Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder

Leffa, Douglas T.; Ferreira, Samira G.; Machado, Nuno J.; Souza, Carolina M.; Rosa, Fernanda da; de Carvalho, Cristiane; Kincheski, Grasielle C.; Takahashi, Reinaldo N.; Porciúncula, Lisiane O.; Souza, Diogo O.; Cunha, Rodrigo A.; Pandolfo, Pablo

doi:10.1111/ejn.14348

Title: Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder

Abstract

Abstract Attention deficit and hyperactivity disorder ( ADHD ) is characterized by impaired levels of hyperactivity, impulsivity, and inattention. Adenosine and endocannabinoid systems tightly interact in the modulation of dopamine signaling, involved in the neurobiology of ADHD . In this study, we evaluated the modulating effects of the cannabinoid and adenosine systems in a tolerance to delay of reward task using the most widely used animal model of ADHD . Spontaneous Hypertensive Rats ( SHR ) and Wistar–Kyoto rats were treated chronically or acutely with caffeine, a non‐selective adenosine receptor antagonist, or acutely with a cannabinoid agonist ( WIN 55212‐2, WIN ) or antagonist ( AM 251). Subsequently, animals were tested in the tolerance to delay of reward task, in which they had to choose between a small, but immediate, or a large, but delayed, reward. Treatment with WIN decreased, whereas treatment with AM 251 increased the choices of the large reward, selectively in SHR rats, indicating a CB ₁ receptor‐mediated increase in impulsive behavior. An acute pre‐treatment with caffeine blocked WIN effects. Conversely, a chronic treatment with caffeine increased the impulsive phenotype and potentiated the WIN effects. The results indicate that both cannabinoid and adenosine receptors modulate impulsive behaviormore »« less

Authors:

Leffa, Douglas T. ^[1]; Ferreira, Samira G. ^[2]; Machado, Nuno J. ^[2]; Souza, Carolina M. ^[2]; Rosa, Fernanda da ^[2]; de Carvalho, Cristiane ^[3]; Kincheski, Grasielle C. ^[4]; Takahashi, Reinaldo N. ^[3]; Porciúncula, Lisiane O. ^[1]; Souza, Diogo O. ^[1]; Cunha, Rodrigo A. ^[5]; Pandolfo, Pablo ^[6]

Department of Biochemistry Universidade Federal do Rio Grande do Sul Porto Alegre Brazil
CNC‐Center for Neuroscience and Cell Biology University of Coimbra Coimbra Portugal
Department of Pharmacology Universidade Federal de Santa Catarina Florianópolis Brazil
Institute of Medical Biochemistry Leopoldo de Meis Universidade Federal do Rio de Janeiro Rio de Janeiro Brazil
CNC‐Center for Neuroscience and Cell Biology University of Coimbra Coimbra Portugal, Faculty of Medicine University of Coimbra Coimbra Portugal
Department of Neurobiology Universidade Federal Fluminense Niterói Brazil

Publication Date:: Fri Feb 08 00:00:00 EST 2019

Sponsoring Org.:: USDOE

OSTI Identifier:: 1494158

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: European Journal of Neuroscience

Additional Journal Information:: Journal Name: European Journal of Neuroscience Journal Volume: 49 Journal Issue: 12; Journal ID: ISSN 0953-816X

Publisher:: Wiley-Blackwell

Country of Publication:: Country unknown/Code not available

Language:: English

Citation Formats


                    Leffa, Douglas T., Ferreira, Samira G., Machado, Nuno J., Souza, Carolina M., Rosa, Fernanda da, de Carvalho, Cristiane, Kincheski, Grasielle C., Takahashi, Reinaldo N., Porciúncula, Lisiane O., Souza, Diogo O., Cunha, Rodrigo A., and Pandolfo, Pablo. Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder.  Country unknown/Code not available: N. p., 2019. 
Web.  doi:10.1111/ejn.14348.

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                    Leffa, Douglas T., Ferreira, Samira G., Machado, Nuno J., Souza, Carolina M., Rosa, Fernanda da, de Carvalho, Cristiane, Kincheski, Grasielle C., Takahashi, Reinaldo N., Porciúncula, Lisiane O., Souza, Diogo O., Cunha, Rodrigo A., & Pandolfo, Pablo. Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder.  Country unknown/Code not available.  https://doi.org/10.1111/ejn.14348

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                    Leffa, Douglas T., Ferreira, Samira G., Machado, Nuno J., Souza, Carolina M., Rosa, Fernanda da, de Carvalho, Cristiane, Kincheski, Grasielle C., Takahashi, Reinaldo N., Porciúncula, Lisiane O., Souza, Diogo O., Cunha, Rodrigo A., and Pandolfo, Pablo. Fri .  
"Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder".  Country unknown/Code not available.  https://doi.org/10.1111/ejn.14348.

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@article{osti_1494158,

  title        = {Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder},

  author       = {Leffa, Douglas T. and Ferreira, Samira G. and Machado, Nuno J. and Souza, Carolina M. and Rosa, Fernanda da and de Carvalho, Cristiane and Kincheski, Grasielle C. and Takahashi, Reinaldo N. and Porciúncula, Lisiane O. and Souza, Diogo O. and Cunha, Rodrigo A. and Pandolfo, Pablo},

  abstractNote = {Abstract Attention deficit and hyperactivity disorder ( ADHD ) is characterized by impaired levels of hyperactivity, impulsivity, and inattention. Adenosine and endocannabinoid systems tightly interact in the modulation of dopamine signaling, involved in the neurobiology of ADHD . In this study, we evaluated the modulating effects of the cannabinoid and adenosine systems in a tolerance to delay of reward task using the most widely used animal model of ADHD . Spontaneous Hypertensive Rats ( SHR ) and Wistar–Kyoto rats were treated chronically or acutely with caffeine, a non‐selective adenosine receptor antagonist, or acutely with a cannabinoid agonist ( WIN 55212‐2, WIN ) or antagonist ( AM 251). Subsequently, animals were tested in the tolerance to delay of reward task, in which they had to choose between a small, but immediate, or a large, but delayed, reward. Treatment with WIN decreased, whereas treatment with AM 251 increased the choices of the large reward, selectively in SHR rats, indicating a CB 1 receptor‐mediated increase in impulsive behavior. An acute pre‐treatment with caffeine blocked WIN effects. Conversely, a chronic treatment with caffeine increased the impulsive phenotype and potentiated the WIN effects. The results indicate that both cannabinoid and adenosine receptors modulate impulsive behavior in SHR : the antagonism of cannabinoid receptors might be effective in reducing impulsive symptoms present in ADHD ; in addition, caffeine showed the opposite effects on impulsive behavior depending on the length of treatment. These observations are of particular importance to consider when therapeutic manipulation of CB 1 receptors is applied to ADHD patients who consume coffee.},

  doi          = {10.1111/ejn.14348},

  journal      = {European Journal of Neuroscience},

  number       = 12,

  volume       = 49,

  place        = {Country unknown/Code not available},

  year         = {Fri Feb 08 00:00:00 EST 2019},

  month        = {Fri Feb 08 00:00:00 EST 2019}

}

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Endocannabinoids (eCBs) modulate neurotransmission by inhibiting the release of a variety of neurotransmitters. The cannabinoid receptor agonist WIN 55.212-2 (WIN) can modulate organophosphorus (OP) anticholinesterase toxicity in rats, presumably by inhibiting acetylcholine (ACh) release. Some OP anticholinesterases also inhibit eCB-degrading enzymes. We studied the effects of the OP insecticide chlorpyrifos (CPF) on cholinergic signs of toxicity, cholinesterase activity and ACh release in tissues from wild type (+/+) and cannabinoid CB1 receptor knockout (-/-) mice. Mice of both genotypes (n = 5-6/treatment group) were challenged with CPF (300 mg/kg, 2 ml/kg in peanut oil, sc) and evaluated for functional and neurochemicalmore »« less
https://doi.org/10.1016/J.TAAP.2011.05.018
Role of adenosine A{sub 2A} receptor signaling in the nicotine-evoked attenuation of reflex cardiac sympathetic control

Journal Article El-Mas, Mahmoud M., E-mail: mahelm@hotmail.com ; El-gowilly, Sahar M ; Fouda, Mohamed A ; ... - Toxicology and Applied Pharmacology

Baroreflex dysfunction contributes to increased cardiovascular risk in cigarette smokers. Given the importance of adenosinergic pathways in baroreflex control, the hypothesis was tested that defective central adenosinergic modulation of cardiac autonomic activity mediates the nicotine-baroreflex interaction. Baroreflex curves relating changes in heart rate (HR) to increases or decreases in blood pressure (BP) evoked by i.v. doses (1-16 {mu}g/kg) of phenylephrine (PE) and sodium nitroprusside (SNP), respectively, were constructed in conscious rats; slopes of the curves were taken as measures of baroreflex sensitivity (BRS). Nicotine (25 and 100 {mu}g/kg i.v.) dose-dependently reduced BRS{sub SNP} in contrast to no effect on BRS{submore »« less
https://doi.org/10.1016/j.taap.2011.04.014
Evaluating Dopamine Reward Pathway in ADHD; clinical implications

Journal Article Volkow, N D ; Wang, G ; Volkow, N D ; ... - JAMA, Journal of the American Medical Association

Attention-deficit/hyperactivity disorder (ADHD) - characterized by symptoms of inattention and hyperactivity-impulsivity - is the most prevalent childhood psychiatric disorder that frequently persists into adulthood, and there is increasing evidence of reward-motivation deficits in this disorder. To evaluate biological bases that might underlie a reward/motivation deficit by imaging key components of the brain dopamine reward pathway (mesoaccumbens). We used positron emission tomography to measure dopamine synaptic markers (transporters and D{sub 2}/D{sub 3} receptors) in 53 nonmedicated adults with ADHD and 44 healthy controls between 2001-2009 at Brookhaven National Laboratory. We measured specific binding of positron emission tomographic radioligands for dopamine transportersmore »« less
https://doi.org/10.1001/jama.2009.1308

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Title: Caffeine and cannabinoid receptors modulate impulsive behavior in an animal model of attentional deficit and hyperactivity disorder

Abstract

Citation Formats

Regulation of endocannabinoid signaling by stress: Implications for stress-related affective disorders journal, August 2008

Differential glutamate-dependent and glutamate-independent adenosine A 1 receptor-mediated modulation of dopamine release in different striatal compartments journal, April 2007

Ostracising caffeine from the pharmacological arsenal for attention-deficit hyperactivity disorder – was this a correct decision? A literature review journal, June 2014

Regulation of Hippocampal Cannabinoid CB1 Receptor Actions by Adenosine A1 Receptors and Chronic Caffeine Administration: Implications for the Effects of Δ9-Tetrahydrocannabinol on Spatial Memory journal, October 2010

A Critical Role of the Adenosine A2A Receptor in Extrastriatal Neurons in Modulating Psychomotor Activity as Revealed by Opposite Phenotypes of Striatum and Forebrain A2A Receptor Knock-Outs journal, March 2008

Presynaptic adenosine A 2A receptors dampen cannabinoid CB 1 receptor-mediated inhibition of corticostriatal glutamatergic transmission : A journal, January 2015

Pre-synaptic adenosine A2A receptors control cannabinoid CB1 receptor-mediated inhibition of striatal glutamatergic neurotransmission: Cross-talk between A2A and CB1 receptors in rat striatum journal, December 2010

Bidirectional regulation of novelty-induced behavioral inhibition by the endocannabinoid system journal, December 2009

Adenosine A2A Receptors in Striatal Glutamatergic Terminals and GABAergic Neurons Oppositely Modulate Psychostimulant Action and DARPP-32 Phosphorylation journal, November 2013

Chronic and acute adenosine A2A receptor blockade prevents long-term episodic memory disruption caused by acute cannabinoid CB1 receptor activation journal, May 2017

Endocannabinoid Signaling in the Brain journal, April 2002

Adenosine A2A Receptors in the Rat Prelimbic Medial Prefrontal Cortex Control Delay-Based Cost-Benefit Decision Making journal, December 2018

Heterodimeric adenosine receptors: a device to regulate neurotransmitter release journal, October 2006

Effects of the cannabinoid CB1 receptor antagonist rimonabant on distinct measures of impulsive behavior in rats journal, March 2007

Optogenetic Activation of Adenosine A2A Receptor Signaling in the Dorsomedial Striatopallidal Neurons Suppresses Goal-Directed Behavior journal, July 2015

Effects of THC on Behavioral Measures of Impulsivity in Humans journal, February 2003

High-Potency Marijuana Impairs Executive Function and Inhibitory Motor Control journal, March 2006

Attention-Deficit/Hyperactivity Disorder: Diagnosis, Lifespan, Comorbidities, and Neurobiology journal, May 2007

Optogenetic activation of intracellular adenosine A2A receptor signaling in the hippocampus is sufficient to trigger CREB phosphorylation and impair memory journal, February 2015

Cannabinoids inhibit the synaptic uptake of adenosine and dopamine in the rat and mouse striatum journal, March 2011

A study of the possible association between adenosine A 2A receptor gene polymorphisms and attention-deficit hyperactivity disorder traits : Adenosine A journal, March 2013

SLV330, a cannabinoid CB1 receptor antagonist, attenuates ethanol and nicotine seeking and improves inhibitory response control in rats journal, March 2011

Striatal adenosine-cannabinoid receptor interactions in rats over-expressing adenosine A 2A receptors journal, November 2015

Attention Deficits and Hyperactivity Following Inhibition of cAMP-Dependent Protein Kinase Within the Medial Prefrontal Cortex of Rats journal, April 2009

Current concepts on the neurobiology of Attention-Deficit/Hyperactivity Disorder journal, April 2002

Caffeine improves attention deficit in neonatal 6-OHDA lesioned rats, an animal model of attention deficit hyperactivity disorder (ADHD) journal, April 2011

Inhibitory control and psychopathology: A meta-analysis of studies using the stop signal task journal, August 2010

Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity journal, January 2014

Striatal Adenosine A2A and Cannabinoid CB1 Receptors Form Functional Heteromeric Complexes that Mediate the Motor Effects of Cannabinoids journal, March 2007

Adenosine A 1 Receptor-mediated Modulation of Dopamine D 1 Receptors in Stably Cotransfected Fibroblast Cells journal, February 1998

The adolescent brain and age-related behavioral manifestations journal, June 2000

Caffeine drinking potentiates cannabinoid transmission in the striatum: Interaction with stress effects journal, March 2009

Combined effects of THC and caffeine on working memory in rats: Effects of caffeine and THC on working memory journal, March 2012

l-Amphetamine improves poor sustained attention while d-amphetamine reduces overactivity and impulsiveness as well as improves sustained attention in an animal model of Attention-Deficit/Hyperactivity Disorder (ADHD) journal, January 2008

Behavioral models of impulsivity in relation to ADHD: Translation between clinical and preclinical studies journal, August 2006

Neurocognitive performance during acute THC intoxication in heavy and occasional cannabis users journal, August 2008

Adenosine A2A receptors and basal ganglia physiology journal, December 2007

The neuropharmacology of impulsive behaviour journal, April 2008

An Update on Adenosine A2A-Dopamine D2 Receptor Interactions: Implications for the Function of G Protein-Coupled Receptors journal, May 2008

Varieties of impulsivity journal, October 1999

Effects of methylphenidate on attentional set-shifting in a genetic model of attention-deficit/hyperactivity disorder journal, January 2012

Toward Systems Neuroscience of ADHD: A Meta-Analysis of 55 fMRI Studies journal, October 2012

Caffeine regulates frontocorticostriatal dopamine transporter density and improves attention and cognitive deficits in an animal model of attention deficit hyperactivity disorder journal, April 2013

Adenosine A2A receptor antagonism and genetic deletion attenuate the effects of dopamine D2 antagonism on effort-based decision making in mice journal, April 2012

Persistent effects of chronic Δ9-THC exposure on motor impulsivity in rats journal, April 2015

Integrated events in central dopamine transmission as analyzed at multiple levels. Evidence for intramembrane adenosine A2A/dopamine D2 and adenosine A1/dopamine D1 receptor interactions in the basal ganglia1Published on the World Wide Web on 12 January 1998.1 journal, May 1998

Is ADHD a disinhibitory disorder? journal, January 2001

Rodent Models of Attention-Deficit/Hyperactivity Disorder journal, June 2005

Translational Approaches to Frontostriatal Dysfunction in Attention-Deficit/Hyperactivity Disorder Using a Computerized Neuropsychological Battery journal, June 2011

Validity of the Executive Function Theory of Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review journal, June 2005

Genetic Deletion of A2A Adenosine Receptors in the Striatum Selectively Impairs Habit Formation journal, December 2009

How does adenosine control neuronal dysfunction and neurodegeneration? journal, August 2016

A Meta-Analytic Review of Stopping Performance in Attention-Deficit/Hyperactivity Disorder: Deficient Inhibitory Motor Control? journal, January 2005

Potential Therapeutic Interest of Adenosine A2A Receptors in Psychiatric Disorders journal, May 2008

Adenosine Transporter ENT1 Regulates the Acquisition of Goal-Directed Behavior and Ethanol Drinking through A2A Receptor in the Dorsomedial Striatum journal, March 2013

Role of CNR1 polymorphisms in moderating the effects of psychosocial adversity on impulsivity in adolescents journal, July 2014

Control of Cannabinoid CB1 Receptor Function on Glutamate Axon Terminals by Endogenous Adenosine Acting at A1 Receptors journal, January 2010

Cannabinoid-induced conditioned place preference in the spontaneously hypertensive rat–an animal model of attention deficit hyperactivity disorder journal, May 2009

Chronic Caffeine Consumption Prevents Memory Disturbance in Different Animal Models of Memory Decline journal, April 2010

Cannabinoid CB1 Receptor Activation Mediates the Opposing Effects of Amphetamine on Impulsive Action and Impulsive Choice journal, October 2011

Methylphenidate reduces impulsive behaviour in juvenile Wistar rats, but not in adult Wistar, SHR and WKY rats journal, April 2007

Enhanced Functional Activity of the Cannabinoid Type-1 Receptor Mediates Adolescent Behavior journal, October 2015

Differential effects of d-amphetamine on impulsive choice in spontaneously hypertensive and Wistar–Kyoto rats journal, January 2009

Increased sensitivity of adolescent spontaneously hypertensive rats, an animal model of attention deficit hyperactivity disorder, to the locomotor stimulation induced by the cannabinoid receptor agonist WIN 55,212-2 journal, June 2007

Regulation of endocannabinoid signaling by stress: Implications for stress-related affective disorders
journal, August 2008

Differential glutamate-dependent and glutamate-independent adenosine A ₁ receptor-mediated modulation of dopamine release in different striatal compartments
journal, April 2007

Ostracising caffeine from the pharmacological arsenal for attention-deficit hyperactivity disorder – was this a correct decision? A literature review
journal, June 2014

Regulation of Hippocampal Cannabinoid CB1 Receptor Actions by Adenosine A1 Receptors and Chronic Caffeine Administration: Implications for the Effects of Δ9-Tetrahydrocannabinol on Spatial Memory
journal, October 2010

A Critical Role of the Adenosine A2A Receptor in Extrastriatal Neurons in Modulating Psychomotor Activity as Revealed by Opposite Phenotypes of Striatum and Forebrain A2A Receptor Knock-Outs
journal, March 2008

Presynaptic adenosine A _2A receptors dampen cannabinoid CB ₁ receptor-mediated inhibition of corticostriatal glutamatergic transmission : A
journal, January 2015

Pre-synaptic adenosine A2A receptors control cannabinoid CB1 receptor-mediated inhibition of striatal glutamatergic neurotransmission: Cross-talk between A2A and CB1 receptors in rat striatum
journal, December 2010

Bidirectional regulation of novelty-induced behavioral inhibition by the endocannabinoid system
journal, December 2009

Adenosine A2A Receptors in Striatal Glutamatergic Terminals and GABAergic Neurons Oppositely Modulate Psychostimulant Action and DARPP-32 Phosphorylation
journal, November 2013

Chronic and acute adenosine A2A receptor blockade prevents long-term episodic memory disruption caused by acute cannabinoid CB1 receptor activation
journal, May 2017

Endocannabinoid Signaling in the Brain
journal, April 2002

Adenosine A2A Receptors in the Rat Prelimbic Medial Prefrontal Cortex Control Delay-Based Cost-Benefit Decision Making
journal, December 2018

Heterodimeric adenosine receptors: a device to regulate neurotransmitter release
journal, October 2006

Effects of the cannabinoid CB1 receptor antagonist rimonabant on distinct measures of impulsive behavior in rats
journal, March 2007

Optogenetic Activation of Adenosine A2A Receptor Signaling in the Dorsomedial Striatopallidal Neurons Suppresses Goal-Directed Behavior
journal, July 2015

Effects of THC on Behavioral Measures of Impulsivity in Humans
journal, February 2003

High-Potency Marijuana Impairs Executive Function and Inhibitory Motor Control
journal, March 2006

Attention-Deficit/Hyperactivity Disorder: Diagnosis, Lifespan, Comorbidities, and Neurobiology
journal, May 2007

Optogenetic activation of intracellular adenosine A2A receptor signaling in the hippocampus is sufficient to trigger CREB phosphorylation and impair memory
journal, February 2015

Cannabinoids inhibit the synaptic uptake of adenosine and dopamine in the rat and mouse striatum
journal, March 2011

A study of the possible association between adenosine A _2A receptor gene polymorphisms and attention-deficit hyperactivity disorder traits : Adenosine A
journal, March 2013

SLV330, a cannabinoid CB1 receptor antagonist, attenuates ethanol and nicotine seeking and improves inhibitory response control in rats
journal, March 2011

Striatal adenosine-cannabinoid receptor interactions in rats over-expressing adenosine A _2A receptors
journal, November 2015

Attention Deficits and Hyperactivity Following Inhibition of cAMP-Dependent Protein Kinase Within the Medial Prefrontal Cortex of Rats
journal, April 2009

Current concepts on the neurobiology of Attention-Deficit/Hyperactivity Disorder
journal, April 2002

Caffeine improves attention deficit in neonatal 6-OHDA lesioned rats, an animal model of attention deficit hyperactivity disorder (ADHD)
journal, April 2011

Inhibitory control and psychopathology: A meta-analysis of studies using the stop signal task
journal, August 2010

Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity
journal, January 2014

Striatal Adenosine A2A and Cannabinoid CB1 Receptors Form Functional Heteromeric Complexes that Mediate the Motor Effects of Cannabinoids
journal, March 2007

Adenosine A ₁ Receptor-mediated Modulation of Dopamine D ₁ Receptors in Stably Cotransfected Fibroblast Cells
journal, February 1998

The adolescent brain and age-related behavioral manifestations
journal, June 2000

Caffeine drinking potentiates cannabinoid transmission in the striatum: Interaction with stress effects
journal, March 2009

Combined effects of THC and caffeine on working memory in rats: Effects of caffeine and THC on working memory
journal, March 2012

l-Amphetamine improves poor sustained attention while d-amphetamine reduces overactivity and impulsiveness as well as improves sustained attention in an animal model of Attention-Deficit/Hyperactivity Disorder (ADHD)
journal, January 2008

Behavioral models of impulsivity in relation to ADHD: Translation between clinical and preclinical studies
journal, August 2006

Neurocognitive performance during acute THC intoxication in heavy and occasional cannabis users
journal, August 2008

Adenosine A2A receptors and basal ganglia physiology
journal, December 2007

The neuropharmacology of impulsive behaviour
journal, April 2008

An Update on Adenosine A2A-Dopamine D2 Receptor Interactions: Implications for the Function of G Protein-Coupled Receptors
journal, May 2008

Varieties of impulsivity
journal, October 1999

Effects of methylphenidate on attentional set-shifting in a genetic model of attention-deficit/hyperactivity disorder
journal, January 2012

Toward Systems Neuroscience of ADHD: A Meta-Analysis of 55 fMRI Studies
journal, October 2012

Caffeine regulates frontocorticostriatal dopamine transporter density and improves attention and cognitive deficits in an animal model of attention deficit hyperactivity disorder
journal, April 2013

Adenosine A2A receptor antagonism and genetic deletion attenuate the effects of dopamine D2 antagonism on effort-based decision making in mice
journal, April 2012

Persistent effects of chronic Δ9-THC exposure on motor impulsivity in rats
journal, April 2015

Integrated events in central dopamine transmission as analyzed at multiple levels. Evidence for intramembrane adenosine A2A/dopamine D2 and adenosine A1/dopamine D1 receptor interactions in the basal ganglia1Published on the World Wide Web on 12 January 1998.1
journal, May 1998

Is ADHD a disinhibitory disorder?
journal, January 2001

Rodent Models of Attention-Deficit/Hyperactivity Disorder
journal, June 2005

Translational Approaches to Frontostriatal Dysfunction in Attention-Deficit/Hyperactivity Disorder Using a Computerized Neuropsychological Battery
journal, June 2011

Validity of the Executive Function Theory of Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review
journal, June 2005

Genetic Deletion of A2A Adenosine Receptors in the Striatum Selectively Impairs Habit Formation
journal, December 2009

How does adenosine control neuronal dysfunction and neurodegeneration?
journal, August 2016

A Meta-Analytic Review of Stopping Performance in Attention-Deficit/Hyperactivity Disorder: Deficient Inhibitory Motor Control?
journal, January 2005

Potential Therapeutic Interest of Adenosine A2A Receptors in Psychiatric Disorders
journal, May 2008

Adenosine Transporter ENT1 Regulates the Acquisition of Goal-Directed Behavior and Ethanol Drinking through A2A Receptor in the Dorsomedial Striatum
journal, March 2013

Role of CNR1 polymorphisms in moderating the effects of psychosocial adversity on impulsivity in adolescents
journal, July 2014

Control of Cannabinoid CB1 Receptor Function on Glutamate Axon Terminals by Endogenous Adenosine Acting at A1 Receptors
journal, January 2010

Cannabinoid-induced conditioned place preference in the spontaneously hypertensive rat–an animal model of attention deficit hyperactivity disorder
journal, May 2009

Chronic Caffeine Consumption Prevents Memory Disturbance in Different Animal Models of Memory Decline
journal, April 2010

Cannabinoid CB1 Receptor Activation Mediates the Opposing Effects of Amphetamine on Impulsive Action and Impulsive Choice
journal, October 2011

Methylphenidate reduces impulsive behaviour in juvenile Wistar rats, but not in adult Wistar, SHR and WKY rats
journal, April 2007

Enhanced Functional Activity of the Cannabinoid Type-1 Receptor Mediates Adolescent Behavior
journal, October 2015

Differential effects of d-amphetamine on impulsive choice in spontaneously hypertensive and Wistar–Kyoto rats
journal, January 2009

Increased sensitivity of adolescent spontaneously hypertensive rats, an animal model of attention deficit hyperactivity disorder, to the locomotor stimulation induced by the cannabinoid receptor agonist WIN 55,212-2
journal, June 2007