Modulation of methylphenidate effects on wheel running and acoustic startle by acute food deprivation in commercially and selectively bred rats

Behavioral effects of the same dose of the same drug can vary in degree and direction between and within individuals. The present study examines behavioral base rates, feeding status, and dispositional differences as sources of inter- and intra-individual heterogeneity in drug response. Modulation of the effects of methylphenidate (MPD) on wheel running and acoustic startle by food deprivation was examined in three experiments. Freely fed or food deprived Harlan Sprague-Dawley rats (running study) or rats selectively bred for low (LoS) and high (HiS) saccharin intake (running and startle studies) were given MPD (10 mg/kg) or saline before testing. Overall drug effects and predictors of drug response were assessed. MPD increased running and startle amplitude and disrupted prepulse inhibition; systematic variation among rats of these effects and their modulation by food deprivation was observed. Deprivation-induced running predicted MPD's effect in Harlan SD and LoS rats. Observation of this relationship among commercial rats suggests that acute deprivation sensitivity has utility as a noninvasive marker for drug responses. Its observation in rats selected on a taste phenotype with known correlates points to fruitful avenues of research on stimulant drugs' mechanisms, especially in dopaminergic pathways, and may be relevant to their clinical usage.

[1]  A. Cools,et al.  Differential effects of ketamine on gating of auditory evoked potentials and prepulse inhibition in rats , 1999, Psychopharmacology.

[2]  A. Swann,et al.  Psychostimulants given in adolescence modulate their effects in adulthood using the open field and the wheel-running assays , 2010, Brain Research Bulletin.

[3]  L. Rohde,et al.  Response to methylphenidate in children and adolescents with ADHD: does comorbid anxiety disorders matters? , 2009, Journal of Neural Transmission.

[4]  R. Tannock,et al.  An Exaggerated Cardiovascular Response to Methylphenidate in ADHD Children with Anxiety , 1995 .

[5]  T. Challman,et al.  Methylphenidate: its pharmacology and uses. , 2000, Mayo Clinic proceedings.

[6]  G. Di Chiara,et al.  Selective psychostimulant sensitization by food restriction: differential changes in accumbens shell and core dopamine , 2003, The European journal of neuroscience.

[7]  B. Yoburn,et al.  Pharmacology, Biochemistry and Behavior , 2012 .

[8]  N. Dess,et al.  Stress-induced attenuation of acoustic startle in low-saccharin-consuming rats , 2008, Biological Psychology.

[9]  N. Dess,et al.  Ingestional responses to metabolic challenges in rats selectively bred for high and low saccharin intake , 2002, Physiology & Behavior.

[10]  D. Stephens,et al.  Food-Induced Behavioral Sensitization, Its Cross-Sensitization to Cocaine and Morphine, Pharmacological Blockade, and Effect on Food Intake , 2006, The Journal of Neuroscience.

[11]  J. Melichar,et al.  Human Taste Thresholds Are Modulated by Serotonin and Noradrenaline , 2006, The Journal of Neuroscience.

[12]  J. Weedon,et al.  The multifaceted effects of oral administration of methylphenidate in juvenile rats: Anxiety, activity, and attention , 2010, European Neuropsychopharmacology.

[13]  C. Berridge,et al.  Both corticotropin-releasing factor and apomorphine reduce prepulse inhibition following repeated central infusion of corticotropin-releasing factor , 2006, Pharmacology Biochemistry and Behavior.

[14]  S. Kollins.  ADHD, Substance Use Disorders, and Psychostimulant Treatment , 2008, Journal of attention disorders.

[15]  R. Harris,et al.  Effects of stimulants, anorectics, and related drugs on schedule-controlled behavior , 2004, Psychopharmacology.

[16]  L. Reijmers,et al.  Acoustic prepulses can facilitate the startle reflex in rats: Discrepancy between rat and human data resolved , 1994, Brain Research Bulletin.

[17]  N. Dess,et al.  Taste and emotionality in rats selectively bred for high versus low saccharin intake , 1996 .

[18]  R. Tannock,et al.  Differential effects of methylphenidate on working memory in ADHD children with and without comorbid anxiety. , 1995, Journal of the American Academy of Child and Adolescent Psychiatry.

[19]  A. Hunter,et al.  Stressor controllability and learned helplessness research in the United States: Sensitization and fatigue processes , 2002, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[20]  Matthew A. Jarrett,et al.  A conceptual review of the comorbidity of attention-deficit/hyperactivity disorder and anxiety: implications for future research and practice. , 2008, Clinical psychology review.

[21]  N. Dess,et al.  Selective breeding for differential saccharin intake as an animal model of drug abuse , 2008, Behavioural pharmacology.

[22]  A. Chicz–DeMet,et al.  Caffeine taste test for panic disorder: Adenosine receptor supersensitivity , 1989, Psychiatry Research.

[23]  K. Taber,et al.  METHYLPHENIDATE (RITALIN): BEHAVIORAL STUDIES IN THE RAT , 2007, The International journal of neuroscience.

[24]  Huda Akil,et al.  Selective Breeding for Divergence in Novelty-seeking Traits: Heritability and Enrichment in Spontaneous Anxiety-related Behaviors , 2006, Behavior genetics.

[25]  M. Carroll,et al.  Higher locomotor response to cocaine in female (vs. male) rats selectively bred for high (HiS) and low (LoS) saccharin intake , 2007, Pharmacology Biochemistry and Behavior.

[26]  N. Swerdlow,et al.  Heritable strain differences in sensitivity to the startle gating-disruptive effects of D2 but not D3 receptor stimulation , 2008, Behavioural pharmacology.

[27]  G. Hanson,et al.  Methylphenidate-Induced Increases in Vesicular Dopamine Sequestration and Dopamine Release in the Striatum: The Role of Muscarinic and Dopamine D2 Receptors , 2008, Journal of Pharmacology and Experimental Therapeutics.

[28]  D. Bush,et al.  Individual differences in elevated plus-maze exploration predicted progressive-ratio cocaine self-administration break points in Wistar rats , 2007, Psychopharmacology.

[29]  L. E. Arnold,et al.  Methyiphenidate vs. amphetamine: Comparative review , 2000 .

[30]  L. Parsons,et al.  Neural basis for a heritable phenotype: differences in the effects of apomorphine on startle gating and ventral pallidal GABA efflux in male Sprague–Dawley and Long–Evans rats , 2009, Psychopharmacology.

[31]  Impulsivity on a Go/No-go task for intravenous cocaine or food in male and female rats selectively bred for high and low saccharin intake , 2008, Behavioural pharmacology.

[32]  R. Meisch,et al.  Food-deprivation increases cocaine-induced conditioned place preference and locomotor activity in rats , 1997, Psychopharmacology.

[33]  T. Davidson,et al.  Development of tolerance to endogenous opiates activated by 24-h food deprivation , 1992, Appetite.

[34]  B. Hamilton,et al.  An Empirical Investigation of the Effects of Heterogeneous Regression Slopes in Analysis of Covariance , 1977 .

[35]  L. Johnston,et al.  Monitoring the Future national survey results on drug use, 1975-2017: Volume I, secondary school students , 2005 .

[36]  M. Carroll,et al.  Wheel running as a predictor of cocaine self-administration and reinstatement in female rats , 2005, Pharmacology Biochemistry and Behavior.

[37]  H. Goez,et al.  Differential Stimulant Response on Attention in Children With Comorbid Anxiety and Oppositional Defiant Disorder , 2007, Journal of child neurology.

[38]  J. McGough,et al.  The pharmacogenomic era: promise for personalizing attention deficit hyperactivity disorder therapy. , 2008, Child and adolescent psychiatric clinics of North America.

[39]  N. Dess,et al.  Temporal Organization of Eating in Low- and High- Saccharin-Consuming Rats , 2007 .

[40]  A. Marriott.  The effects of amphetamine, caffeine and methylphenidate on the locomotor activity of rats in an unfamiliar environment. , 1968, International journal of neuropharmacology.

[41]  E. Cook,et al.  Dopamine Transporter Genotype and Methylphenidate Dose Response in Children with ADHD , 2005, Neuropsychopharmacology.

[42]  L. Johnston,et al.  Monitoring the Future national survey results on drug use, 1975-2018: Volume II, college students and adults ages 19-60 , 2005 .

[43]  J. H. Steiger.  Tests for comparing elements of a correlation matrix. , 1980 .

[44]  M. Paulus,et al.  An Insular View of Anxiety , 2006, Biological Psychiatry.

[45]  N. Swerdlow,et al.  Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. , 2000, Behavioural pharmacology.

[46]  N. Dess,et al.  Ethanol consumption in rats selectively bred for differential saccharin intake. , 1998, Alcohol.

[47]  N. Dess,et al.  Exploring Adaptations to Famine: Rats Selectively Bred for Differential Intake of Saccharin Differ on Deprivation-Induced Hyperactivity and Emotionality , 2000, International Journal of Comparative Psychology.

[48]  R. Tannock,et al.  Anxiety, Methylphenidate Response, and Working Memory in Children With ADHD , 2008, Journal of attention disorders.

[49]  N. Swerdlow,et al.  Strain differences in the disruption of prepulse inhibition of startle after systemic and intra-accumbens amphetamine administration , 2007, Pharmacology Biochemistry and Behavior.

[50]  L. Simpson.  A study of the interaction between amphetamine and food deprivation. , 1974, Psychopharmacologia.

[51]  K. D’anci,et al.  Dietary Modulation of the Behavioral Consequences of Psychoactive Drugs , 2005 .

[52]  S. Irwin,et al.  Individual differences. I. Correlation between control locomotor activity and sensitivity to stimulant and depressant drugs. , 1958, The Journal of pharmacology and experimental therapeutics.

[53]  L. Johnston,et al.  Monitoring the Future national survey results on drug use, 1975-2017: Volume II, college students and adults ages 19-55 , 2008 .

[54]  K. Carr.  Chronic food restriction: Enhancing effects on drug reward and striatal cell signaling , 2007, Physiology & Behavior.

[55]  M. Le Moal,et al.  Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. , 2000, Science.

[56]  J. Swanson,et al.  Adverse reactions to methylphenidate treatment for attention-deficit/hyperactivity disorder: structure and associations with clinical characteristics and symptom control. , 2009, Journal of child and adolescent psychopharmacology.

[57]  Barbara Tillmann,et al.  The feeling of familiarity of music and odors: the same neural signature? , 2007, Cerebral cortex.

[58]  D. S. Fokkema,et al.  Dose–response characteristics of ketamine effect on locomotion, cognitive function and central neuronal activity , 2006, Brain Research Bulletin.

[59]  Patrick M. O'Malley,et al.  Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2004. , 2003 .

[60]  N. Swerdlow,et al.  Toward Understanding the Biology of a Complex Phenotype: Rat Strain and Substrain Differences in the Sensorimotor Gating-Disruptive Effects of Dopamine Agonists , 2000, The Journal of Neuroscience.

[61]  K. Cosgrove,et al.  Wheel-running attenuates intravenous cocaine self-administration in rats Sex differences , 2002, Pharmacology Biochemistry and Behavior.

[62]  S. Lamarque,et al.  Spontaneous appetence for wheel-running: a model of dependency on physical activity in rat , 2006, European Psychiatry.

[63]  E. Cook,et al.  Affective individual differences and startle reflex modulation. , 1991, Journal of abnormal psychology.

[64]  P. Marinković,et al.  Behavioral and biochemical effects of various food-restriction regimens in the rats , 2007, Physiology & Behavior.

[65]  M. Monuteaux,et al.  Are Girls with ADHD at Risk for Eating Disorders? Results from a Controlled, Five-Year Prospective Study , 2007, Journal of developmental and behavioral pediatrics : JDBP.

[66]  A. Ettenberg,et al.  Runway self-administration of intracerebroventricular cocaine: evidence of mixed positive and negative drug actions , 2007, Behavioural pharmacology.

[67]  T. Belke,et al.  Responding for sucrose and wheel-running reinforcement: effect of D-amphetamine , 2005, Behavioural pharmacology.

[68]  K. Proulx,et al.  Comparisons of Behavioral and Neurochemical Characteristics between WKY, WKHA, and Wistar Rat Strains , 2002, Neuropsychopharmacology.

[69]  T. Garland,et al.  Differential sensitivity to acute administration of Ritalin, apormorphine, SCH 23390, but not raclopride in mice selectively bred for hyperactive wheel-running behavior , 2003, Psychopharmacology.

[70]  D. Feifel.  Individual differences in prepulse inhibition of startle as a measure of individual dopamine function. , 1999, Behavioral neuroscience.

[71]  Yan Li,et al.  Coexistence of Anhedonia and anxiety-independent increased novelty-seeking behavior in the chronic mild stress model of depression , 2010, Behavioural Processes.

[72]  M. Carroll,et al.  Impulsivity (delay discounting) for food and cocaine in male and female rats selectively bred for high and low saccharin intake , 2007, Pharmacology Biochemistry and Behavior.

[73]  M. J. Gill,et al.  The contribution of the central nucleus of the amygdala to individual differences in amphetamine-induced hyperactivity , 2009, Behavioural Brain Research.

[74]  J. Feldon,et al.  Apomorphine-Induced Prepulse Inhibition Disruption is Associated with a Paradoxical Enhancement of Prepulse Stimulus Reactivity , 2004, Neuropsychopharmacology.

[75]  L. Dwoskin,et al.  Age and sex differences in the locomotor effect of repeated methylphenidate in rats classified as high or low novelty responders , 2006, Psychopharmacology.

[76]  T. Belke,et al.  Effects of cocaine on fixed-interval responding reinforced by the opportunity to run. , 2001, Journal of the experimental analysis of behavior.

[77]  J. Kennedy,et al.  Dopamine Transporter Gene (DAT1) Associated with Appetite Suppression to Methylphenidate in a Case–Control Study of Binge Eating Disorder , 2007, Neuropsychopharmacology.

[78]  D. Coghill,et al.  Adverse Effects of Pharmacotherapies for Attention-Deficit Hyperactivity Disorder , 2008, CNS drugs.

[79]  G. Higgins,et al.  Differences between three rat strains in sensitivity to prepulse inhibition of an acoustic startle response: influence of apomorphine and phencyclidine pretreatment , 1994, Journal of psychopharmacology.

[80]  F. Dellu-Hagedorn,et al.  Dimensional Analysis of ADHD Subtypes in Rats , 2007, Biological Psychiatry.

[81]  N. Swerdlow,et al.  Sensitivity to the dopaminergic regulation of prepulse inhibition in rats: Evidence for genetic, but not environmental determinants , 2001, Pharmacology Biochemistry and Behavior.

[82]  C. Berridge.  Neural Substrates of Psychostimulant-Induced Arousal , 2006, Neuropsychopharmacology.

[83]  P. Quinn,et al.  Attention-deficit/hyperactivity disorder and its comorbidities in women and girls: An evolving picture , 2008, Current psychiatry reports.

[84]  G. Sandner,et al.  Relationship between PPI and baseline startle response , 2006, Cognitive Neurodynamics.

[85]  Q. Greba,et al.  Ventral tegmental area dopamine neurons mediate the shock sensitization of acoustic startle: a potential site of action for benzodiazepine anxiolytics. , 2002, Behavioral neuroscience.

[86]  M. Geyer,et al.  Parametric determinants in pre-stimulus modification of acoustic startle: interaction with ketamine , 2005, Psychopharmacology.

[87]  Martin H. Teicher,et al.  Rate dependency revisited: understanding the effects of methylphenidate in children with attention deficit hyperactivity disorder. , 2003, Journal of child and adolescent psychopharmacology.

[88]  Matthew A. Jarrett,et al.  Comorbidity as a predictor and moderator of treatment outcome in youth with anxiety, affective, attention deficit/hyperactivity disorder, and oppositional/conduct disorders. , 2008, Clinical psychology review.

[89]  R. Bevins,et al.  Individual differences in rats' reactivity to novelty and the unconditioned and conditioned locomotor effects of methamphetamine , 2004, Pharmacology Biochemistry and Behavior.

[90]  D. Amaral,et al.  Acoustic Startle Reflex in Rhesus Monkeys: A Review , 2008, Reviews in the neurosciences.

[91]  M. Bardo,et al.  Novelty seeking and drug use: contribution of an animal model. , 2005, Experimental and clinical psychopharmacology.

[92]  W. Mcbride,et al.  Amphetamine-modified acoustic startle responding and prepulse inhibition in adult and adolescent alcohol-preferring and -nonpreferring rats , 2003, Pharmacology Biochemistry and Behavior.

[93]  N. Dess,et al.  Ethanol withdrawal and proclivity are inversely related in rats selectively bred for differential saccharin intake. , 2005, Alcohol.

[94]  W. Pelham,et al.  The effects of methylphenidate on prepulse inhibition during attended and ignored prestimuli among boys with attention-deficit hyperactivity disorder , 2002, Psychopharmacology.

[95]  N. Swerdlow,et al.  A novel rat strain with enhanced sensitivity to the effects of dopamine agonists on startle gating , 2008, Pharmacology Biochemistry and Behavior.