Modulatory influence of dopamine receptors on consolidation of object recognition memory

The role of dopamine receptors in regulating the formation of recognition memory remains poorly understood. Here we show the effects of systemic administration of dopamine receptor agonists and antagonists on the formation of memory for novel object recognition in rats. In Experiment I, rats received an intraperitoneal (i.p.) injection of vehicle, the selective D1 receptor agonist SKF38393 (1.0 and 5.0mg/kg), or the D2 receptor agonist quinpirole (1.0 and 5.0mg/kg) immediately after training. In Experiment II, rats received an injection of vehicle, the dopamine receptor antagonist SCH23390 (0.1 and 0.05 mg/kg), or the D2 receptor antagonist raclopride (0.5 and 0.1mg/kg) before training, followed by an injection of vehicle or the nonselective dopamine receptor agonist apomorphine (0.05 mg/kg) immediately after training. SKF38393 at 5mg/kg produced an enhancement of novel object recognition memory measured at both 24 and 72 h after training, whereas the dose of 10mg/kg impaired 24-h retention. Posttraining administration of quinpirole did not affect 24-h retention. Apomorphine enhanced memory in rats given pretraining raclopride, suggesting that the effect was mediated by selective activation of D1 receptors. The results indicate that activation of D1 receptors can enhance recognition memory consolidation. Importantly, pharmacological activation of D1 receptors enhanced novel object recognition memory even under conditions in which control rats showed significant retention.

[1]  R. Ponnusamy,et al.  Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. , 2005, Learning & memory.

[2]  M. Mehta,et al.  Dopaminergic enhancement of cognitive function. , 2006, Current pharmaceutical design.

[3]  J. Seamans,et al.  Memory enhancement by post-training peripheral administration of low doses of dopamine agonists: possible autoreceptor effect. , 1993, Behavioral and neural biology.

[4]  A. Oliverio,et al.  Role of dopamine receptors subtypes, D1-like and D2-like, within the nucleus accumbens subregions, core and shell, on memory consolidation in the one-trial inhibitory avoidance task. , 2008, Learning & memory.

[5]  G. Lynch,et al.  The neurobiology of learning and memory , 1989, Cognition.

[6]  P. Spano,et al.  Opposite effects of dopamine D2 and D3 receptors on learning and memory in the rat. , 1997, European journal of pharmacology.

[7]  T. Bussey,et al.  Glutamate Receptors in Perirhinal Cortex Mediate Encoding, Retrieval, and Consolidation of Object Recognition Memory , 2005, The Journal of Neuroscience.

[8]  C. Garbay,et al.  Involvement of D2 dopamine receptors in the opposing effects of two CCK-B agonists in a spatial recognition memory task: role of the anterior nucleus accumbens , 2000, Psychopharmacology.

[9]  D. Ingram,et al.  Involvement of dopamine D2 receptors in complex maze learning and acetylcholine release in ventral hippocampus of rats , 2001, Neuroscience.

[10]  Mitul A. Mehta,et al.  The dopaminergic basis of human behaviors: A review of molecular imaging studies , 2009, Neuroscience & Biobehavioral Reviews.

[11]  E. Stip,et al.  Differential Effects of D2- and D4-Blocking Neuroleptics on the Procedural Learning of Schizophrenic Patients , 1996, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[12]  S. J. Martin,et al.  Interrogating rodents regarding their object and spatial memory , 2005, Current Opinion in Neurobiology.

[13]  P. Nathan,et al.  Molecular Imaging of the Dopaminergic System and its Association with Human Cognitive Function , 2006, Biological Psychiatry.

[14]  A. Gibbs,et al.  Effects of amisulpride on emotional memory using a dual-process model in healthy male volunteers , 2010, Journal of psychopharmacology.

[15]  T. Jay,et al.  D1 receptor modulation of memory retrieval performance is associated with changes in pCREB and pDARPP-32 in rat prefrontal cortex , 2006, Behavioural Brain Research.

[16]  Peter E. Wais,et al.  The Hippocampus Supports both the Recollection and the Familiarity Components of Recognition Memory , 2006, Neuron.

[17]  P. Grasby,et al.  Dopamine D2 receptor occupancy levels of acute sulpiride challenges that produce working memory and learning impairments in healthy volunteers , 2007, Psychopharmacology.

[18]  S. Moses,et al.  Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships , 2005, Brain Research Bulletin.

[19]  J. Delacour,et al.  A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data , 1988, Behavioural Brain Research.

[20]  J. Delacour,et al.  The roman strains of rats as a psychogenetic tool for pharmacological investigation of working memory: example with RU 41656 , 2005, Psychopharmacology.

[21]  S. O'dell,et al.  Methamphetamine Influences on Recognition Memory: Comparison of Escalating and Single-Day Dosing Regimens , 2008, Neuropsychopharmacology.

[22]  T. Nabeshima,et al.  Aripiprazole ameliorates phencyclidine-induced impairment of recognition memory through dopamine D1 and serotonin 5-HT1A receptors , 2008, Psychopharmacology.

[23]  T. Nabeshima,et al.  Dopamine D1 receptors regulate protein synthesis-dependent long-term recognition memory via extracellular signal-regulated kinase 1/2 in the prefrontal cortex. , 2007, Learning & memory.

[24]  J. Braszko D2 dopamine receptor blockade prevents cognitive effects of Ang IV and des-Phe6 Ang IV , 2006, Physiology & Behavior.

[25]  R. Prediger,et al.  Antagonistic interaction between adenosine A2A and dopamine D2 receptors modulates the social recognition memory in reserpine-treated rats , 2005, Behavioural pharmacology.

[26]  Sophie L. Dix,et al.  Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition , 1999, Behavioural Brain Research.

[27]  E. Levin,et al.  Nicotinic, muscarinic and dopaminergic actions in the ventral hippocampus and the nucleus accumbens: effects on spatial working memory in rats , 1996, Brain Research.

[28]  R. Roesler,et al.  Amelioration of recognition memory impairment associated with iron loading or aging by the type 4-specific phosphodiesterase inhibitor rolipram in rats , 2008, Neuropharmacology.

[29]  E. Kandel,et al.  D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Puglisi‐Allegra,et al.  Object recognition impairment in Fmr1 knockout mice is reversed by amphetamine: involvement of dopamine in the medial prefrontal cortex , 2004, Behavioural pharmacology.

[31]  S. O'dell,et al.  Neurotoxic methamphetamine regimen severely impairs recognition memory in rats , 2003, Synapse.

[32]  J. Seamans,et al.  The principal features and mechanisms of dopamine modulation in the prefrontal cortex , 2004, Progress in Neurobiology.

[33]  H. Miyakawa,et al.  Activation of dopamine D1 receptors enhances long-term depression of synaptic transmission induced by low frequency stimulation in rat hippocampal CA1 neurons , 1995, Neuroscience Letters.

[34]  José María Delgado-García,et al.  Plastic modifications induced by object recognition memory processing , 2010, Proceedings of the National Academy of Sciences.

[35]  B. O'dowd,et al.  Insights into the Role of Dopamine Receptor Systems in Learning and Memory , 2007, Reviews in the neurosciences.

[36]  I. Izquierdo,et al.  Differential neurobehavioral deficits induced by apomorphine and its oxidation product, 8-oxo-apomorphine-semiquinone, in rats. , 2002, European journal of pharmacology.

[37]  T. Bussey,et al.  Removal of cholinergic input to perirhinal cortex disrupts object recognition but not spatial working memory in the rat , 2005, The European journal of neuroscience.

[38]  José María Delgado-García,et al.  Associative Learning and CA3–CA1 Synaptic Plasticity Are Impaired in D1R Null, Drd1a−/− Mice and in Hippocampal siRNA Silenced Drd1a Mice , 2010, The Journal of Neuroscience.

[39]  Rick A Bevins,et al.  Dopamine antagonism in a novel-object recognition and a novel-object place conditioning preparation with rats , 1999, Behavioural Brain Research.

[40]  T. Bussey,et al.  Transient Inactivation of Perirhinal Cortex Disrupts Encoding, Retrieval, and Consolidation of Object Recognition Memory , 2005, The Journal of Neuroscience.

[41]  J. Braszko,et al.  Effect of D3 dopamine receptors blockade on the cognitive effects of angiotensin IV in rats , 2008, Neuropeptides.

[42]  D. Blanchard,et al.  Infralimbic D2 receptor influences on anxiety-like behavior and active memory/attention in CD-1 mice , 2003, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[43]  Marc G Caron,et al.  Dopamine receptors and brain function , 1996, Neuropharmacology.

[44]  P. Goldman-Rakic,et al.  D1 receptors in prefrontal cells and circuits , 2000, Brain Research Reviews.

[45]  S. O'dell,et al.  A sensitizing regimen of methamphetamine causes impairments in a novelty preference task of object recognition , 2006, Behavioural Brain Research.

[46]  S. Sajikumar,et al.  Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD , 2004, Neurobiology of Learning and Memory.

[47]  Malcolm W. Brown,et al.  Neuronal Responses Related to Long-Term Recognition Memory Processes in Prefrontal Cortex , 2004, Neuron.

[48]  G. Williams,et al.  Under the curve: Critical issues for elucidating D1 receptor function in working memory , 2006, Neuroscience.

[49]  J. J. Chrobak,et al.  Delayed-non-match-to-sample performance in the radial arm maze: effects of dopaminergic and gabaergic agents , 2005, Psychopharmacology.

[50]  S. O'dell,et al.  Impaired Object Recognition Memory Following Methamphetamine, but not p-Chloroamphetamine- or d-Amphetamine-Induced Neurotoxicity , 2005, Neuropsychopharmacology.

[51]  M. Maroun,et al.  Differential involvement of dopamine D1 receptor and MEK signaling pathway in the ventromedial prefrontal cortex in consolidation and reconsolidation of recognition memory. , 2009, Learning & memory.

[52]  D. Mumby,et al.  Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. , 2002, Learning & memory.

[53]  D. Mumby,et al.  Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats , 2001, Behavioural Brain Research.

[54]  R. Roesler,et al.  Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory , 2006, Neuroscience Letters.

[55]  J. Braszko Dopamine D4 receptor antagonist L745,870 abolishes cognitive effects of intracerebroventricular angiotensin IV and des-Phe6-Ang IV in rats , 2009, European Neuropsychopharmacology.

[56]  R. Roesler,et al.  Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats , 2005, Behavioural Brain Research.

[57]  T. Jay,et al.  Modulation of recognition and temporal order memory retrieval by dopamine D1 receptor in rats , 2005, Neurobiology of Learning and Memory.

[58]  T. Robbins,et al.  Sulpiride alleviates the attentional impairments of rats with medial prefrontal cortex lesions , 2003, Behavioural Brain Research.