Skip to main content
SpringerLink
Log in

The role of dopaminergic transmission through D1-like and D2-like receptors in amphetamine-induced rat ultrasonic vocalizations

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Systemic amphetamine (AMPH) administration increases the rate of 50-kHz ultrasonic vocalizations (USVs) in adult rats and preferentially enhances the ‘trill’ subtype; these effects of AMPH critically depend on noradrenergic transmission, but the possible contributions of dopamine are unclear.

Objective

To assess the role of dopamine in 50-kHz USVs emitted drug-free and following systemic AMPH administration.

Methods

Adult male Long–Evans rats pre-selected for high AMPH-induced calling rates were tested with AMPH (1 mg/kg, intraperitoneal (IP)) and saline following pretreatment with the following dopamine receptor antagonists: SCH 23390 (0.005–0.02 mg/kg, subcutaneous (SC)), SCH 39166 (0.03–0.3 mg/kg, SC), haloperidol (0.1, 0.2 mg/kg, IP), sulpiride (20–80 mg/kg, SC), raclopride (0.1–0.5 mg/kg, SC), clozapine (4 mg/kg, SC), risperidone (0.5 mg/kg, SC), and pimozide (1 mg/kg, IP). The dopamine and noradrenaline reuptake inhibitors (GBR 12909 and nisoxetine, respectively) were also tested, alone and in combination.

Results

SCH 23390, SCH 39166, haloperidol, and raclopride dose-dependently inhibited vocalizations under AMPH and suppressed the proportion of trill calls. Sulpiride, however, had no discernable effect on call rate or profile, even at a high dose that reduced locomotor activity. Single doses of clozapine, risperidone, and pimozide all markedly decreased calling under saline and AMPH. Finally, GBR 12909 and nisoxetine failed to promote 50-kHz USVs detectably or alter the subtype profile, when tested alone or in combination.

Conclusions

The rate of 50-kHz USVs and the call subtype profile following systemic AMPH administration depends on dopaminergic neurotransmission through D1-like and D2-like receptors. However, inhibiting dopamine and/or noradrenaline reuptake appears insufficient to induce calling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Acquas E, Di Chiara G (1994) D1 receptor blockade stereospecifically impairs the acquisition of drug-conditioned place preference and place aversion. Behav Pharmacol 5:555–569

    Article  PubMed  CAS  Google Scholar 

  • Acquas E, Carboni E, Leone P, Di CG (1989) SCH 23390 blocks drug-conditioned place-preference and place-aversion: anhedonia (lack of reward) or apathy (lack of motivation) after dopamine-receptor blockade? Psychopharmacology (Berl) 99:151–155

    Article  CAS  Google Scholar 

  • Agmo A, Soria P (1999) The duration of the effects of a single administration of dopamine antagonists on ambulatory activity and motor coordination. J Neural Transm 106:219–227

    Article  PubMed  CAS  Google Scholar 

  • Ahrens AM, Ma ST, Maier EY, Duvauchelle CL, Schallert T (2009) Repeated intravenous amphetamine exposure: rapid and persistent sensitization of 50-kHz ultrasonic trill calls in rats. Behav Brain Res 197:205–209

    Article  PubMed  CAS  Google Scholar 

  • Alburges ME, Hunt ME, McQuade RD, Wamsley JK (1992) D1-receptor antagonists: comparison of [3H]SCH39166 to [3H]SCH23390. J Chem Neuroanat 5:357–366

    Article  PubMed  CAS  Google Scholar 

  • Andersen PH (1989) The dopamine inhibitor GBR 12909: selectivity and molecular mechanism of action. Eur J Pharmacol 166:493–504

    Article  PubMed  CAS  Google Scholar 

  • Arnt J (1988) The discriminative stimulus properties of the D-1 agonist SK&F 38393 and the D-2 agonist (−)-NPA are mediated by separate mechanisms. Life Sci 42:565–574

    Article  PubMed  CAS  Google Scholar 

  • Arnt J (1995) Differential effects of classical and newer antipsychotics on the hypermotility induced by two dose levels of d-amphetamine. Eur J Pharmacol 283:55–62

    Article  PubMed  CAS  Google Scholar 

  • Arnt J (1996) Inhibitory effects on the discriminative stimulus properties of d-amphetamine by classical and newer antipsychotics do not correlate with antipsychotic activity. Relation to effects on the reward system? Psychopharmacology (Berl) 124:117–125

    Article  CAS  Google Scholar 

  • Arnt J, Skarsfeldt T (1998) Do novel antipsychotics have similar pharmacological characteristics? A review of the evidence. Neuropsychopharmacology 18:63–101

    Article  PubMed  CAS  Google Scholar 

  • Batsche K, Ashby CR Jr, Lee C, Schwartz J, Wang RY (1994) The behavioral effects of the stereoisomers of 4-methylaminorex, a psychostimulant, in the rat. J Pharmacol Exp Ther 269:1029–1039

    PubMed  CAS  Google Scholar 

  • Bialy M, Kalata U, Nikolaev-Diak A, Nikolaev E (2010) D1 receptors involved in the acquisition of sexual experience in male rats. Behav Brain Res 206:166–176

    Article  PubMed  CAS  Google Scholar 

  • Bischoff S, Heinrich M, Sonntag JM, Krauss J (1986) The D-1 dopamine receptor antagonist SCH 23390 also interacts potently with brain serotonin (5-HT2) receptors. Eur J Pharmacol 129:367–370

    Article  PubMed  CAS  Google Scholar 

  • Brauer LH, de Wit H (1997) High dose pimozide does not block amphetamine-induced euphoria in normal volunteers. Pharmacol Biochem Behav 56:265–272

    Article  PubMed  CAS  Google Scholar 

  • Brauer LH, Goudie AJ, de Wit H (1997) Dopamine ligands and the stimulus effects of amphetamine: animal models versus human laboratory data. Psychopharmacology (Berl) 130:2–13

    Article  CAS  Google Scholar 

  • Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine–dopamine interaction and acoustic coding. Behav Brain Res 182:261–273

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50:43–50

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM, Komadoski M, St PJ (2012) Quinpirole-induced 50 kHz ultrasonic vocalization in the rat: role of D2 and D3 dopamine receptors. Behav Brain Res 226:511–518

    Article  PubMed  CAS  Google Scholar 

  • Burgdorf J, Moskal JR (2009) Frequency modulated 50 kHz ultrasonic vocalizations reflect a positive emotional state in the rat: neural substrates and therapeutic implications. In: Brudzynski SM (ed) Handbook of mammalian vocalization. Academic, Oxford, pp 209–214

    Google Scholar 

  • Burgdorf J, Wood PL, Kroes RA, Moskal JR, Panksepp J (2007) Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies. Behav Brain Res 182:274–283

    Article  PubMed  Google Scholar 

  • Burgdorf J, Panksepp J, Brudzynski SM, Beinfeld MC, Cromwell HC, Kroes RA et al (2008) The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Dev Psychobiol 51:34–46

    Article  Google Scholar 

  • Burgdorf J, Panksepp J, Moskal JR (2010) Frequency-modulated 50 kHz ultrasonic vocalizations: a tool for uncovering the molecular substrates of positive affect. Neurosci Biobehav Rev 35:1831–1836

    Article  PubMed  Google Scholar 

  • Callahan PM, Appel JB, Cunningham KA (1991) Dopamine D1 and D2 mediation of the discriminative stimulus properties of d-amphetamine and cocaine. Psychopharmacology (Berl) 103:50–55

    Article  CAS  Google Scholar 

  • Carboni E, Silvagni A, Vacca C, Di CG (2006) Cumulative effect of norepinephrine and dopamine carrier blockade on extracellular dopamine increase in the nucleus accumbens shell, bed nucleus of stria terminalis and prefrontal cortex. J Neurochem 96:473–481

    Article  PubMed  CAS  Google Scholar 

  • Cervo L, Samanin R (1996) Effects of dopaminergic and glutamatergic receptor antagonists on the establishment and expression of conditioned locomotion to cocaine in rats. Brain Res 731:31–38

    Article  PubMed  CAS  Google Scholar 

  • Christensen AV, Arnt J, Hyttel J, Larsen JJ, Svendsen O (1984) Pharmacological effects of a specific dopamine D-1 antagonist SCH 23390 in comparison with neuroleptics. Life Sci 34:1529–1540

    Article  PubMed  CAS  Google Scholar 

  • Ciucci MR, Ma ST, Fox C, Kane JR, Ramig LO, Schallert T (2007) Qualitative changes in ultrasonic vocalization in rats after unilateral dopamine depletion or haloperidol: a preliminary study. Behav Brain Res 182:284–289

    Article  PubMed  CAS  Google Scholar 

  • Ciucci MR, Ahrens AM, Ma ST, Kane JR, Windham EB, Woodlee MT, Schallert T (2009) Reduction of dopamine synaptic activity: degradation of 50-kHz ultrasonic vocalization in rats. Behav Neurosci 123:328–336

    Article  PubMed  Google Scholar 

  • Collins LE, Galtieri DJ, Collins P, Jones SK, Port RG, Paul NE, Hockemeyer J, Muller CE, Salamone JD (2010) Interactions between adenosine and dopamine receptor antagonists with different selectivity profiles: effects on locomotor activity. Behav Brain Res 211:148–155

    Article  PubMed  CAS  Google Scholar 

  • Collins LE, Sager TN, Sams AG, Pennarola A, Port RG, Shahriari M, Salamone JD (2012) The novel adenosine A2A antagonist Lu AA47070 reverses the motor and motivational effects produced by dopamine D2 receptor blockade. Pharmacol Biochem Behav 100:498–505

    Article  PubMed  CAS  Google Scholar 

  • Crissman AM, O’Donnell JM (2002) Effects of antidepressants in rats trained to discriminate centrally administered isoproterenol. J Pharmacol Exp Ther 302:606–611

    Article  PubMed  CAS  Google Scholar 

  • Davids E, Zhang K, Kula NS, Tarazi FI, Baldessarini RJ (2002) Effects of norepinephrine and serotonin transporter inhibitors on hyperactivity induced by neonatal 6-hydroxydopamine lesioning in rats. J Pharmacol Exp Ther 301:1097–1102

    Article  PubMed  CAS  Google Scholar 

  • de Paulis T, Kumar Y, Johansson L, Ramsby S, Florvall L, Hall H, Angeby-Moller K, Ogren SO (1985) Potential neuroleptic agents. 3. Chemistry and antidopaminergic properties of substituted 6-methoxysalicylamides. J Med Chem 28:1263–1269

    Article  PubMed  Google Scholar 

  • Dekeyne A, Gobert A, Iob L, Cistarelli L, Melon C, Millan MJ (2001) Discriminative stimulus properties of the selective norepinephrine reuptake inhibitor, reboxetine, in rats. Psychopharmacology (Berl) 158:213–218

    Article  CAS  Google Scholar 

  • Emerich DF, Sanberg PR (1991) Neuroleptic dysphoria. Biol Psychiatry 29:201–203

    Article  PubMed  CAS  Google Scholar 

  • Exner M, Furmidge LJ, White FJ, Clark D (1989) Inhibitory effects of partial D2 dopamine receptor agonists on the d-amphetamine discriminative cue. Behav Pharmacol 1:101–111

    Article  PubMed  Google Scholar 

  • Ferrari F, Giuliani D (1995) Behavioural assessment in rats of the antipsychotic potential of the potent dopamine D2 receptor antagonist, (-)eticlopride. Pharmacol Res 31:261–267

    Article  PubMed  CAS  Google Scholar 

  • Furmidge LJ, Exner M, Clark D (1991) Role of dopamine D1 and D2 receptors in mediating the d-amphetamine discriminative cue. Eur J Pharmacol 202:191–199

    Article  PubMed  CAS  Google Scholar 

  • Garcia Horsman P, Paredes RG (2004) Dopamine antagonists do not block conditioned place preference induced by paced mating behavior in female rats. Behav Neurosci 118:356–364

    Article  PubMed  CAS  Google Scholar 

  • Grilly DM, Loveland A (2001) What is a “low dose” of d-amphetamine for inducing behavioral effects in laboratory rats? Psychopharmacology (Berl) 153:155–169

    Article  CAS  Google Scholar 

  • Guyon A, Assouly-Besse F, Biala G, Puech AJ, Thiebot MH (1993) Potentiation by low doses of selected neuroleptics of food-induced conditioned place preference in rats. Psychopharmacology (Berl) 110:460–466

    Article  CAS  Google Scholar 

  • Hall H, Sallemark M, Jerning E (1986) Effects of remoxipride and some related new substituted salicylamides on rat brain receptors. Acta Pharmacol Toxicol (Copenh) 58:61–70

    Article  CAS  Google Scholar 

  • Hietala J, Seppala T, Lappalainen J, Syvalahti E (1992) Quantification of SCH 39166, a novel selective D1 dopamine receptor antagonist, in rat brain and blood. Psychopharmacology (Berl) 106:455–458

    Article  CAS  Google Scholar 

  • Hillegaart V, Ahlenius S (1987) Effects of raclopride on exploratory locomotor activity, treadmill locomotion, conditioned avoidance behaviour and catalepsy in rats: behavioural profile comparisons between raclopride, haloperidol and preclamol. Pharmacol Toxicol 60:350–354

    Article  PubMed  CAS  Google Scholar 

  • Hiroi N, White NM (1991) The amphetamine conditioned place preference: differential involvement of dopamine receptor subtypes and two dopaminergic terminal areas. Brain Res 552:141–152

    Article  PubMed  CAS  Google Scholar 

  • Ho BT, Huang JT (1975) Role of dopamine in d-amphetamine-induced discriminative responding. Pharmacol Biochem Behav 3:1085–1092

    Article  PubMed  CAS  Google Scholar 

  • Hoffman DC, Beninger RJ (1985) The D1 dopamine receptor antagonist, SCH 23390 reduces locomotor activity and rearing in rats. Pharmacol Biochem Behav 22:341–342

    Article  PubMed  CAS  Google Scholar 

  • Hoffman DC, Donovan H (1995a) Effects of typical, atypical, and novel antipsychotic drugs on amphetamine-induced place conditioning in rats. Drug Dev Res 36:193–198

    Article  CAS  Google Scholar 

  • Hoffman DC, Donovan H (1995b) Catalepsy as a rodent model for detecting antipsychotic drugs with extrapyramidal side effect liability. Psychopharmacology (Berl) 120:128–133

    Article  CAS  Google Scholar 

  • Hooks MS, Jones DN, Holtzman SG, Juncos JL, Kalivas PW, Justice JB Jr (1994) Individual differences in behavior following amphetamine, GBR-12909, or apomorphine but not SKF-38393 or quinpirole. Psychopharmacology (Berl) 116:217–225

    Article  CAS  Google Scholar 

  • Horvitz JC, Ettenberg A (1991) Conditioned incentive properties of a food-paired conditioned stimulus remain intact during dopamine receptor blockade. Behav Neurosci 105:536–541

    Article  PubMed  CAS  Google Scholar 

  • Imperato A, Di Chiara G (1985) Dopamine release and metabolism in awake rats after systemic neuroleptics as studied by trans-striatal dialysis. J Neurosci 5:297–306

    PubMed  CAS  Google Scholar 

  • Ishiwata K, Kobayashi T, Kawamura K, Matsuno K, Senda M (2001) [11C]Raclopride binding was reduced in vivo by sigma(1) receptor ligand SA4503 in the mouse brain, while [11C]SA4503 binding was not by raclopride. Nucl Med Biol 28:787–792

    Article  PubMed  CAS  Google Scholar 

  • Jafari S, Fernandez-Enright F, Huang XF (2012) Structural contributions of antipsychotic drugs to their therapeutic profiles and metabolic side effects. J Neurochem 120:371–384

    Article  PubMed  CAS  Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 128:961–977

    Article  PubMed  Google Scholar 

  • Le Foll B, Gallo A, Le SY, Lu L, Gorwood P (2009) Genetics of dopamine receptors and drug addiction: a comprehensive review. Behav Pharmacol 20:1–17

    Article  PubMed  CAS  Google Scholar 

  • Leone P, Di Chiara G (1987) Blockade of D-1 receptors by SCH 23390 antagonizes morphine- and amphetamine-induced place preference conditioning. Eur J Pharmacol 135:251–254

    Article  PubMed  CAS  Google Scholar 

  • Leyton M, aan het Rot M, Booij L, Baker GB, Young SN, Benkelfat C (2007) Mood-elevating effects of d-amphetamine and incentive salience: the effect of acute dopamine precursor depletion. J Psychiatry Neurosci 32:129–136

    PubMed  Google Scholar 

  • Leyton M, Casey KF, Delaney JS, Kolivakis T, Benkelfat C (2005) Cocaine craving, euphoria, and self-administration: a preliminary study of the effect of catecholamine precursor depletion. Behav Neurosci 119:1619–1627

    Article  PubMed  CAS  Google Scholar 

  • Liao Y, Venhuis BJ, Rodenhuis N, Timmerman W, Wikstrom H, Meier E, Bartoszyk GD, Bottcher H, Seyfried CA, Sundell S (1999) New (sulfonyloxy)piperazinyldibenzazepines as potential atypical antipsychotics: chemistry and pharmacological evaluation. J Med Chem 42:2235–2244

    Article  PubMed  CAS  Google Scholar 

  • Ljungberg T, Ungerstedt U (1985) A rapid and simple behavioural screening method for simultaneous assessment of limbic and striatal blocking effects of neuroleptic drugs. Pharmacol Biochem Behav 23:479–485

    Article  PubMed  CAS  Google Scholar 

  • Maggio R, Aloisi G, Silvano E, Rossi M, Millan MJ (2009) Heterodimerization of dopamine receptors: new insights into functional and therapeutic significance. Parkinsonism Relat Disord 15(Suppl 4):S2–S7

    Article  PubMed  Google Scholar 

  • McKittrick CR, Abercrombie ED (2007) Catecholamine mapping within nucleus accumbens: differences in basal and amphetamine-stimulated efflux of norepinephrine and dopamine in shell and core. J Neurochem 100:1247–1256

    Article  PubMed  CAS  Google Scholar 

  • McMillen BA, German DC, Sanghere MK, Warnack W, Shore PA (1980) Pimozide: delayed onset of action at rat striatal pre- and postsynaptic dopamine receptors. J Pharmacol Exp Ther 215:150–155

    PubMed  CAS  Google Scholar 

  • McQuade RD, Duffy RA, Anderson CC, Crosby G, Coffin VL, Chipkin RE, Barnett A (1991a) [3H]SCH 39166, a new D1-selective radioligand: in vitro and in vivo binding analyses. J Neurochem 57:2001–2010

    Article  PubMed  CAS  Google Scholar 

  • McQuade RD, Duffy RA, Coffin VL, Chipkin RE, Barnett A (1991b) In vivo binding of SCH 39166: a D-1 selective antagonist. J Pharmacol Exp Ther 257:42–49

    PubMed  CAS  Google Scholar 

  • Mehta MA, Sahakian BJ, McKenna PJ, Robbins TW (1999) Systemic sulpiride in young adult volunteers simulates the profile of cognitive deficits in Parkinson’s disease. Psychopharmacology (Berl) 146:162–174

    Article  CAS  Google Scholar 

  • Menzaghi F, Whelan KT, Risbrough VB, Rao TS, Lloyd GK (1997) Effects of a novel cholinergic ion channel agonist SIB-1765F on locomotor activity in rats. J Pharmacol Exp Ther 280:384–392

    PubMed  CAS  Google Scholar 

  • Meyer ME, Cottrell GA, Van HC, Potter TJ (1993) Effects of dopamine D1 antagonists SCH23390 and SK&F83566 on locomotor activities in rats. Pharmacol Biochem Behav 44:429–432

    Article  PubMed  CAS  Google Scholar 

  • Millan MJ, Dekeyne A (2007) Discriminative stimulus properties of the selective norepinephrine reuptake inhibitor, reboxetine, in rats: a characterization with alpha/beta-adrenoceptor subtype selective ligands, antidepressants, and antagonists at neuropeptide receptors. Int J Neuropsychopharmacol 10:579–593

    Article  PubMed  CAS  Google Scholar 

  • Millan MJ, Seguin L, Gobert A, Cussac D, Brocco M (2004) The role of dopamine D3 compared with D2 receptors in the control of locomotor activity: a combined behavioural and neurochemical analysis with novel, selective antagonists in rats. Psychopharmacology (Berl) 174:341–357

    Article  CAS  Google Scholar 

  • Mithani S, Martin-Iverson MT, Phillips AG, Fibiger HC (1986) The effects of haloperidol on amphetamine- and methylphenidate-induced conditioned place preferences and locomotor activity. Psychopharmacology (Berl) 90:247–252

    Article  CAS  Google Scholar 

  • Moore S, Kenyon P (1994) Atypical antipsychotics, clozapine and sulpiride do not antagonise amphetamine-induced stereotyped locomotion. Psychopharmacology (Berl) 114:123–130

    Article  CAS  Google Scholar 

  • Morelli M, Di CG (1985) Catalepsy induced by SCH 23390 in rats. Eur J Pharmacol 117:179–185

    Article  PubMed  CAS  Google Scholar 

  • Morgenstern R, Fink H, Oelssner W (1983) LSD-potentiated apomorphine hypermotility: a model for differentiating antipsychotic drugs. Pharmacol Biochem Behav 18:13–17

    Article  PubMed  CAS  Google Scholar 

  • Morpurgo C, Theobald W (1964) Influence of antiparkinson drugs and amphetamine on some pharmacological effects of phenothiazine derivatives used as neuroleptics. Psychopharmacologia 6:178–191

    Article  PubMed  CAS  Google Scholar 

  • Nicklaus KJ, McGonigle P, Molinoff PB (1988) [3H]SCH 23390 labels both dopamine-1 and 5-hydroxytryptamine1c receptors in the choroid plexus. J Pharmacol Exp Ther 247:343–348

    PubMed  CAS  Google Scholar 

  • Nielsen EB, Andersen PH (1992) Dopamine receptor occupancy in vivo: behavioral correlates using NNC-112, NNC-687 and NNC-756, new selective dopamine D1 receptor antagonists. Eur J Pharmacol 219:35–44

    Article  PubMed  CAS  Google Scholar 

  • Nielsen EB, Jepsen SA (1985) Antagonism of the amphetamine cue by both classical and atypical antipsychotic drugs. Eur J Pharmacol 111:167–176

    Article  PubMed  CAS  Google Scholar 

  • Nielsen EB, Randrup K, Andersen PH (1989) Amphetamine discrimination: effects of dopamine receptor agonists. Eur J Pharmacol 160:253–262

    Article  PubMed  CAS  Google Scholar 

  • Ogren SO, Hall H, Kohler C, Magnusson O, Sjostrand SE (1986) The selective dopamine D2 receptor antagonist raclopride discriminates between dopamine-mediated motor functions. Psychopharmacology (Berl) 90:287–294

    CAS  Google Scholar 

  • Ouagazzal A, Nieoullon A, Amalric M (1993) Effects of dopamine D1 and D2 receptor blockade on MK-801-induced hyperlocomotion in rats. Psychopharmacology (Berl) 111:427–434

    Article  CAS  Google Scholar 

  • Poncelet M, Dangoumau L, Soubrie P, Simon P (1987) Effects of neuroleptic drugs, clonidine and lithium on the expression of conditioned behavioral excitation in rats. Psychopharmacology (Berl) 92:393–397

    Article  CAS  Google Scholar 

  • Potvin S, Stip E, Roy JY (2003) Clozapine, quetiapine and olanzapine among addicted schizophrenic patients: towards testable hypotheses. Int Clin Psychopharmacol 18:121–132

    PubMed  Google Scholar 

  • Powell KR, Iuvone PM, Holtzman SG (2001) The role of dopamine in the locomotor stimulant effects and tolerance to these effects of caffeine. Pharmacol Biochem Behav 69:59–70

    Article  PubMed  CAS  Google Scholar 

  • Prinssen EP, Ellenbroek BA, Stamatovic B, Cools AR (1993) The effects of haloperidol and raclopride in the paw test are influenced similarly by SCH 39166. Eur J Pharmacol 231:275–280

    Article  PubMed  CAS  Google Scholar 

  • Rama Rao VA, Bailey J, Bishop M, Coppen A (1981) A clinical and pharmacodynamic evaluation of sulpiride. Psychopharmacology (Berl) 73:77–80

    Article  Google Scholar 

  • Ramsson ES, Howard CD, Covey DP, Garris PA (2011) High doses of amphetamine augment, rather than disrupt, exocytotic dopamine release in the dorsal and ventral striatum of the anesthetized rat. J Neurochem 119:1162–1172

    Article  PubMed  CAS  Google Scholar 

  • Rondou P, Haegeman G, Van CK (2010) The dopamine D4 receptor: biochemical and signalling properties. Cell Mol Life Sci 67:1971–1986

    Article  PubMed  CAS  Google Scholar 

  • Sacaan AI, Menzaghi F, Dunlop JL, Correa LD, Whelan KT, Lloyd GK (1996) Epibatidine: a nicotinic acetylcholine receptor agonist releases monoaminergic neurotransmitters: in vitro and in vivo evidence in rats. J Pharmacol Exp Ther 276:509–515

    PubMed  CAS  Google Scholar 

  • Salmi P, Malmgren K, Svensson TH, Ahlenius S (1998) Stimulation of forward locomotion by SCH-23390 and raclopride in d-amphetamine-treated rats. Naunyn Schmiedebergs Arch Pharmacol 357:593–599

    Article  PubMed  CAS  Google Scholar 

  • Sanchez C, Arnt J, Dragsted N, Hyttel J, Lembol HL, Meier E, Perregaard J, Skarsfeldt T (1991) Neurochemical and in vivo pharmacological profile of sertindole, a limbic-selective neuroleptic compound. Drug Dev Res 22:239–250

    Article  CAS  Google Scholar 

  • Schaefer GJ, Michael RP (1984) Drug interactions on spontaneous locomotor activity in rats. Neuroleptics and amphetamine-induced hyperactivity. Neuropharmacology 23:909–914

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JP, Packard MG (2000) Role of dopamine receptor subtypes in the acquisition of a testosterone conditioned place preference in rats. Neurosci Lett 282:17–20

    Article  PubMed  CAS  Google Scholar 

  • Seeman P, Van Tol HH (1994) Dopamine receptor pharmacology. Trends Pharmacol Sci 15:264–270

    Article  PubMed  CAS  Google Scholar 

  • Seeman P, Corbett R, Van Tol HH (1997) Atypical neuroleptics have low affinity for dopamine D2 receptors or are selective for D4 receptors. Neuropsychopharmacology 16:93–110

    Article  PubMed  CAS  Google Scholar 

  • Sharp T, Zetterstrom T, Ljungberg T, Ungerstedt U (1986) Effect of sulpiride on amphetamine-induced behaviour in relation to changes in striatal dopamine release in vivo. Eur J Pharmacol 129:411–415

    Article  PubMed  CAS  Google Scholar 

  • Shen YL, Chen YC, Liao RM (2010) Dopamine receptor antagonists impair place conditioning after acute stress in rats. Behav Pharmacol 21:77–82

    Article  PubMed  CAS  Google Scholar 

  • Shippenberg TS, Herz A (1987) Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists. Brain Res 436:169–172

    Article  PubMed  CAS  Google Scholar 

  • Shippenberg TS, Herz A (1988) Motivational effects of opioids: influence of D-1 versus D-2 receptor antagonists. Eur J Pharmacol 151:233–242

    Article  PubMed  CAS  Google Scholar 

  • Simola N, Ma ST, Schallert T (2009) Influence of acute caffeine on 50-kHz ultrasonic vocalizations in male adult rats and relevance to caffeine-mediated psychopharmacological effects. Int J Neuropsychopharmacol 13:123–132

    Article  PubMed  Google Scholar 

  • Smith FL, St JC, Yang TF, Lyness WH (1989) Role of specific dopamine receptor subtypes in amphetamine discrimination. Psychopharmacology (Berl) 97:501–506

    Article  CAS  Google Scholar 

  • Smith KS, Berridge KC, Aldridge JW (2011) Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc Natl Acad Sci U S A 108:E255–E264

    Article  PubMed  CAS  Google Scholar 

  • Sorge RE, Clarke PB (2009) Rats self-administer intravenous nicotine delivered in a novel smoking-relevant procedure: effects of dopamine antagonists. J Pharmacol Exp Ther 330:633–640

    Article  PubMed  CAS  Google Scholar 

  • Spivak KJ, Amit Z (1986) Effects of pimozide on appetitive behavior and locomotor activity: dissimilarity of effects when compared to extinction. Physiol Behav 36:457–463

    Article  PubMed  CAS  Google Scholar 

  • Spyraki C, Fibiger HC, Phillips AG (1982) Dopaminergic substrates of amphetamine-induced place preference conditioning. Brain Res 253:185–193

    Article  PubMed  CAS  Google Scholar 

  • Tagliamonte A, DeMontis G, Olianas M, Vargiu L, Corsini GU, Gessa GL (1975) Selective increase of brain dopamine synthesis by sulpiride. J Neurochem 24:707–710

    PubMed  CAS  Google Scholar 

  • Taracha E, Hamed A, Krzascik P, Lehner M, Skorzewska A, Plaznik A, Chrapusta SJ (2012) Inter-individual diversity and intra-individual stability of amphetamine-induced sensitization of frequency-modulated 50-kHz vocalization in Sprague–Dawley rats. Psychopharmacology (Berl) 222:619–632

    Article  CAS  Google Scholar 

  • Thompson B, Leonard KC, Brudzynski SM (2006) Amphetamine-induced 50 kHz calls from rat nucleus accumbens: a quantitative mapping study and acoustic analysis. Behav Brain Res 168:64–73

    Article  PubMed  CAS  Google Scholar 

  • Tice MA, Hashemi T, Taylor LA, Duffy RA, McQuade RD (1994) Characterization of the binding of SCH 39166 to the five cloned dopamine receptor subtypes. Pharmacol Biochem Behav 49:567–571

    Article  PubMed  CAS  Google Scholar 

  • Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613–672

    Article  PubMed  CAS  Google Scholar 

  • Varty GB, Higgins GA (1997) Investigations into the nature of a 7-OH-DPAT discriminative cue: comparison with d-amphetamine. Eur J Pharmacol 339:101–107

    Article  PubMed  CAS  Google Scholar 

  • Vivian JA, Miczek KA (1991) Ultrasounds during morphine withdrawal in rats. Psychopharmacology (Berl) 104:187–193

    Article  CAS  Google Scholar 

  • Voruganti L, Awad AG (2004) Neuroleptic dysphoria: towards a new synthesis. Psychopharmacology (Berl) 171:121–132

    Article  CAS  Google Scholar 

  • Voruganti L, Cortese L, Oyewumi L, Cernovsky Z, Zirul S, Awad A (2000) Comparative evaluation of conventional and novel antipsychotic drugs with reference to their subjective tolerability, side-effect profile and impact on quality of life. Schizophr Res 43:135–145

    Article  PubMed  CAS  Google Scholar 

  • Wadenberg ML, Hertel P, Fernholm R, Hygge BK, Ahlenius S, Svensson TH (2000a) Enhancement of antipsychotic-like effects by combined treatment with the alpha1-adrenoceptor antagonist prazosin and the dopamine D2 receptor antagonist raclopride in rats. J Neural Transm 107:1229–1238

    Article  PubMed  CAS  Google Scholar 

  • Wadenberg ML, Kapur S, Soliman A, Jones C, Vaccarino F (2000b) Dopamine D2 receptor occupancy predicts catalepsy and the suppression of conditioned avoidance response behavior in rats. Psychopharmacology (Berl) 150:422–429

    Article  CAS  Google Scholar 

  • Wall SC, Gu H, Rudnick G (1995) Biogenic amine flux mediated by cloned transporters stably expressed in cultured cell lines: amphetamine specificity for inhibition and efflux. Mol Pharmacol 47:544–550

    PubMed  CAS  Google Scholar 

  • Wamsley JK, Hunt ME, McQuade RD, Alburges ME (1991) [3H]SCH39166, a D1 dopamine receptor antagonist: binding characteristics and localization. Exp Neurol 111:145–151

    Article  PubMed  CAS  Google Scholar 

  • West WB, Van Groll BJ, Appel JB (1995) Stimulus effects of d-amphetamine II: DA, NE, and 5-HT mechanisms. Pharmacol Biochem Behav 51:69–76

    Article  PubMed  CAS  Google Scholar 

  • White IM, Ciancone MT, Haracz JL, Rebec GV (1992) A lever-release version of the conditioned avoidance response paradigm: effects of haloperidol, clozapine, sulpiride, and BMY-14802. Pharmacol Biochem Behav 41:29–35

    Article  PubMed  CAS  Google Scholar 

  • Williams SN, Undieh AS (2010) Brain-derived neurotrophic factor signaling modulates cocaine induction of reward-associated ultrasonic vocalization in rats. J Pharmacol Exp Ther 332:463–468

    Article  PubMed  CAS  Google Scholar 

  • Wintink AJ, Brudzynski SM (2001) The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats. Pharmacol Biochem Behav 70:317–323

    Article  PubMed  CAS  Google Scholar 

  • Wohr M, Schwarting RK (2010) Rodent ultrasonic communication and its relevance for models of neuropsychiatric disorders. e-Neuroforum 1:71–80

    Article  Google Scholar 

  • Wohr M, Houx B, Schwarting RK, Spruijt B (2008) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93:766–776

    Article  PubMed  CAS  Google Scholar 

  • Wong DT, Bymaster FP (1976) Effect of nisoxetine on uptake of catecholamines in synaptosomes isolated from discrete regions of rat brain. Biochem Pharmacol 25:1979–1983

    Article  PubMed  CAS  Google Scholar 

  • Wong DT, Threlkeld PG, Best KL, Bymaster FP (1982) A new inhibitor of norepinephrine uptake devoid of affinity for receptors in rat brain. J Pharmacol Exp Ther 222:61–65

    PubMed  CAS  Google Scholar 

  • Wright JM, Gourdon JC, Clarke PB (2010) Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacology (Berl) 211:1–13

    Article  CAS  Google Scholar 

  • Wright JM, Deng L, Clarke PB (2012a) Failure of rewarding and locomotor stimulant doses of morphine to promote adult rat 50-kHz ultrasonic vocalizations. Psychopharmacology (Berl) (in press)

  • Wright JM, Dobosiewicz MR, Clarke PB (2012b) Alpha- and beta-adrenergic receptors differentially modulate the emission of spontaneous and amphetamine-induced 50-kHz ultrasonic vocalizations in adult rats. Neuropsychopharmacology 37:808–821

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Supported by a Natural Science and Engineering Research Council of Canada (NSERC) discovery grant (155055, to P.B.S.C) and an NSERC Postgraduate Scholarship D (to J.M.W). The authors would like to acknowledge the NIMH Chemical Synthesis and Drug Supply Program for generously providing clozapine, GBR 12909 2HCl, and (±)-nisoxetine HCl for this study. P.B.S.C. is a member of the Center for Studies in Behavioral Neurobiology at Concordia University in Montreal. The authors have no financial relationship with the organization that sponsored this research. All experiments comply with the current laws of Canada.

Author information

Authors and Affiliations

  1. Department of Pharmacology and Therapeutics, McGill University, McIntyre Medical Building Rm. 1320 3655 Promenade Sir William Osler, Montreal, QC, H3G 1Y6, Canada

    Jennifer M. Wright, May R. S. Dobosiewicz & Paul B. S. Clarke

Authors
  1. Jennifer M. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. May R. S. Dobosiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul B. S. Clarke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul B. S. Clarke.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Experiments 8: GBR 12909 failed to significantly promote 50-kHz calling at any dose 20–40 min post-injection (a) and 40–60 min post-injection (b). *p < 0.05 versus vehicle control (Wilcoxon with Holm–Bonferroni correction) (DOC 80 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wright, J.M., Dobosiewicz, M.R.S. & Clarke, P.B.S. The role of dopaminergic transmission through D1-like and D2-like receptors in amphetamine-induced rat ultrasonic vocalizations. Psychopharmacology 225, 853–868 (2013). https://doi.org/10.1007/s00213-012-2871-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-012-2871-1

Keywords

Search

Navigation