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Post-treatment locomotor activity was recorded, in terms of the number of crossings and rearing of the rats in 30 min, in all the 3 groups, 5 min after drug injection. In the isolation-induced aggression model, lithium-treated rats showed a statistical significant decrease in aggressive behaviour i. However, no significant difference was found in the latency time of the first attack. The saccharine preference test did not reveal any significant decrease in the consumption of saccharine by the lithium-treated rats throughout the duration of 4 days.

Lamotrigine did not change the sucrose consumption in the non-stressed rats Table 1. Lamotrigine markedly reduced the aggressive behaviour i. In the morphine-sensitized hyperlocomotion model, lamotrigine-treated rats did not show any significant difference in the crossing and rearing parameters, compared to the control group Table 1. The development of anticonvulsants as carbamazepine, valproate, lamotrigine, etc. The efficacy of the 2 therapeutic agents utilized in the present study, lithium and lamotrigine, is well established in BD.

Lithium acts in BD by suppressing the inositol signalling through depletion of intracellular inositol and by inhibiting glycogen synthase kinase-3 GSK Depression and mania are the 2 most important facets of BD, hence animal models targeting these two facets were chosen in the present study. FST and TST have been thought to create behavioural despair in rats so that they lose hope to escape the stressful environment.

Lack of escape-related behaviour in the rats is considered immobility. It is believed that the chronic mild stress induced in rats is analogous to the psychological stress that humans face, implicated in the aetiology of depression. The increase in the sucrose-seeking behaviour in chronically stressed rats after drug therapy is thought to be representing a reward-seeking behaviour, which is usually absent in anhedonia.

However, these limitations should not devalue their substantial predictive and face validities. In the present study, the CST showed maximum predictive validity amongst models targeting the depression facet of BD as both lithium and lamotrigine showed statistically superior results compared to the FST and TST. This finding is seconded by a previous study which showed that lithium potentiated the antidepressant effect of imipramine and fluoxetine in rats exposed to chronic mild stress.

The animal models employed to evaluate the mania facet of BD were the isolation-induced aggression test, saccharine preference test, and morphine-sensitized hyperlocomotion test. Isolation results in formation of an aggressive behaviour pattern usually absent in normally reared rats. Increase in the brain level of serotonin, dopamine, and norepinephrine has been associated with this increased aggression. This model is based on the corollary that rats with a low preference for saccharine are usually associated with higher anxiety or have been exposed to depressogenic manipulations.

This drug-induced increased locomotor activity is linked with increased dopamine biosynthesis and dopamine-1 receptor firing in the mesolimbic area of the brain. In the present study, amongst the 3 models employed to evaluate mania, the isolation-induced aggression model was found to have the highest predictive validity with superior significance for both lithium and lamotrigine. The significant decrease in the aggressive behaviour in the lithium and lamotrigine groups is in accordance with previous studies.

The Black Swiss strain of mice is identified as having high baseline saccharine consumption, hence is usually preferred in this test. From the above observations the authors propose that CST and isolation-induced aggression test should be a part of a battery of tests used to evaluate mood stabilizers rather than an independent model due to the numerous limitations of present study.

Notably, genetically manipulated models and kindling models were not employed in the study. The predictive validities of other therapeutic agents as valproate, carbamazepine, and atypical antipsychotics were also not evaluated. Amphetamine-induced hyperlocomotion model, considered as the gold standard model for mania was not included in the study due to significant procedural hurdles in its procurement even for scientific research.

Further studies utilizing the above mentioned models along with other standard drugs would help create a comprehensive battery of tests, addressing various facets of BD, to evaluate mood stabilizers and help congregate the data obtained from the present study. Acknowledgments The authors are thankful to Mr.

Dharmender and Mr. Anil Kumar for providing a helping hand in taking care of the rats in the Animal House. Torrent Pharmaceuticals Limited, New Delhi is acknowledged for providing the authors with lithium and lamotrigine salts, free of charge. References 1. Can Fam Physician ;e58—e PMID: Meltzer H.

Basic and Clinical Pharmacology. Antipsychotic Agents and Lithium. New York: McGraw-Hill; The prevalence and disability of bipolar spectrum disorders in the US population: re-analysis of the ECA database taking into account sub- threshold cases. J Affect Disord ;— Kupfer DJ.

The increasing medical burden in bipolar disorder. JAMA ;— Gould TD, Einat H. Animal models of bipolar disorder and mood stabilizer efficacy: a critical need for improvement. Neurosci Biobehav Rev ;— Animal models of neuropsychiatric disorders.

Nat Neurosci ;— Einat H. Establishment of a battery of simple models for facets of bipolar disorder: a practical approach to achieve increased validity, better screening and possible insights into endophenotypes of disease.

Behav Genet ;— Long-term lithium administration abolishes the resistance to stress in rats sensitized to morphine. Brain Res ;— Involvement of AMPA receptors in the antidepressant-like effects of lithium in the mouse tail suspension test and forced swim test. Neuropharmacology ;— Dual monoamine modulation for the antidepressant-like effect of lamotrigine in the modified forced swimming test.

Eur Neuropsychopharmacol ;— Evaluation of the effects of lamotrigine, valproate and carbamazepine in a rodent model of mania. Behav Brain Res ;— Animal models of bipolar disorder. Removing obstacles in neuroscience drug discovery: the future path for animal models. Neuropsychopharmacology ;— Predictive animal models of mania: hits, misses and future directions. The break point was defined as the terminal ratio obtained at the end of each 12 hr session.

A 12 hr light dark cycle was maintained on , off hr. Animals remained in the operant chamber between tests for the duration of the experiment. Univariate post-hoc ANOVA analysis was conducted at each dose to determine which doses differed between genotypes. Genetic differences in progressive-ratio performance were analyzed using a two way repeated-measures ANOVA with each subjects average number of lever presses and average number of reinforcements obtained during the last three days under the FR4 and progressive ratio schedules as the dependent variables.

Data are reported for only those animals with electrode tips located in the lateral hypothalamic portion of the medial forebrain bundle Fig 1. Analysis of the final electrode location was based upon the location of the electrode tip for both genotypes using the Franklin and Paxinos atlas as the common reference using common landmarks such as the fornix, third ventricle, ventromedial hypothalamus and external capsule of each genotype.

In the C57 mice, electrodes were surgically implanted in 12 mice, 11 subjects completed the experiment and had correct electrode placements. One subject was eliminated due to an incorrect electrode placement. In the DBA mice, Electrodes were surgically implanted in 15 mice, 10 subjects completed the experiment and had correct electrode placements.

Five subjects were eliminated due to incorrect electrode placements. There were more missed placements in the DBA group due to the need to adjust stereotaxic coordinates. The symbols are separated to left and right sides in the coronal plane in order to unclutter the diagram, actual placements occurred on the same side in both genotypes, Only those subjects with a verified lateral hypothalamic electrode location were included in the analysis. All of the C57 mice learned to manually turn the manipulandum when each quarter-turn was rewarded with a msec train of Hz lateral hypothalamic electrical stimulation.

The DBA mice were not insensitive to the stimulation since they would quickly orient to and approach the stimulus lights and often contacted the stimulus lights with their nose and mouth during experimenter delivered electrical stimulation. The 6 DBA mice that learned the response took on average 2. Once the animals were seen to respond reliably, they were shifted to the rate-frequency protocol. The stimulation current was adjusted for each mouse in order to position the rate-frequency curve at an M50 value of approximately Hz.

One DBA mouse was dropped from the analysis due to the inability to shift its M50 value lower than Hz. The stimulation current required to produce M50 values that did not differ significantly between genotypes was M for C57 mice and At these current intensities the average M50 value for C57 mice was M and Morphine-induced shifts in rate-frequency curves.

Morphine shifted the rate-frequency functions to the left Fig 2 and decreased M50 values Fig 3. In DBA mice morphine shifted rate-frequency functions to the right Fig. The potentiation of brain stimulation reward in C57 mice and the antagonism in DBA mice were directly related to the dose of morphine Fig. The decrease in M50 values in the C57 mice were statistically significant at the 1. The increase in M50 values in the DBA mice were statistically significant at the 1.

In addition to causing a rightward shift of the rate-frequency curve, morphine depressed the maximum response rate in the DBA animals, and at the highest dose completely suppressed responding. Morphine dose-effect function in C57 and DBA mice. Amphetamine-induced shifts in rate-frequency curves.

Each point represents the mean of 9 and 5, C57 and DBA mice, respectively. In contrast to morphine, amphetamine shifted the rate-frequency curves to the left Fig 4 and decreased M50 values Fig 5 equally in the two genotypes. Amphetamine had no effect on maximal response rate in either genotype. Amphetamine dose-effect function in C57 and DBA mice. Lever presses made each day for water reinforcement. At the start of the water-training protocol, a single lever press resulted in liquid delivery; thereafter, completion of each 50 reinforcements resulted in an increase of the fixed ratio requirement.

The FR requirement was set to the previous day's last FR on days 2, 3, and 4. Each genotype was successfully trained to stable rates of lever pressing for water reinforcement Fig. The DBA animals were found clearly capable of lever-pressing at rates of at least responses per day. This would prove to be approximately times the rate of responding sustained under morphine reinforcement.

Surgery followed the water training period. Significantly higher rates were maintained at the 0. The response rates of the C57 mice were higher for low doses of drug than for saline Fig. The relatively high level of responding during saline substitution is due in part to the water training history and the high levels of responding made at the immediate prior dose.

In the DBA mice, there was no significant difference between lever-pressing for saline and lever-pressing for morphine; further, there were no significant differences in responding across the three morphine dose conditions. Morphine intake in the DBA mice was predictable from the rate of responding under saline reinforcement; the animals made the same number of responses per day regardless of morphine dose and received the amount of drug that accompanied that number of responses at each dose.

Drug intake in both genotypes corresponds directly to response rate and dose. Drug intake in the C57 mice doubled drug intake in the DBA mice at the two lower morphine doses 0. Average drug intake at the initial dose, 1. Intravenous morphine self-administration a Lever pressing behavior as a function of increasing morphine dose per injection. The number of lever presses does not include those that occurred during the time out period. The insert represents the number of lever presses as a function of session number in the order that each dose was tested.

Panels b and c represent the number of lever presses Panel b obtained under a Fixed Ratio 4 and Progressive Ratio schedule of reinforcement. As a consequence of the increased demands placed on obtaining each injection, the number of reinforcements and drug intake decreased when the subjects were placed on the progressive ratio schedule Fig 7c. Thus, in the DBA animals, morphine failed to sustain levels of responding sufficient to maintain a constant rate of drug intake; the number of reinforcements obtained under the progressive ratio schedule dropped significantly compared to the FR4 schedule of reinforcement.

The goal of this study was to characterize the rewarding effects of morphine in the two genotypes most commonly used to map candidate gene loci associated with drug abuse, C57 and DBA. Two measures of reward were used, potentiation of rewarding brain stimulation and intravenous drug self-administration. In both measures, these genotypes differed dramatically in their response to morphine. Morphine potentiated rewarding brain stimulation in the C57 mice, however it appears to have antagonized rewarding stimulation in the DBA mice.

Consistent with these findings, intravenous morphine delivery did not serve as a positive reinforcer in DBA mice under conditions that were effective in the C57 mice. Lateral hypothalamic electrical stimulation is strongly rewarding Wise and Rompre Previous studies in our laboratory found dopamine D2 knockout wildtype C57 background and even subjects without dopamine D2 receptors readily learned the operant that leads to electrical stimulation of the lateral hypothalamus within one session Elmer et al.

An unexpected finding in the current study was that a significant number of the DBA mice, four out of ten, did not turn the wheel for lateral hypothalamic stimulation despite seemingly correct electrode placements. All four of the DBA mice that did not meet criteria never turned the wheel even though they would quickly orient to and approach the stimulus lights and often times contact the stimulus lights with their nose and mouth in the same manner as the C57 mice during experimenter delivered electrical stimulation.

In addition, the DBA mice that did learn the response were significantly delayed in reaching criteria 12 responses per min during the first four sessions compared to the C57 mice. All of the C57 mice learned to turn the wheel and reached criteria within the first session whereas the successful DBA mice on average took longer to reach the same criteria. Previous studies in inbred or selectively bred mouse or rat strains have generally either not found or not described differences in the rate of learning an operant for brain stimulation reward Cazala and Cardo ; Cazala et al.

The delay seen in the DBA mice is not the result of a general learning deficit since DBA mice learn to lever press water training prior to i. The delayed acquisition may reflect a low efficacy physiological stimulus frequency and current requirements were slightly higher in the DBAs that did acquire under the experimental conditions described in this report including operandum, brain region etc.

Since there is a significant difference in the constitution of the mesolimbic and mesocortical system between these two genotypes D'Este et al. The effects of morphine on brain stimulation reward in DBA and C57 mice were dramatically different. Morphine potentiated rewarding stimulation in the C57 mice, however it appears to have antagonized rewarding brain stimulation in the DBA mice.

Direct observation of the DBA mice during the session suggests that the antagonism was not due to response-limiting effects; the mice typically obtained several stimulations during the initial trials and moved around the cage during the session but showed no interest in the wheel during the remainder of the session.

The rightward shift appears to reflect a motivational or aversive component similar to elevations in brain stimulation reward thresholds produced by dopamine D2 receptor antagonists Benaliouad et al. Differential sensitivity in either or both of these systems may explain the rightward shift in the DBA mice. If the previously cited differences in kappa opioid system confer kappa agonist-like effect to morphine in DBA mice, morphine could elevate brain stimulation reward thresholds presumably by inhibiting dopamine neurons that project to the NAc Ford et al.

Another potential mechanism to explain the qualitative differences in morphine's effects is differential constitution or agonist activity at the dopamine D2 receptor. Morphine administration in dopamine D2 receptor knockout mice results in a similar rightward shift in the rate-frequency function Elmer et al. This rightward shift was hypothesized to occur as a result of depolarization block due to the combined effects of D2R autoreceptor deletion, morphine-induced disinhibition, and lateral hypothalamic stimulation Henry et al.

However, decreased D2R function is unlikely to be responsible for the rightward shift in the present study since the DBA mice have similar D2R B max and affinity as the C57 mice Hitzemann et al. Nevertheless, the previously mentioned differences in mesocorticolimbic dopamine system may interact uniquely with morphine to produce rightward shifts in the DBA mice.

Speculations concerning mechanism explanations should be tempered by the fact numerous genetic and neurochemical difference exist between these genotypes at baseline and following morphine administration Grice et al. The anomalous effects of morphine in the DBA mouse were also reflected in the IV morphine self-administration findings.

IV morphine delivery did not serve as a positive reinforcer in DBA mice under conditions that were effective in the C57 mice. Whereas DBA mice responded at the same low levels for IV saline and IV morphine, and did not alter their rate of responding when morphine doses were altered, C57 mice responded at increased rates for the low dose of morphine and at decreased rates for the high dose of morphine.

Thus the behavior of the C57 animals was under the pharmacological control of morphine whereas the behavior of the DBA animals was not. That the DBA animals were capable of responding more for morphine than saline was clear from their level of responding for water prior to the introduction of IV morphine reinforcement.

That they were not incapacitated by the morphine itself was clear from the fact that the same low rate of responding seen with IV saline was also seen with IV morphine. Thus morphine served effectively as a reinforcer in C57 mice, but served no more effectively than IV saline in DBA mice. The possibility exists that under different environmental circumstances, including a lower dose range, morphine may serve more effectively as a reinforcer in DBA mice has been shown with psychomotor stimulants Cabib et al.

However, preliminary data in our laboratory suggest that under the same conditions, lower doses are also no more effective than saline. Overall, the brain stimulation reward and IV drug self-administration studies demonstrate that the effects of morphine are qualitatively different between genotypes and suggest that morphine has greater addiction liability in the C57 mouse.

In contrast to the qualitatively different effects of morphine in C57 and DBA mice, amphetamine potentiated the rewarding effects of hypothalamic brain stimulation to a remarkably similar degree in the two strains.

The similarity is somewhat surprising given the significant differences in morphine potentiation of lateral hypothamic stimulation and the previously described differences in the mesocorticolimbic dopamine system D'Este et al. In addition, there are significant differences between the two genotypes in the neurochemical effects of amphetamine Ventura et al.

However, it is worth noting that previous studies using drug self-administration paradigms provide evidence to support equivalent reinforcement from stimulants cocaine between the DBA and C57 mice Grahame and Cunningham ; Rocha et al.

C57 and DBA mice play a prominent role in behavior genetic efforts designed to map gene loci associated with behavior and identify candidate genes involved in drug addiction. The success of the gene-mapping endeavor is equally dependent on the fidelity of the molecular and behavioral components of this research effort; false information in either component could result in spurious associations and pursuit of false candidate genes. The results of this study offer strong evidence that morphine is rewarding in the C57 genotype and not in the DBA genotype and provide a solid anchor for the behavioral phenotyping component of the gene-mapping endeavor.

Psychopharmacology Berl. Author manuscript; available in PMC Feb 1. Elmer , 1 J. Pieper , 2 L. Wise 2. Author information Copyright and License information Disclaimer. Correspondence: Greg Elmer, Ph. Copyright notice. The publisher's final edited version of this article is available at Psychopharmacology Berl. See other articles in PMC that cite the published article. Objectives The purpose of this study was to utilize classically accepted models of drug abuse liability to determine relative susceptibility to the rewarding effects of morphine.

Methods The ability of morphine or amphetamine to potentiate lateral hypothalamic brain stimulation and intravenous morphine self-administration across three doses in a Fixed Ratio schedule and highest dose in Progressive Ratio schedules was investigated in both genotypes. Conclusions These findings provide strong evidence that morphine is rewarding in the C57 genotype and not in the DBA genotype.

Keywords: Intravenous, self-administration, recombinant inbred strain, QTL, opioid, addiction, intracranial self-stimulation. Introduction Considerable evidence exists for a strong heritable component to opioid addiction Merikangas et al.

Apparatus Seven mouse operant conditioning chambers were used Coulbourn, Whitehall, Pennsylvania. Surgery Each subject was surgically prepared with an electrode implanted in the left lateral hypothalamus. Training Subjects were given one week to recover from surgery. Effects of morphine and amphetamine on BSR Brain Stimulation Reward Once responding in the rate-frequency paradigm became stable, the effects of morphine and amphetamine were assessed in each subject. Statistical analysis Three main dependent measures were used, the percent of animals reaching training criterion, the number of days required to reach criterion and the stimulation frequency required for half-maximal responding.

Procedure First, the mice were trained on a modified progressive ratio schedule for water reinforcement. Apparatus Ten mouse operant chambers were used. Water Training Naive subjects were water deprived for hr, then placed in the operant chamber. Surgery Following completion of the water training, subjects were surgically prepared with a catheter implanted in the jugular vein. Results Brain Stimulation Reward Data are reported for only those animals with electrode tips located in the lateral hypothalamic portion of the medial forebrain bundle Fig 1.

Open in a separate window. Fig 1. Training All of the C57 mice learned to manually turn the manipulandum when each quarter-turn was rewarded with a msec train of Hz lateral hypothalamic electrical stimulation. Fig 2. Fig 3. Fig 4. Effects of Amphetamine on BSR In contrast to morphine, amphetamine shifted the rate-frequency curves to the left Fig 4 and decreased M50 values Fig 5 equally in the two genotypes. Fig 5. Fig 6. Intravenous drug self-administration Water Training Each genotype was successfully trained to stable rates of lever pressing for water reinforcement Fig.

Fig 7. Discussion The goal of this study was to characterize the rewarding effects of morphine in the two genotypes most commonly used to map candidate gene loci associated with drug abuse, C57 and DBA. Further evidence for a quantitative trait locus on murine chromosome 10 controlling morphine preference in inbred mice.

Psychiatr Genet. Behavior genetic analysis of innate locomotor activity and acquisition of morphine self- administration behavior. Behavioural Pharmacology. Voluntary consumption of morphine in 15 inbred mouse strains. Psychopharmacology Berl ; —8. Life Sci.

Blockade of 5-HT2a receptors reduces haloperidol-induced attenuation of reward. A study of oral morphine preference in inbred mouse strains. Quantitative trait loci mapping of three loci controlling morphine preference using inbred mouse strains. Nat Genet. Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience.

Depressive-like effects of the kappa-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats. J Pharmacol Exp Ther. Intracranial self-stimulation ICSS in rodents to study the neurobiology of motivation. Nat Protoc. Hypothalamic self-stimulation and operant activity in the mottled mutant mouse. Brain Res Bull. Hypothalamic self-stimulation in three inbred strains of mice. Brain Res. Effects of the albino gene on self-stimulation behavior in the lateral hypothalamus in the mouse.

Physiol Behav. Genetic differences in the rewarding and activating effects of morphine and ethanol. Psychopharmacology Berl ; — Morphine-induced place conditioning in Fischer and Lewis rats: acquisition and dose-response in a fully biased procedure.

Pharmacol Biochem Behav. Sample size determination in step-down and step-up multiple tests for comparing treatments with a control. J Stat Plan Infer. Parametric analysis of brain stimulation reward in the rat: II. Temporal summation in the reward system. J Comp Physiol Psychol. Responding for brain stimulation reward in the bed nucleus of the stria terminalis in alcohol-preferring rats following alcohol and amphetamine pretreatments.

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