfused intracardially with PBS, followed by 10% formalin. The brain was removed and stored in 10% formalin for at least 1 week. The brains were then blocked, and coronal sections (100 µm) were taken at the level of the nucleus accumbens with a vibratome. The sections were mounted on gelatin-coated slides and stained with cresyl violet. Probe and cannula placements were determined according to the atlas of Paxinos and Watson (1986)
Data analysis. The effect of amphetamine or GBR-12909 on extracellular dopamine was evaluated using a two-way ANOVA with repeated measures over dose. Pairwise comparisons between cocaine and saline treatment groups were made with Fisher's LSD. The effect of calcium channel antagonists on basal extracellular levels of dopamine was examined by averaging the last two samples of baseline collection and comparing this with the average of the last two samples with a calcium antagonist alone with a paired t test. The effect of botulinum toxin B on basal extracellular dopamine was determined by comparing the average of the last two baseline samples in rats pretreated with a microinfusion of botulinum toxin B with the average of the last two baseline samples from rats pretreated with a saline microinfusion with a t test.
RESULTS
Behavioral sensitization to cocaine
Table 1 shows the total horizontal photocell counts for the 2 hr after the first and last injection of daily cocaine or saline. The behavioral response to the last cocaine injection was enhanced relative to the first cocaine administration in all groups. In contrast, there was no consistent change in the behavioral response to saline on the seventh compared to the first injection.
Table 1. Effect of seven daily intraperitoneal administrations of saline or cocaine on horizontal activity in the rat
n Day 1a Day 7 Statisticsb Amphetamine Saline 13 7973 (658)c 9907 (2032) t(12) = 0.929, p = 0.3711 Cocaine 12 11513 (1464) 20039 (2565) t(11) = 02.39, p = 0.0358 GBR-12909 Saline 9 4747 (467) 7588 (1063) t(8) = 02.42, p = 0.0422 Cocaine 8 13119 (2159) 25159 (3574) t(7) = 03.04, p < 0.0188 Amphetamine + verapamil Saline 7 4002 (627) 6840 (533) t(6) = 03.45, p = 0.0136 Cocaine 9 14402 (1627) 25123 (1755) t(8) = 09.14, p = 0.0001 Amphetamine + diltiazem Saline 10 4035 (1036) 5322 (762) t(9) = 01.14, p = 0.2822 Cocaine 10 13738 (2212) 19085 (7247) t(9) = 02.99, p = 0.0153 Amphetamine + Saline 10 4419 (360) 5627 (907) t(9) = 01.36, p = 0.2064 Cocaine 8 13460 (2352) 21193 (3793) t(7) = 02.55, p = 0.0382 Botulinum toxin-amphetamine Saline 7 5894 (1029) 6418 (1164) t(6) = 0.452, p = 0.6673 Cocaine 10 15096 (3380) 21260 (4325) t(9) = 01.30, p = 0.2265 Botulinum toxin-GBR-12909 Saline 6 3466 (146) 5962 (1245) t(5) = 01.89, p = 0.1168 Cocaine 6 11826 (4786) 32261 (4093) t(5) = 07.66, p = 0.0006 Amphetamine + KN-93 Saline 9 3739 (551) 7578 (1438) t(8) = 02.53, p = 0.0351 Cocaine 8 9266 (2345) 21481 (2472) t(7) = 04.28, p = 0.0036 Amphetamine + KN-92 Saline 9 7025 (902) 5583 (911) t(8) = 01.13, p = 0.2935 Cocaine 8 16799 (3311) 22599 (4717) t(7) = 01.14, p = 0.2900 GBR-12909 + KN-93 Saline 11 5928 (953) 9270 (1324) t(10) = 02.16, p = 0.0558 Cocaine 16 12376 (1975) 19257 (2643) t(15) = 01.93, p = 0.0729 a Cocaine or saline was administered daily for 1 week. Day 1 corresponds to the first and day 7 the last daily injection. Horizontal activity was measured on days 1 and 7 after an intraperitoneal injection of cocaine (15 mg/kg) or saline. On days 2-6, the subjects received an intraperitoneal injection of either cocaine (30 mg/kg) or saline and were returned to their home cage. b Paired t test; degrees of freedom in parentheses. c The data are presented as the total horizontal photocell counts (SE) recorded over the first 120 min after cocaine or saline injection. Effect of calcium channel blockers, KN-93, KN-92, and botulinum toxin on basal levels of extracellular dopamine
Table 2 outlines the influence of the calcium channel blockers, the CaM-KII inhibitor KN-93, the KN-93 control compound KN-92, or botulinum toxin on basal levels of extracellular dopamine in the nucleus accumbens shell. Preliminary dose-response curves were conducted for the channel blockers and KN-93 to determine a dose that decreased basal extracellular dopamine by 30-50% from baseline. As shown in Table 2, the calcium channel blockers reduced the extracellular dopamine concentration in the nucleus accumbens by 24-52% relative to baseline in rats pretreated with either saline or cocaine. Because the preliminary dose-response curve for KN-93 did not reveal a change in the basal extracellular levels of dopamine, the dose used was based on IC50 values from in vitro studies allowing for an estimated 10% efficiency of diffusion across the dialysis membrane (Sumi et al., 1991
Table 2. Effects of calcium channel antagonists, KN-93, KN-92, or botulinum toxin B on the baseline concentration of extracellular dopamine in the nucleus accumbens shell
n Baselinea Drugb % Baseline Botulinum toxin-amphetaminec Saline 13/7 39 (7) 19 (4)* 49 Cocaine 12/10 41 (8) 12 (2)* 29 Botulinum toxin-GBR-12909 Saline 9/6 31 (13) 15 (9) 48 Cocaine 8/6 31 (12) 15 (15) 48 Amphetamine + verapamil Saline 7 42 (10) 29 (8)* 69 Cocaine 9 29 (6) 22 (4)* 76 Amphetamine + diltiazem Saline 10 25 (6) 16 (3)* 64 Cocaine 10 54 (15) 40 (18) 74 Amphetamine + conotoxin Saline 10 25 (7) 16 (3)* 64 Cocaine 8 21 (5) 12 (4) 74 Amphetamine + KN-93 Saline 9 32 (8) 35 (8) 109 Cocaine 8 33 (5) 38 (6) 115 Amphetamine + KN-92 Saline 9 51 (10) 63 (11) 124 Cocaine 8 79 (15) 78 (10) 99 GBR-12909 + KN-93 Saline 11 25 (3) 29 (5) 116 Cocaine 16 35 (6) 43 (9) 123 a Baseline extracellular dopamine in the nucleus accumbens shell (uncorrected for recovery). These values represent the mean (SE) fmol/sample of the average of the last two baseline samples (60-100 min from the onset of the experiment). b Alterations in baseline extracellular dopamine induced by calcium channel antagonists KN-93, KN-92, or botulinum toxin. These values represent the mean (SE) fmol/sample of the average of the last two samples taken 60-100 min after one of these compounds was included in the microdialysis buffer (160-200 min from the onset of the experiment). c The baseline and drug data from the botulinum toxin experiments are from separate groups of rats. The baseline amphetamine group represents the combination of subjects that either did (n = 8) or did not (n = 17) receive a saline microinfusion (0.3 µl/60 sec) into the nucleus accumbens the day before the microdialysis experiment. The data from these subjects did not significantly differ and were pooled. All of the animals in the baseline GBR-12909 group received an intra-accumbens microinfusion of saline before the implantation of the microdialysis probe. These baseline samples correspond to the amphetamine and GBR-12909 baseline data presented in Figure 1. The "drug" column represents animals that received an intra-accumbal microinfusion of botulinum toxin (1.0 ng/µl, 0.3 µl) the day before the microdialysis experiment (i.e., the baseline values of the amphetamine and GBR-12909 experiments summarized in Fig. 3). * Significant difference between the drug and baseline dopamine values (p < 0.05, t test).
In contrast to the calcium channel antagonists, KN-93, and KN-92, which were administered through the microdialysis probe, botulinum toxin B was microinfused into the nucleus accumbens before inserting the microdialysis probe. This method of administration was required because the molecular weight of botulinum toxin B (>100,000) is beyond the cutoff for diffusion through the dialysis membrane. As shown in Table 2, this route of administration was effective because botulinum toxin reduced the baseline levels of dopamine in the nucleus accumbens 51-71% relative to the basal levels obtained in the experiments summarized in Figure 1. 
Fig. 1. The effect of amphetamine (A) and GBR-12909 (B) on extracellular dopamine in the nucleus accumbens 3 weeks after repeated saline or cocaine treatment. Baseline samples were collected for 100 min, and then three increasing concentrations of amphetamine (0.1, 1.0, and 10 µM) or GBR-12909 (1, 10, and 100 µM) were incorporated into the dialysis buffer for 100 min each (400 min experiment total). The data are depicted as the mean ± SE fmol dopamine per 20 min sample and were statistically evaluated with a two-way repeated measures ANOVA (amphetamine dose × pretreatment with repeated measures/dose). For amphetamine there was a significant main effect of amphetamine (F(19,437) = 34.42; p < 0.0001) and a significant amphetamine × pretreatment interaction (F(38,437) = 4.01; p < 0.0001). For GBR-12909, there was a significant main effect of amphetamine (F(19,285) = 6.31; p < 0.0001) and a significant amphetamine × pretreatment interaction (F(19,285) = 2.104; p = 0.0051). *Significant difference from saline (p < 0.05, Fisher's LSD).
[View Larger Version of this Image (18K GIF file)]
Effect of amphetamine or GBR-12909
The data outlined in Figure 1A demonstrate that amphetamine produced a dose-dependent increase in extracellular dopamine in the nucleus accumbens shell and that this effect was significantly enhanced in animals pretreated with cocaine. Likewise, the capacity of GBR-12909 to increase extracellular dopamine was enhanced in cocaine- relative to saline-pretreated rats (Fig. 1B).Effect of calcium channel antagonists
Figure 2 demonstrates that blockade of calcium channels with verapamil (L-type), diltiazem (L-type), or
Fig. 2. Effects of L-type (100 µM verapamil and 10 µM diltiazem) and N-type (1 µM conotoxin) calcium channel antagonists on amphetamine-induced increases in extracellular dopamine in the nucleus accumbens of saline- and cocaine-pretreated rats. After 100 min of baseline, a calcium antagonist was incorporated into the dialysis buffer for 100 min. For the next 300 min of the experiment, three increasing doses of amphetamine (0.1-10 µM, 100 min each) were included in the dialysis buffer in the presence of the same calcium channel blocker. In all three experiments, there was a significant main effect of amphetamine dose [verapamil (V), F(24,336) = 15.25, p < 0.0001; conotoxin (C), F(24,384) = 19.21, p < 0.0001; diltiazem (D), F(24,342) = 60.28, p < 0.0001]. There were no other significant main effects or interactions.
[View Larger Version of this Image (16K GIF file)]
Effect of botulinum toxin B
Figure 3 shows that, even though the maximal effect of amphetamine was blunted by pretreatment with botulinum toxin B, the augmented increase in extracellular dopamine among cocaine-sensitized rats was unaffected. In contrast, botulinum toxin B pretreatment eliminated the capacity of GBR-12909 to elevate extracellular dopamine in both the cocaine and saline groups.
Fig. 3. The effect of botulinum toxin B on amphetamine (top)- or GBR-12909 (bottom)-induced increases in extracellular dopamine in the nucleus accumbens of saline- and cocaine-pretreated rats. Botulinum toxin B (1.0 ng/µl, 0.3 µl) was unilaterally microinfused (via a 33 gauge cannula) into the nucleus accumbens through the microdialysis cannula 15 min before the placement of the microdialysis probe. For the amphetamine experiment, a two-way ANOVA revealed a significant main effect of amphetamine dose (F(19,285) = 24.28, p < 0.0001) and a significant interaction between treatment groups and dose of amphetamine (F(19,285) = 1.59, p = 0.058). For the GBR-12909 experiment, there was a significant main effect of GBR-12909 dose (F(19,190) = 2.12, p = 0.0058); there were no other significant main effects or interactions. *Significant difference from saline (p < 0.05, Fisher's LSD).
[View Larger Version of this Image (18K GIF file)]
Effect of KN-93 and KN-92
Figure 4 illustrates that, similar to the calcium channel antagonists (see Fig. 2), inhibition of CaM-KII with KN-93 prevented the augmented increase in extracellular dopamine induced by amphetamine in cocaine-pretreated animals. KN-93 also inhibited the augmented increase in extracellular dopamine produced by GBR-12909 in subjects pretreated with cocaine. KN-93 did not alter the capacity of amphetamine or GBR-12909 to elevate extracellular dopamine in the nucleus accumbens of saline-pretreated subjects. In contrast, KN-92, the control compound for KN-93, did not influence the amphetamine-induced increase in extracellular dopamine in the nucleus accumbens in saline-pretreated rats or the augmented release of dopamine observed in cocaine-sensitized rats.
Fig. 4. The effect of the CaM-KII blocker, KN-93, on amphetamine- or GBR-12909-induced increases in extracellular dopamine in the nucleus accumbens of saline- and cocaine-pretreated rats. Baseline samples were collected for 100 min, followed by 100 min of KN-93 (10 µM). For the remaining 300 min of the experiment, three increasing concentrations of amphetamine (0.1, 1.0, and 10 µM) or GBR-12909 (1, 10, and 100 µM) were incorporated into the dialysis buffer for 100 min each with 10 µM KN-93. For the amphetamine experiment, there was a significant main effect of amphetamine dose (F(19,285) = 26.25; p < 0.0001), with no other significant treatment effects or interactions. For the GBR-12909 experiment, there was a significant main effect of GBR-12909 dose (F(19,475) = 9.77; p < 0.0001), with no other significant treatment effects or interactions. The effects of the KN-93 control compound, KN-92, also were assessed on amphetamine-induced increases in extracellular dopamine in the nucleus accumbens of saline- and cocaine-pretreated rats. The design of the experiment was identical to the amphetamine experiment described above, except that KN-92 (10 µM) was substituted for KN-93. The analysis of this experiment revealed a significant main effect of amphetamine dose (F(19,285) = 8.77; p < 0.0001) and a significant amphetamine × treatment interaction (F(19,285) = 1.59; p = 0.05). *Significant difference from saline (p < 0.05, Fisher's LSD).
[View Larger Version of this Image (23K GIF file)]
Histology
Figure 5A depicts microdialysis probe placements in the shell of the nucleus accumbens. The dialysis probes were located in the medial compartment of the shell, not in the lateral limb. Many probes were at the lateral edge of the shell adjacent to the core. Also, in several cases a portion of the active region of the probes was located in the ventral neostriatum. Figure 5, B and C, shows micrographs depicting probe tracts in the nucleus accumbens of rats treated with KN-93 plus GBR-12909 and botulinum toxin B plus amphetamine through the probe, respectively. Note the lack of neurotoxicity after either treatment other than the mechanical damage produced by the microdialysis probe.
Fig. 5. Histological evaluation of dialysis probe placements in the medial nucleus accumbens. A, Composite of the location of all dialysis probe tracts used in data analysis. B, Micrograph taken at the level of the nucleus accumbens. In this animal, KN-93 and GBR-12909 were simultaneously incorporated into the microdialysis buffer. C, Micrograph of the nucleus accumbens of a rat that was microinfused with botulinum toxin B; amphetamine subsequently was applied locally to the nucleus accumbens. Scale bar, 100 µM. Note the lack of neurotoxicity in B and C, other than the mechanical damage produced by the microdialysis probe. The white arrows indicate the mechanical damage produced by the microdialysis probe. The black arrows point to intact cells located near the microdialysis probe.
[View Larger Version of this Image (109K GIF file)]
DISCUSSION
The present results demonstrate that the enhanced increase in extracellular dopamine in the nucleus accumbens shell of cocaine-sensitized rats arises from the induction of a requirement for calcium- and CaM-KII-dependent mechanisms. This finding is consistent with the calcium-dependent increase in extracellular dopamine induced by dopamine reuptake blockers, such as GBR-12909. However, because the amphetamine-induced increase in extracellular dopamine occurs in the absence of calcium-mediated vesicular exocytosis in saline-pretreated rats, the calcium-dependent portion of the amphetamine neurochemical response represents a shift in the mechanism of action of this drug after the repeated administration of cocaine.Behavioral sensitization and dopamine in the nucleus accumbens
Consistent with previous findings (Pierce and Kalivas, 1995Role of calcium
The present data clearly indicate a role for L- and N-type calcium conductances in the augmented increase in extracellular dopamine induced by amphetamine or GBR-12909 in the nucleus accumbens of cocaine-sensitized rats. The results of the GBR-12909 experiments are consistent with evidence that impairing impulse flow or presynaptic calcium influx severely impairs the ability of dopamine reuptake blockers to increase extracellular dopamine (Carboni et al., 1989
The distinction between the mechanisms of action of GBR-12909 and amphetamine was verified in the experiments in which animals were pretreated with an intra-accumbens microinjection of botulinum toxin B, which cleaves synaptobrevin, thereby preventing vesicular fusion with the plasma membrane (Burgoyne and Morgan, 1995 Role of CaM-KII
The CaM-KII inhibitor KN-93 abolished the augmented increase in extracellular dopamine produced by either amphetamine or GBR-12909 in rats sensitized to cocaine. The induction of a CaM-KII-dependent mechanism in the expression of behavioral sensitization to psychostimulants is consistent with biochemical measurements showing increased calmodulin activity in rats pretreated with daily amphetamine (Gnegy et al., 1991
A second possibility resides in the influence of CaM-KII on synaptic vesicles. CaM-KII promotes the undocking of vesicles from cytoskeletal proteins in preparation for exocytosis by phosphorylating synapsin I (Lin et al., 1990 Clinical implications
The data presented herein show that repeated cocaine initiates an enduring requirement for calcium and the activation of CaM-KII for the augmented increase in dopamine in the nucleus accumbens induced by amphetamine or GBR-12909. A pathophysiological change in dopamine transmission in the nucleus accumbens is a major candidate in the etiology of psychostimulant-induced psychiatric disorders (Segal et al., 1981
FOOTNOTES
Received Oct. 28, 1996; revised Feb. 3, 1997; accepted Feb. 6, 1997.
This research was supported in part by the Washington State Alcohol and Drug Abuse Program and U.S. Public Health Service Grants MH-40817, DA-03906, Research Career Development Award DA-00158 (P.W.K.), and National Research Service Award DA-05589 (R.C.P.).
Correspondence should be addressed to Dr. Chris Pierce, Department of VCAPP, Washington State University, Pullman, WA 99164-6520.
REFERENCES
- Burgoyne RD, Morgan A (1995) Ca2+ and secretory-vesicle dynamics. Trends Neurosci 18:191-196[ISI][Medline].
- Calabresi P, Pisani a Mercuri NB, Bernardi G (1994) Post-receptor mechanisms underlying striatal long-term depression. J Neurosci 14:4871-4881[Abstract].
- Carboni E, Imperato A, Perezzani L, Di Chiara G (1989) Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats. Neuroscience 28:653-661[ISI][Medline].
- Di Chiara G (1995) The role of dopamine in drug abuse from the perspective of its role in motivation. Drug Alcohol Depend 38:95-137[ISI][Medline].
- Ellinwood EH (1967) Amphetamine psychosis. I. Description of the individuals and process. J Nerv Ment Dis 144:273-283[ISI].
- Fischer JF, Cho AK (1979) Chemical release of dopamine from striatal homogenates: evidence for an exchange diffusion model. J Pharmacol Exp Ther 208:203-209
[Free Full Text] .- Gnegy ME, Hewlett GHK, Yee SL, Welsh MJ (1991) Alterations in calmodulin content and localization in areas of rat brain after repeated intermittent amphetamine. Brain Res 562:6-12[ISI][Medline].
- Heidbreder CA, Thompson AC, Shippenberg TS (1996) Role of extracellular dopamine in the initiation and long-term expression of behavioral sensitization to cocaine. J Pharmacol Exp Ther 278:490-502
[Abstract/Free Full Text] .- Iwata S, Hewlett GHK, Ferrell ST, Czernik AJ, Meiri K, Gnegy ME (1996) Increased in vivo phosphorylation state of neuromodulin and synapsin I in striatum from rats treated with repeated amphetamine. J Pharmacol Exp Ther 278:1428-1434
[Abstract/Free Full Text] .- Kalivas PW, Duffy P (1993) Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals. J Neurosci 13:266-275[Abstract].
- Karler R, Turkanis SA, Partlow LM, Calder LD (1991) Calcium channel blockers in behavioral sensitization. Life Sci 49:165-170[ISI][Medline].
- Koob GF, Bloom FE (1988) Cellular and molecular mechanisms of drug dependence. Science 242:715-723
[Abstract/Free Full Text] .- Kuzcenski R (1983) Biochemical actions of amphetamine and other stimulant. In: Stimulants: neurochemical, behavioral and clinical perspectives (Creese I, ed), pp 31-61. New York: Raven.
- Liang NY, Rutledge CO (1982) Comparison of the release of [3H]dopamine from isolated corpus striatum by amphetamine, fenfluamine and unlabeled dopamine. J Pharmacol Exp Ther 202:544-557
[Free Full Text] .- Lin JW, Sugimori M, Llinas RR, McGuiness TL, Greengard P (1990) Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. Proc Natl Acad Sci USA 82:8257-8261.
- Lisman J (1994) The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 17:406-412[ISI][Medline].
- Martellotta MC, Kuzmin A, Muglia P, Gessa GL, Fratta W (1994) Effections of the calcium antagonist isadipine on cocaine intravenous self-administration in rats. Psychopharmacology 113:378-380[Medline].
- Martin-Iverson MT, Reimer AR (1994) Effects of minodipine and/or haloperidol on the expression of conditioned locomotion and sensitization to cocaine in rats. Psychopharmacology 114:315-320[Medline].
- Nestler EJ (1992) Molecular mechanisms of drug addiction. J Neurosci 12:2439-2450[ISI][Medline].
- Nomikos GG, Damsma G, Wenkstern D, Fibiger HC (1990) In vivo characterization of locally applied dopamine uptake inhibitors by striatal microdialysis. Synapse 6:106-112[ISI][Medline].
- Pani L, Carboni S, Kusmin A, Gessa GL, Rossetti ZL (1990) Nimodipine inhibits cocaine-induced dopamine release and motor stimulation. Eur J Pharmacol 176:245-246[ISI][Medline].
- Pani L, Kuzmin A, Martellotta MC, Gessa GL, Fratta W (1991) The calcium antagonist PN 200-110 inhibits the reinforcing properties of cocaine. Brain Res Bull 26:445-447[ISI][Medline].
- Paulson PE, Robinson TE (1995) Amphetamine-induced time-dependent sensitization of dopamine neurotransmission in the dorsal and ventral striatum: a microdialysis study in behaving rats. Synapse 19:56-65[ISI][Medline].
- Paxinos G, Watson C (1986) In: The rat brain in stereotaxic coordinates. New York: Academic.
- Pierce RC, Kalivas PW (1995) Amphetamine produces sensitized increases in locomotion and extracellular dopamine preferentially in the nucleus accumbens shell of rats administered repeated cocaine. J Pharmacol Exp Ther 275:1019-1029
[Abstract/Free Full Text] .- Post RM, Weiss SRB (1988) Sensitization and kindling: implications for the evolution of psychiatric symptomatology. In: Sensitization in the nervous system (Kalivas PW, Barnes CD, eds), pp 257-292. Caldwell, NJ: Telford.
- Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 18:247-291[Medline].
- Robinson TE, Whishaw IQ (1988) Normalization of extracellular dopamine in the striatum following recovery from a partial unilateral 6-OHDA lesion of the substantia nigra: a microdialysis study in freely moving rats. Brain Res 450:209-224[ISI][Medline].
- Rosenweig-Lipson S, Barrett JE (1995) Modification of the behavioral effects of (±)BAY k 8644, cocaine and d-amphetamine by L-type calcium channel blockers in squirrel monkeys. J Pharmacol Exp Ther 274:842-851
[Abstract/Free Full Text] .- Schweizer FE, Betz H, Augustine GJ (1995) From vesicle docking to endocytosis: intermediate reactions of exocytosis. Neuron 14:689-696[ISI][Medline].
- Segal DS, Kuczenski R (1992a) In vivo microdialysis reveals a diminished amphetamine-induced dopamine response corresponding to behavioral sensitization produced by repeated amphetamine pretreatment. Brain Res 521:330-332.
- Segal DS, Kuczenski R (1992b) Repeated cocaine administration induces behavioral sensitization and corresponding decreased extracellular dopamine responses in caudate and accumbens. Brain Res 577:351-355[ISI][Medline].
- Segal DS, Geyer MA, Schuckit MA (1981) Stimulant-induced psychosis: an evaluation of animal models. In: Essays in neurochemistry and neuropharmacology, Vol 5 (Youdim MBH, Lovenberg W, Sharman DF, Lagnado JR, eds), pp 95-129. London: Wiley.
- Seiden LS, Sabol KE, Ricuarte GA (1993) Amphetamine: effects on catecholamine systems and behavior. Annu Rev Pharmacol Toxicol 33:639-677[ISI][Medline].
- Sumi M, Kiuchi K, Ishikawa T, Ishii A, Hagiwara M, Nagatsu T, Hidaka H (1991) The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181:968-975[ISI][Medline].
- Uchikawa T, Kiuchi Y, Yura A, Nakachi N, Yamazaki Y, Yokomizo C, Oguchi K (1995) Ca2+-dependent enhancement of [3H]dopamine uptake in rat striatum: possible involvement of calmodulin-dependent kinases. J Neurochem 65:2065-2071[ISI][Medline].
- Van der Zee P, Koger HS, Gootjes J, Hespe W (1980) Aryl 1,4-dialk(en)ylpiperazines as selective and very potent inhibitors of dopamine uptake. Eur J Med Chem Chim Ther 15:363-370.
- Warburton EC, Mitchell SN, Joseph MH (1996) Calcium dependence of sensitized dopamine release in rat nucleus accumbens following amphetamine challenge: implications for the disruption of latent inhibition. Behav Pharmacol 7:119-129.[ISI][Medline]
- Westerink BHC, Hofsteede RM, Tuntler J, de Vries JB (1989) Use of calcium antagonism for the characterization of drug-evoked dopamine release from the brain of conscious rats determined by microdialysis. J Neurochem 52:722-729[ISI][Medline].
- Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94:469-492[ISI][Medline].
- Wolf ME, White FJ, Nassar R, Brooderson RJ, Khansa MR (1993) Differential development of autoreceptor subsensitivity and enhanced dopamine release during amphetamine sensitization. J Pharmacol Exp Ther 264:249-255
[Abstract/Free Full Text] .
Copyright ©1997 Society for Neuroscience 0270-6474/1997/173254-08$05.00/0
This article has been cited by other articles:
X. Sun, M. Milovanovic, Y. Zhao, and M. E. Wolf
Acute and Chronic Dopamine Receptor Stimulation Modulates AMPA Receptor Trafficking in Nucleus Accumbens Neurons Cocultured with Prefrontal Cortex Neurons
J. Neurosci., April 16, 2008; 28(16): 4216 - 4230.
[Abstract] [Full Text] [PDF]
B. J. Venton, A. T. Seipel, P. E. M. Phillips, W. C. Wetsel, D. Gitler, P. Greengard, G. J. Augustine, and R. M. Wightman
Cocaine increases dopamine release by mobilization of a synapsin-dependent reserve pool.
J. Neurosci., March 22, 2006; 26(12): 3206 - 3209.
[Abstract] [Full Text] [PDF]
R. D. Blakely, L. J. DeFelice, and A. Galli
Biogenic Amine Neurotransmitter Transporters: Just When You Thought You Knew Them
Physiology, August 1, 2005; 20(4): 225 - 231.
[Abstract] [Full Text] [PDF]
L. Kantor, M. Zhang, B. Guptaroy, Y. H. Park, and M. E. Gnegy
Repeated Amphetamine Couples Norepinephrine Transporter and Calcium Channel Activities in PC12 Cells
J. Pharmacol. Exp. Ther., December 1, 2004; 311(3): 1044 - 1051.
[Abstract] [Full Text] [PDF]
O. Cooper and O. Isacson
Intrastriatal Transforming Growth Factor {alpha} Delivery to a Model of Parkinson's Disease Induces Proliferation and Migration of Endogenous Adult Neural Progenitor Cells without Differentiation into Dopaminergic Neurons
J. Neurosci., October 13, 2004; 24(41): 8924 - 8931.
[Abstract] [Full Text] [PDF]
A. Rajadhyaksha, I. Husson, S. S. Satpute, K. D. Kuppenbender, J. Q. Ren, R. M. Guerriero, D. G. Standaert, and B. E. Kosofsky
L-Type Ca2+ Channels Mediate Adaptation of Extracellular Signal-Regulated Kinase 1/2 Phosphorylation in the Ventral Tegmental Area after Chronic Amphetamine Treatment
J. Neurosci., August 25, 2004; 24(34): 7464 - 7476.
[Abstract] [Full Text] [PDF]
E. Backes and S. E. Hemby
Discrete Cell Gene Profiling of Ventral Tegmental Dopamine Neurons after Acute and Chronic Cocaine Self-Administration
J. Pharmacol. Exp. Ther., November 1, 2003; 307(2): 450 - 459.
[Abstract] [Full Text] [PDF]
K. McFarland, C. C. Lapish, and P. W. Kalivas
Prefrontal Glutamate Release into the Core of the Nucleus Accumbens Mediates Cocaine-Induced Reinstatement of Drug-Seeking Behavior
J. Neurosci., April 15, 2003; 23(8): 3531 - 3537.
[Abstract] [Full Text] [PDF]
H. Khoshbouei, H. Wang, J. D. Lechleiter, J. A. Javitch, and A. Galli
Amphetamine-induced Dopamine Efflux. A VOLTAGE-SENSITIVE AND INTRACELLULAR Na+-DEPENDENT MECHANISM
J. Biol. Chem., March 28, 2003; 278(14): 12070 - 12077.
[Abstract] [Full Text] [PDF]
C. A. Paladini, S. Robinson, H. Morikawa, J. T. Williams, and R. D. Palmiter
Dopamine controls the firing pattern of dopamine neurons via a network feedback mechanism
PNAS, March 4, 2003; 100(5): 2866 - 2871.
[Abstract] [Full Text] [PDF]
P. Vezina, D. S. Lorrain, G. M. Arnold, J. D. Austin, and N. Suto
Sensitization of Midbrain Dopamine Neuron Reactivity Promotes the Pursuit of Amphetamine
J. Neurosci., June 1, 2002; 22(11): 4654 - 4662.
[Abstract] [Full Text] [PDF]
C. J. Swanson, D. A. Baker, D. Carson, P. F. Worley, and P. W. Kalivas
Repeated Cocaine Administration Attenuates Group I Metabotropic Glutamate Receptor-Mediated Glutamate Release and Behavioral Activation: A Potential Role for Homer
J. Neurosci., November 15, 2001; 21(22): 9043 - 9052.
[Abstract] [Full Text] [PDF]
Y. Schmitz, C. J. Lee, C. Schmauss, F. Gonon, and D. Sulzer
Amphetamine Distorts Stimulation-Dependent Dopamine Overflow: Effects on D2 Autoreceptors, Transporters, and Synaptic Vesicle Stores
J. Neurosci., August 15, 2001; 21(16): 5916 - 5924.
[Abstract] [Full Text] [PDF]
K. C. Bradley and R. L. Meisel
Sexual Behavior Induction of c-Fos in the Nucleus Accumbens and Amphetamine-Stimulated Locomotor Activity Are Sensitized by Previous Sexual Experience in Female Syrian Hamsters
J. Neurosci., March 15, 2001; 21(6): 2123 - 2130.
[Abstract] [Full Text] [PDF]
M. Okada, D. J. Nutt, T. Murakami, G. Zhu, A. Kamata, Y. Kawata, and S. Kaneko
Adenosine Receptor Subtypes Modulate Two Major Functional Pathways for Hippocampal Serotonin Release
J. Neurosci., January 15, 2001; 21(2): 628 - 640.
[Abstract] [Full Text] [PDF]
ABSTRACT
