Zebrafish models to study drug abuse-related phenotypes

Abstract Mounting evidence implicates the zebrafish (Danio rerio) as a promising model species for reward and addiction research. Modeling drug abuse-related behavior in both adult and larval zebrafish produced a wealth of clinically translatable data, also demonstrating their sensitivity to various drugs of abuse and the ability to develop tolerance. Several studies have also applied withdrawal paradigms to model the adverse effects of drug abuse in zebrafish. In this review, we summarize recent findings of a wide spectrum of zebrafish drug abuse-related behavioral and physiological phenotypes, discuss the existing challenges, and outline potential future directions of research in this field.

[1]  C. Migeon,et al.  Reaction of the Adrenal Cortex to Emotional Stress , 1956, Psychosomatic medicine.

[2]  Chemically altered permanent behavior patterns in fish and their cure by reserpine. , 1956, Science.

[3]  Interaction of serotonin and lysergic acid diethylamide in the Siamese fighting fish. , 1957, The Journal of pharmacology and experimental therapeutics.

[4]  J. Arbit Effects of LSD-25 upon Betta splendens: reliability of a bioassay technique. , 1957, Journal of applied physiology.

[5]  H. Owens,et al.  Effects of Lysergic Acid Diethylamide on Urinary 17-Ketosteroid and 17-OH Corticosteroid Levels of Female Rats , 1963, Nature.

[6]  A. M. Sackler,et al.  Metabolic and endocrine effects of lysergic acid diethylamide (LSD-25) on male rats. , 1966, The Journal of endocrinology.

[7]  R. Morfin,et al.  Blood-brain barrier for serotonin in the eel (Anguilla anguilla L.). , 1981, Comparative biochemistry and physiology. C: Comparative pharmacology.

[8]  P. Tyrer,et al.  Identification and management of benzodiazepine dependence. , 1984, Postgraduate medical journal.

[9]  H. Ashton Benzodiazepine withdrawal: an unfinished story. , 1984, British medical journal.

[10]  G. Barr,et al.  Place conditioning with morphine and phencyclidine: dose dependent effects. , 1985, Life sciences.

[11]  H. Anisman,et al.  Amphetamine withdrawal: a behavioral evaluation. , 1986, Life sciences.

[12]  F. Bloom,et al.  Opponent process theory of motivation: Neurobiological evidence from studies of opiate dependence , 1989, Neuroscience & Biobehavioral Reviews.

[13]  B. Leonard,et al.  Rodent models of alcoholism: a review. , 1989, Alcohol and alcoholism.

[14]  J. RicoIrles,et al.  [Alcohol withdrawal syndrome]. , 1990, Anales de medicina interna.

[15]  J. Brady Animal models for assessing drugs of abuse , 1991, Neuroscience & Biobehavioral Reviews.

[16]  R. Balster Drug abuse potential evaluation in animals. , 1991, British journal of addiction.

[17]  D. Braida,et al.  Dose-dependent conditioned place preference produced by etonitazene and morphine. , 1992, European journal of pharmacology.

[18]  J. Crabbe,et al.  Genetic animal models of alcohol and drug abuse. , 1994, Science.

[19]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  G. Bammer,et al.  Why? Who? How? Estimating numbers of illicit drug users: lessons from a case study from the Australian Capital Territory , 1996, Australian and New Zealand journal of public health.

[21]  J. Levine,et al.  Different Mechanisms Mediate Development and Expression of Tolerance and Dependence for Peripheral μ-Opioid Antinociception in Rat , 1997, The Journal of Neuroscience.

[22]  Khan,et al.  Role of serotonin in fish immunomodulation , 1997, The Journal of experimental biology.

[23]  R. Gerlai,et al.  Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects , 2000, Pharmacology Biochemistry and Behavior.

[24]  M. Farré,et al.  Pharmacology of MDMA in Humans , 2000, Annals of the New York Academy of Sciences.

[25]  H. Becker Animal Models of Alcohol Withdrawal , 2000, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[26]  M. Parmentier,et al.  Cocaine, but not morphine, induces conditioned place preference and sensitization to locomotor responses in CB1 knockout mice , 2000, The European journal of neuroscience.

[27]  S. R. Vorel,et al.  Relapse to Cocaine-Seeking After Hippocampal Theta Burst Stimulation , 2001, Science.

[28]  S. Chen,et al.  Altered sensitivity of CD81-deficient mice to neurobehavioral effects of cocaine. , 2001, Brain research. Molecular brain research.

[29]  S. Checkley,et al.  Salivary cortisol during opiate dependence and withdrawal , 2001, Addiction biology.

[30]  J. Melichar,et al.  Addiction and withdrawal--current views. , 2001, Current opinion in pharmacology.

[31]  John E. Dowling,et al.  Behavioral screening for cocaine sensitivity in mutagenized zebrafish , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Fendt,et al.  Anxiogenic-like effects of opiate withdrawal seen in the fear-potentiated startle test, an interdisciplinary probe for drug-related motivational states , 2001, Psychopharmacology.

[33]  J. Becker,et al.  The alcohol hangover. , 2001, Annals of internal medicine.

[34]  M. Wullimann,et al.  Development of the catecholaminergic system in the early zebrafish brain: an immunohistochemical study. , 2002, Brain research. Developmental brain research.

[35]  Richard A Rabin,et al.  Ethanol effects on three strains of zebrafish: model system for genetic investigations , 2003, Pharmacology Biochemistry and Behavior.

[36]  Mark A. Smith,et al.  Sensitivity to the effects of opioids in rats with free access to exercise wheels: µ-opioid tolerance and physical dependence , 2003, Psychopharmacology.

[37]  G. Aston-Jones,et al.  Enhanced Morphine Preference Following Prolonged Abstinence: Association with Increased Fos Expression in the Extended Amygdala , 2003, Neuropsychopharmacology.

[38]  P. Stoddard,et al.  Serotonin modulates the electric waveform of the gymnotiform electric fish Brachyhypopomus pinnicaudatus , 2003, Journal of Experimental Biology.

[39]  J. Gewirtz,et al.  Elevated startle during withdrawal from acute morphine: a model of opiate withdrawal and anxiety , 2003, Psychopharmacology.

[40]  R. Drake,et al.  Benzodiazepine use and abuse among patients with severe mental illness and co-occurring substance use disorders. , 2003, Psychiatric services.

[41]  U. Banerjee Acquisition of conditioned avoidance response in rats under the influence of addicting drugs , 2004, Psychopharmacologia.

[42]  M. Stein,et al.  Does a U-shaped relationship exist between alcohol use and DSM-III-R mood and anxiety disorders? , 2004, Journal of affective disorders.

[43]  M. Carvan,et al.  Strain-dependent effects of developmental ethanol exposure in zebrafish. , 2004, Neurotoxicology and teratology.

[44]  E. Levin,et al.  Nicotinic involvement in memory function in zebrafish. , 2004, Neurotoxicology and teratology.

[45]  T. Eisenstein,et al.  Neurological basis of drug dependence and its effects on the immune system , 2004, Journal of Neuroimmunology.

[46]  Joseph A Banken,et al.  Drug Abuse Trends among Youth in the United States , 2004, Annals of the New York Academy of Sciences.

[47]  P. Rogers,et al.  Effects of caffeine and caffeine withdrawal on mood and cognitive performance degraded by sleep restriction , 2005, Psychopharmacology.

[48]  R. Chessick,et al.  Effect of pretreatment with tryptamine, tryptophan and DOPA on LSD reaction in tropical fish , 1964, Psychopharmacologia.

[49]  Kayta Kobayashi,et al.  Acute effects of alcohol on larval zebrafish: a genetic system for large-scale screening , 2004, Pharmacology Biochemistry and Behavior.

[50]  B. Thisse,et al.  Evolution and expression of D2 and D3 dopamine receptor genes in zebrafish , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[51]  G. Hulse,et al.  Benzodiazepine dependence , 2004, Australian family physician.

[52]  S. Crowe,et al.  Persistence of cognitive effects after withdrawal from long-term benzodiazepine use: a meta-analysis. , 2004, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[53]  R. Sinha,et al.  Gender differences in cardiovascular and corticoadrenal response to stress and drug cues in cocaine dependent individuals , 2006, Psychopharmacology.

[54]  E. Dyck Flashback: Psychiatric Experimentation with LSD in Historical Perspective , 2005, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[55]  D. Beversdorf,et al.  Cognitive Impairment in Acute Cocaine Withdrawal , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[56]  O1 PREVIOUS EXPERIENCE OF ETHANOL WITHDRAWAL REDUCES WITHDRAWAL-INDUCED ANXIETY AND ELEVATIONS IN PLASMA CORTICOSTERONE, BUT INCREASES WITHDRAWAL-INDUCED C-FOS EXPRESSION IN LIMBIC AREAS , 2005 .

[57]  L. Zon,et al.  In vivo drug discovery in the zebrafish , 2005, Nature Reviews Drug Discovery.

[58]  K. Miczek,et al.  Automatic quantification of withdrawal from 5-day diazepam in rats: ultrasonic distress vocalizations and hyperreflexia to acoustic startle stimuli , 2005, Psychopharmacology.

[59]  S. B. Caine,et al.  Animal models of drug craving , 2005, Psychopharmacology.

[60]  A. Rubinstein,et al.  Zebrafish assays for drug toxicity screening , 2006, Expert opinion on drug metabolism & toxicology.

[61]  R. Kivisaari,et al.  Cognitive function during early abstinence from opioid dependence: a comparison to age, gender, and verbal intelligence matched controls , 2006, BMC psychiatry.

[62]  Rachel Blaser,et al.  Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio) , 2006, Pharmacology Biochemistry and Behavior.

[63]  Laure Bally-Cuif,et al.  The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse. , 2006, Methods.

[64]  E. Caldiroli,et al.  Relationship Between Plasma Cortisol Levels, Withdrawal Symptoms and Craving in Abstinent and Treated Heroin Addicts , 2006, Journal of addictive diseases.

[65]  D. Braida,et al.  Hallucinatory and rewarding effect of salvinorin A in zebrafish: κ-opioid and CB1-cannabinoid receptor involvement , 2007, Psychopharmacology.

[66]  B. Lau,et al.  Dissociation of food and opiate preference by a genetic mutation in zebrafish , 2006, Genes, brain, and behavior.

[67]  H. Yoshioka,et al.  Characterization and expression of serotonin transporter genes in zebrafish. , 2006, The Tohoku journal of experimental medicine.

[68]  S. Neuhauss,et al.  Genetic identification of AChE as a positive modulator of addiction to the psychostimulant D-amphetamine in zebrafish. , 2006, Journal of neurobiology.

[69]  Assessing stress in zebrafish: Anxiolytic effects of nicotine , 2006 .

[70]  R. Sircar,et al.  Repeated ethanol treatment in adolescent rats alters cortical NMDA receptor. , 2006, Alcohol.

[71]  H. Spaink,et al.  Genetic and transcriptome characterization of model zebrafish cell lines. , 2006, Zebrafish.

[72]  S. Friedman,et al.  Estimates of injecting drug users at the national and local level in developing and transitional countries, and gender and age distribution , 2006, Sexually Transmitted Infections.

[73]  Edward D. Levin,et al.  Anxiolytic effects of nicotine in zebrafish , 2007, Physiology & Behavior.

[74]  H. Krishnan,et al.  Drug-Induced Epigenetic Changes Produce Drug Tolerance , 2007, PLoS biology.

[75]  D. Dietz,et al.  Corticosterone fails to produce conditioned place preference or conditioned place aversion in rats , 2007, Behavioural Brain Research.

[76]  B. Lockwood,et al.  A choice behavior for morphine reveals experience-dependent drug preference and underlying neural substrates in developing larval zebrafish , 2007, Neuroscience.

[77]  V. Connaughton,et al.  Effects of nicotine on growth and development in larval zebrafish. , 2007, Zebrafish.

[78]  S. Friedman,et al.  Estimating the Prevalence of Injection Drug Users in the U.S. and in Large U.S. Metropolitan Areas from 1992 to 2002 , 2008, Journal of Urban Health.

[79]  Klaus-Peter Lesch,et al.  3,4-Methylenedioxymethamphetamine Self-Administration is Abolished in Serotonin Transporter Knockout Mice , 2007, Biological Psychiatry.

[80]  Caroline H. Brennan,et al.  Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways , 2008, Journal of Experimental Biology.

[81]  Yi-lang Tang,et al.  Dysfunction of the Hypothalamic–Pituitary–Adrenal Axis in Opioid Dependent Subjects: Effects of Acute and Protracted Abstinence , 2008, The American journal of drug and alcohol abuse.

[82]  H. Müller,et al.  Characterisation of the zebrafish serotonin transporter functionally links TM10 to the ligand binding site , 2008, Journal of neurochemistry.

[83]  W. Alderton,et al.  Zebrafish: An in vivo model for the study of neurological diseases , 2008, Neuropsychiatric disease and treatment.

[84]  Edward W Boyer,et al.  Clinical Toxicology , 2018 .

[85]  J. Nagy Alcohol Related Changes in Regulation of NMDA Receptor Functions , 2008, Current neuropharmacology.

[86]  J. C. Winter,et al.  Marked decrease of LSD-induced stimulus control in serotonin transporter knockout mice , 2008, Pharmacology Biochemistry and Behavior.

[87]  Ceri E. Van Slyke,et al.  The Zebrafish Information Network: the zebrafish model organism database provides expanded support for genotypes and phenotypes , 2007, Nucleic Acids Res..

[88]  D. Overstreet,et al.  Withdrawal emotional-regulation in infant rats from genetic animal models of depression , 2008, Behavioural Brain Research.

[89]  J. Moreau,et al.  Trace Amine-Associated Receptor 1 Modulates Dopaminergic Activity , 2008, Journal of Pharmacology and Experimental Therapeutics.

[90]  A. Roach,et al.  Non-Associative Learning in Larval Zebrafish , 2008, Neuropsychopharmacology.

[91]  P. Bria,et al.  Treatment: Withdrawal Syndrome Alcohol Protracted Withdrawal Syndrome: The Role of Anhedonia , 2008 .

[92]  G. Lieschke,et al.  Manipulation of gene expression during zebrafish embryonic development using transient approaches. , 2008, Methods in molecular biology.

[93]  M. Brandão,et al.  Analysis of the chronic intake of and withdrawal from diazepam on emotional reactivity and sensory information processing in rats , 2008, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[94]  D. Epstein,et al.  Serum Cortisol Secretion During Heroin Abstinence Is Elevated Only Nocturnally , 2008, The American journal of drug and alcohol abuse.

[95]  Sonal R. Prajapati,et al.  Differences in acute alcohol-induced behavioral responses among zebrafish populations. , 2008, Alcoholism, clinical and experimental research.

[96]  C. Lüscher,et al.  Absence and Rescue of Morphine Withdrawal in GIRK/Kir3 Knock-out Mice , 2008, The Journal of Neuroscience.

[97]  E. Gouzoulis-Mayfrank [Dual diagnosis psychosis and substance use disorders: theoretical foundations and treatment]. , 2008, Zeitschrift fur Kinder- und Jugendpsychiatrie und Psychotherapie.

[98]  M. Tavares,et al.  Hormonal, Neurochemical, and Behavioral Response to a Forced Swim Test in Adolescent Rats throughout Cocaine Withdrawal , 2008, Annals of the New York Academy of Sciences.

[99]  N. Mirza,et al.  Strain- and model-dependent effects of chlordiazepoxide, L-838,417 and zolpidem on anxiety-like behaviours in laboratory mice , 2008, Pharmacology Biochemistry and Behavior.

[100]  H. Emrich,et al.  The Pharmacology of Lysergic Acid Diethylamide: A Review , 2008, CNS neuroscience & therapeutics.

[101]  L. Bally-Cuif,et al.  Comparative analysis of serotonin receptor (HTR1A/HTR1B families) and transporter (slc6a4a/b) gene expression in the zebrafish brain , 2008, The Journal of comparative neurology.

[102]  J. Jentsch Impulsivity in Animal Models for Drug Abuse Disorders. , 2008, Drug discovery today. Disease models.

[103]  I. Zhdanova,et al.  Gender differences in zebrafish responses to cocaine withdrawal , 2008, Physiology & Behavior.

[104]  A. Arner,et al.  Structure and Function of Skeletal Muscle in Zebrafish Early Larvae , 2008, The Journal of general physiology.

[105]  Howard Cabral,et al.  Anxiogenic effects of cocaine withdrawal in zebrafish , 2008, Physiology & Behavior.

[106]  M. Geyer,et al.  Spontaneous Nicotine Withdrawal Potentiates the Effects of Stress in Rats , 2008, Neuropsychopharmacology.

[107]  M. Haney,et al.  Actions of delta-9-tetrahydrocannabinol in cannabis: Relation to use, abuse, dependence , 2009, International review of psychiatry.

[108]  M. Miles,et al.  Characterization of pharmacological and behavioral differences to nicotine in C57Bl/6 and DBA/2 mice , 2009, Neuropharmacology.

[109]  W. Solecki,et al.  Motivational effects of opiates in conditioned place preference and aversion paradigm—a study in three inbred strains of mice , 2009, Psychopharmacology.

[110]  W. Koek,et al.  Precipitated and conditioned withdrawal in morphine-treated rats , 2010, Psychopharmacology.

[111]  A. Mesripour,et al.  Increase in brain corticosterone concentration and recognition memory impairment following morphine withdrawal in mice , 2009, Stress.

[112]  E. Levin,et al.  Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety , 2009, Pharmacology Biochemistry and Behavior.

[113]  Chris Cruickshank,et al.  A review of the clinical pharmacology of methamphetamine. , 2009, Addiction.

[114]  Marcus Zulian Teixeira Antidepressants, suicidality and rebound effect: evidence of similitude? , 2009, Homeopathy.

[115]  A. Adan,et al.  Alcohol hangover: a critical review of explanatory factors , 2009, Human psychopharmacology.

[116]  Stuart C. Sealfon,et al.  Psychedelics and schizophrenia , 2009, Trends in Neurosciences.

[117]  W. Ling,et al.  Treatment for amphetamine withdrawal. , 2009, The Cochrane database of systematic reviews.

[118]  J. Crabbe,et al.  Sex differences in acute ethanol withdrawal severity after adrenalectomy and gonadectomy in Withdrawal Seizure-Prone and Withdrawal Seizure-Resistant mice. , 2009, Alcohol.

[119]  J. Parsons,et al.  Club Drug Use and Dependence among Young Adults Recruited through Time-Space Sampling , 2009, Public health reports.

[120]  C. Blanco,et al.  Social anxiety disorder and alcohol use disorder co-morbidity in the National Epidemiologic Survey on Alcohol and Related Conditions , 2009, Psychological Medicine.

[121]  George R. Uhl,et al.  Dramatically Decreased Cocaine Self-Administration in Dopamine But Not Serotonin Transporter Knock-Out Mice , 2009, The Journal of Neuroscience.

[122]  R. Brooner,et al.  The construct and measurement equivalence of cocaine and opioid dependences: a National Drug Abuse Treatment Clinical Trials Network (CTN) study. , 2009, Drug and alcohol dependence.

[123]  Robbert Creton,et al.  Automated analysis of behavior in zebrafish larvae , 2009, Behavioural Brain Research.

[124]  M. Nosten-Bertrand,et al.  Evidence of long-term expression of behavioral sensitization to both cocaine and ethanol in dopamine transporter knockout mice , 2009, Psychopharmacology.

[125]  H. Alaei,et al.  Forced exercise improves passive avoidance memory in morphine-exposed rats. , 2009, Pakistan journal of biological sciences : PJBS.

[126]  R. Gerlai,et al.  Acute and chronic alcohol dose: population differences in behavior and neurochemistry of zebrafish , 2009, Genes, brain, and behavior.

[127]  Allan V. Kalueff,et al.  Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish , 2009, Behavioural Brain Research.

[128]  R. Sinha,et al.  Elevated cortisol and learning and memory deficits in cocaine dependent individuals: Relationship to relapse outcomes , 2009, Psychoneuroendocrinology.

[129]  Carsten Marr,et al.  Zebrafish reward mutants reveal novel transcripts mediating the behavioral effects of amphetamine , 2009, Genome Biology.

[130]  A. Parrott,et al.  Cortisol and 3,4-Methylenedioxymethamphetamine: Neurohormonal Aspects of Bioenergetic Stress in Ecstasy Users , 2009, Neuropsychobiology.

[131]  M. Prendergast,et al.  Sex differences in caffeine neurotoxicity following chronic ethanol exposure and withdrawal. , 2009, Alcohol and alcoholism.

[132]  Jie Shi,et al.  Time-Dependent Neuroendocrine Alterations and Drug Craving during the First Month of Abstinence in Heroin Addicts , 2009, The American journal of drug and alcohol abuse.

[133]  S. Shiffman,et al.  Tobacco dependence and withdrawal: science base, challenges and opportunities for pharmacotherapy. , 2009, Pharmacology & therapeutics.

[134]  [Zebrafish--useful model for pharmacodynamics and toxicity screening of traditional Chinese medicine]. , 2009, Zhongguo Zhong yao za zhi = Zhongguo zhongyao zazhi = China journal of Chinese materia medica.

[135]  R. Ali,et al.  Opioid antagonists with minimal sedation for opioid withdrawal. , 2009, The Cochrane database of systematic reviews.

[136]  Jennifer K. Bando,et al.  Sex differences in ethanol-induced hypothermia in ethanol-naïve and ethanol-dependent/withdrawn rats. , 2009, Alcoholism, clinical and experimental research.

[137]  R C MacPhail,et al.  Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. , 2010, Neurotoxicology and teratology.

[138]  Siddharth Gaikwad,et al.  Modeling withdrawal syndrome in zebrafish , 2010, Behavioural Brain Research.

[139]  P. Popik,et al.  Human opiorphin: The lack of physiological dependence, tolerance to antinociceptive effects and abuse liability in laboratory mice , 2010, Behavioural Brain Research.

[140]  S. Haggarty,et al.  Zebrafish Behavioral Profiling Links Drugs to Biological Targets and Rest/Wake Regulation , 2010, Science.

[141]  J. Roberts,et al.  Alcohol Levels Do Not Accurately Predict Physical or Mental Impairment in Ethanol-Tolerant Subjects: Relevance to Emergency Medicine and Dram Shop Laws , 2010, Journal of Medical Toxicology.

[142]  D. Tibboel,et al.  Weaning of opioids and benzodiazepines at home after critical illness in infants: a cost-effective approach. , 2010, Journal of opioid management.

[143]  S. A. Marshall,et al.  Similar withdrawal severity in adolescents and adults in a rat model of alcohol dependence. , 2010, Alcohol.

[144]  J. Kennedy,et al.  Cocaine and amphetamine regulated transcript (CART) gene in the comorbidity of schizophrenia with alcohol use disorders and nicotine dependence , 2010, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[145]  A. Swann The strong relationship between bipolar and substance‐use disorder , 2010, Annals of the New York Academy of Sciences.

[146]  R. Bevins,et al.  Competition between novelty and cocaine conditioned reward is sensitive to drug dose and retention interval. , 2010, Behavioral neuroscience.

[147]  Christina N. Toms,et al.  Does Acute Alcohol Exposure Modulate Aggressive Behaviors in the Zebrafish ( Danio rerio ), or is the Bark Worse than the Bite? , 2010 .

[148]  A. Santucci,et al.  Anxiety-like responses in adolescent rats following a 10–11-day withdrawal period from repeated cocaine administration , 2010, Brain Research Bulletin.

[149]  Wolfgang Driever,et al.  Genetic dissection of dopaminergic and noradrenergic contributions to catecholaminergic tracts in early larval zebrafish , 2009, The Journal of comparative neurology.

[150]  Siddharth Gaikwad,et al.  Characterization of behavioral and endocrine effects of LSD on zebrafish , 2010, Behavioural Brain Research.

[151]  Ngoc Kim Nhung Nguyen,et al.  Zebrafish Behavior in Novel Environments: Effects of Acute Exposure to Anxiolytic Compounds and Choice of Danio rerio Line. , 2010, International journal of comparative psychology.

[152]  Siddharth Gaikwad,et al.  The Developing Utility of Zebrafish in Modeling Neurobehavioral Disorders , 2010, International Journal of Comparative Psychology.

[153]  S. Rawls,et al.  β-Lactam antibiotic inhibits development of morphine physical dependence in rats , 2010, Behavioural pharmacology.

[154]  L. Amato,et al.  Anticonvulsants for alcohol withdrawal. , 2010, The Cochrane database of systematic reviews.

[155]  S. Neuhauss,et al.  Behavioral Neurobiology: How Larval Fish Orient towards the Light , 2010, Current Biology.

[156]  M. Sayette,et al.  Differences in negative mood-induced smoking reinforcement due to distress tolerance, anxiety sensitivity, and depression history , 2010, Psychopharmacology.

[157]  P. Bhutada,et al.  Inhibitory influence of mecamylamine on ethanol withdrawal-induced symptoms in C57BL/6J mice , 2010, Behavioural pharmacology.

[158]  J. Crabbe,et al.  REVIEW: Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked? , 2010, Addiction biology.

[159]  Ensuring integrated treatment for people with mental health and substance use problems. , 2010, Nursing times.

[160]  W. Carlezon,et al.  Diazepam and cocaine potentiate brain stimulation reward in C57BL/6J mice , 2010, Behavioural Brain Research.

[161]  J. Rehm,et al.  Anxiety and Mood Disorders and Cannabis Use , 2010, The American journal of drug and alcohol abuse.

[162]  Mark D. Morrissey,et al.  Individual differences in activity predict locomotor activity and conditioned place preference to amphetamine in both adolescent and adult rats , 2010, Pharmacology Biochemistry and Behavior.

[163]  Siddharth Gaikwad,et al.  Analyzing habituation responses to novelty in zebrafish (Danio rerio) , 2010, Behavioural Brain Research.

[164]  J. Levine,et al.  Shared Mechanisms for Opioid Tolerance and a Transition to Chronic Pain , 2010, The Journal of Neuroscience.

[165]  A. Kalueff,et al.  Domain interplay in mice and men: New possibilities for the “natural kinds” theory of emotion , 2011 .

[166]  M. Miguéns,et al.  Strain differences in the dose–response relationship for morphine self-administration and impulsive choice between Lewis and Fischer 344 rats , 2011, Journal of psychopharmacology.

[167]  Structure and Function of Skeletal Muscle in Zebrafi sh Early Larvae , .