Psychopharmacology

, Volume 224, Issue 4, pp 477–487 | Cite as

Failure of rewarding and locomotor stimulant doses of morphine to promote adult rat 50-kHz ultrasonic vocalizations

  • Jennifer M. Wright
  • Lan Deng
  • Paul B. S. Clarke
Original Investigation

Abstract

Rationale

Frequency-modulated 50-kHz ultrasonic vocalizations (USVs) are emitted by adult rats in response to psychostimulants and non-pharmacological appetitive stimuli and thus have been proposed to model positive affect.

Objective

The main aim was to determine whether rewarding doses of morphine increase 50-kHz call rate or alter the relative prevalence of the trill call subtype.

Methods

In experiment 1, USVs were recorded from adult male Long–Evans rats after subchronic morphine (1 mg/kg subcutaneous (SC)) administration, acute challenge with morphine (1 and 3 mg/kg SC) or amphetamine (1 mg/kg IP, positive control), and in conjunction with locomotor activity tests with morphine (1 and 3 mg/kg SC). In experiments 2 and 3, the USV altering, rewarding, and locomotor effects of morphine were examined using a conditioned place preference (CPP) procedure.

Results

In experiment 1, morphine (1 mg/kg) initially suppressed calling; rats became tolerant to this effect with repeated exposure. Tested subsequently in singly- and pair-tested rats, morphine markedly decreased USVs but significantly increased locomotor activity. In experiments 2 and 3, morphine produced a significant CPP without increasing either unconditioned or conditioned USV emission. Morphine did not detectably alter the relative prevalence of 50-kHz call subtypes.

Conclusions

Although 50-kHz calls, and the trill call subtype in particular, have been proposed as an animal model of positive mood, not all euphoriant drugs acutely increase the rate of 50-kHz calling or consistently promote trill calls.

Keywords

Ultrasonic vocalizations Rat Morphine Opioid Amphetamine Reward Conditioned place preference Locomotor activity 

Supplementary material

213_2012_2776_MOESM1_ESM.doc (246 kb)
ESM 1(DOC 245 kb)

References

  1. 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 197:205–209PubMedCrossRefGoogle Scholar
  2. Angrist B, Sathananthan G, Wilk S, Gershon S (1974) Amphetamine psychosis: behavioral and biochemical aspects. J Psychiatr Res 11:13–23PubMedCrossRefGoogle Scholar
  3. Babbini M, Davis WM (1972) Time–dose relationships for locomotor activity effects of morphine after acute or repeated treatment. Br J Pharmacol 46:213–224PubMedCrossRefGoogle Scholar
  4. Bardo MT, Rowlett JK, Harris MJ (1995) Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci Biobehav Rev 19:39–51PubMedCrossRefGoogle Scholar
  5. Bechara A, van der Kooy D (1985) Opposite motivational effects of endogenous opioids in brain and periphery. Nature 314:533–534PubMedCrossRefGoogle Scholar
  6. Bechara A, Zito KA, van der Kooy D (1987) Peripheral receptors mediate the aversive conditioning effects of morphine in the rat. Pharmacol Biochem Behav 28:219–225PubMedCrossRefGoogle Scholar
  7. Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26:507–513PubMedCrossRefGoogle Scholar
  8. Biala G, Kruk M (2007) Amphetamine-induced anxiety-related behavior in animal models. Pharmacol Rep 59:636–644PubMedGoogle Scholar
  9. Bird SJ, Kuhar MJ (1977) Iontophoretic application of opiates to the locus coeruleus. Brain Res 122:523–533PubMedCrossRefGoogle Scholar
  10. Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine–dopamine interaction and acoustic coding. Behav Brain Res 182:261–273PubMedCrossRefGoogle Scholar
  11. Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50:43–50PubMedGoogle Scholar
  12. Brudzynski SM, Pniak A (2002) Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J Comp Psychol 116:73–82PubMedCrossRefGoogle Scholar
  13. 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 209–214Google Scholar
  14. Burgdorf J, Knutson B, Panksepp J, Shippenberg TS (2001) Evaluation of rat ultrasonic vocalizations as predictors of the conditioned aversive effects of drugs. Psychopharmacology (Berl) 155:35–42CrossRefGoogle Scholar
  15. Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J (2008) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 122:357–367PubMedCrossRefGoogle Scholar
  16. 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 35:1831–1836PubMedCrossRefGoogle Scholar
  17. Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51:667–672PubMedCrossRefGoogle Scholar
  18. 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 182:284–289PubMedCrossRefGoogle Scholar
  19. Covington HEI, Miczek KA (2003) Vocalizations during withdrawal from opiates and cocaine: possible expressions of affective distress. Eur J Pharmacol 467:1–13PubMedCrossRefGoogle Scholar
  20. Dinh HK, Larkin A, Gatlin L, Piepmeier E Jr (1999) Rat ultrasound model for measuring pain resulting from intramuscularly injected antimicrobials. PDA J Pharm Sci Technol 53:40–43PubMedGoogle Scholar
  21. Fernandes M, Kluwe S, Coper H (1977) The development of tolerance to morphine in the rat. Psychopharmacology (Berl) 54:197–201CrossRefGoogle Scholar
  22. File SE, Hyde JR (1979) A test of anxiety that distinguishes between the actions of benzodiazepines and those of other minor tranquilisers and of stimulants. Pharmacol Biochem Behav 11:65–69PubMedCrossRefGoogle Scholar
  23. Fog R (1970) Behavioural effects in rats of morphine and amphetamine and of a combination of the two drugs. Psychopharmacologia 16:305–312PubMedCrossRefGoogle Scholar
  24. Foltin RW, Fischman MW (1991) Assessment of abuse liability of stimulant drugs in humans: a methodological survey. Drug Alcohol Depend 28:3–48PubMedCrossRefGoogle Scholar
  25. Hamdani S, White NM (2011) Ultrasonic vocalization ratios reflect the influence of motivational state and amygdala lesions on different types of taste avoidance learning. Behav Brain Res 217:88–98PubMedCrossRefGoogle Scholar
  26. Hamed A, Taracha E, Szyndler J, Krzascik P, Lehner M, Maciejak P, Skorzewska A, Plaznik A (2012) The effects of morphine and morphine conditioned context on 50 kHz ultrasonic vocalisation in rats. Behav Brain Res 229:447–450PubMedCrossRefGoogle Scholar
  27. Haney M, Miczek KA (1994) Ultrasounds emitted by female rats during agonistic interactions: effects of morphine and naltrexone. Psychopharmacology (Berl) 114:441–448CrossRefGoogle Scholar
  28. Haney M, Miczek KA (1995) Delta opioid receptors: reflexive, defensive and vocal affective responses in female rats. Psychopharmacology (Berl) 121:204–212CrossRefGoogle Scholar
  29. Jasinski DR, Preston KL (1986) Evaluation of mixtures of morphine and d-amphetamine for subjective and physiological effects. Drug Alcohol Depend 17:1–13PubMedCrossRefGoogle Scholar
  30. Kaltwasser MT (1990) Acoustic signaling in the black rat (Rattus rattus). J Comp Psychol 104:227–232PubMedCrossRefGoogle Scholar
  31. Knutson B, Burgdorf J, Panksepp J (1999) High-frequency ultrasonic vocalizations index conditioned pharmacological reward in rats. Physiol Behav 66:639–643PubMedCrossRefGoogle Scholar
  32. Knutson B, Burgdorf J, Panksepp J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 128:961–977PubMedCrossRefGoogle Scholar
  33. Korf J, Bunney BS, Aghajanian GK (1974) Noradrenergic neurons: morphine inhibition of spontaneous activity. Eur J Pharmacol 25:165–169PubMedCrossRefGoogle Scholar
  34. Lett BT (1989) Repeated exposures intensify rather than diminish the rewarding effects of amphetamine, morphine, and cocaine. Psychopharmacology (Berl) 98:357–362CrossRefGoogle Scholar
  35. Litvin Y, Blanchard DC, Blanchard RJ (2007) Rat 22 kHz ultrasonic vocalizations as alarm cries. Behav Brain Res 182:166–172PubMedCrossRefGoogle Scholar
  36. Maier EY, Ahrens AM, Ma ST, Schallert T, Duvauchelle CL (2010) Cocaine deprivation effect: cue abstinence over weekends boosts anticipatory 50-kHz ultrasonic vocalizations in rats. Behav Brain Res 214:75–79PubMedCrossRefGoogle Scholar
  37. Meyer PJ, Ma ST, Robinson TE (2011) A cocaine cue is more preferred and evokes more frequency-modulated 50-kHz ultrasonic vocalizations in rats prone to attribute incentive salience to a food cue. Psychopharmacology (Berl) 219:999–1009CrossRefGoogle Scholar
  38. Mueller D, Perdikaris D, Stewart J (2002) Persistence and drug-induced reinstatement of a morphine-induced conditioned place preference. Behav Brain Res 136:389–397PubMedCrossRefGoogle Scholar
  39. Nakamura H, Ishii K, Shimizu M (1978) Some altered responses in rats formerly dependent on morphine. Psychopharmacology (Berl) 56:269–277CrossRefGoogle Scholar
  40. Niel L, Weary DM (2006) Behavioural responses of rats to gradual-fill carbon dioxide euthanasia and reduced oxygen concentrations. Appl Anim Behav Sci 100:295–308CrossRefGoogle Scholar
  41. Panksepp J, Burgdorf J (2000) 50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables. Behav Brain Res 115:25–38PubMedCrossRefGoogle Scholar
  42. Parker LA, Mcdonald RV (2000) Reinstatement of both a conditioned place preference and a conditioned place aversion with drug primes. Pharmacol Biochem Behav 66:559–561PubMedCrossRefGoogle Scholar
  43. Parker LA, Limebeer CL, Slomke J (2006) Renewal effect: context-dependent extinction of a cocaine- and a morphine-induced conditioned floor preference. Psychopharmacology (Berl) 187:133–137CrossRefGoogle Scholar
  44. Parsons S (2000) Advantages and disadvantages of techniques for transforming and analyzing chiropteran echolocation calls. J Mammal 81:927–938CrossRefGoogle Scholar
  45. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Meth 14:149–167CrossRefGoogle Scholar
  46. Robinson TE, Becker JB (1986) Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res 396:157–198PubMedCrossRefGoogle Scholar
  47. Rutten K, van der Kam EL, De VJ, Tzschentke TM (2011) Critical evaluation of the use of extinction paradigms for the assessment of opioid-induced conditioned place preference in rats. Pharmacology 87:286–296PubMedCrossRefGoogle Scholar
  48. Sadananda M, Natusch C, Karrenbauer B, Schwarting RK (2012) 50-kHz calls in rats: effects of MDMA and the 5-HT(1A) receptor agonist 8-OH-DPAT. Pharmacol Biochem Behav 101:258–264PubMedCrossRefGoogle Scholar
  49. Sales GD, Pye D (1974) Ultrasonic communication by animals. Chapman and Hall, LondonCrossRefGoogle Scholar
  50. Shoaib M, Stolerman IP, Kumar RC (1994) Nicotine-induced place preferences following prior nicotine exposure in rats. Psychopharmacology (Berl) 113:445–452CrossRefGoogle Scholar
  51. Siegel S, MacRae J (1984) Environmental specificity of tolerance. Trends Neurosci 7:140–143CrossRefGoogle Scholar
  52. 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 13:123–132PubMedCrossRefGoogle Scholar
  53. Simola N, Fenu S, Costa G, Pinna A, Plumitallo A, Morelli M (2012) Pharmacological characterization of 50-kHz ultrasonic vocalizations in rats: comparison of the effects of different psychoactive drugs and relevance in drug-induced reward. Neuropharmacology 63:224–234Google Scholar
  54. Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613–672PubMedCrossRefGoogle Scholar
  55. Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462PubMedCrossRefGoogle Scholar
  56. Vasko MR, Domino EF (1978) Tolerance development to the biphasic effects of morphine on locomotor activity and brain acetylcholine in the rat. J Pharmacol Exp Ther 207:848–858PubMedGoogle Scholar
  57. Vivian JA, Miczek KA (1991) Ultrasounds during morphine withdrawal in rats. Psychopharmacology (Berl) 104:187–193CrossRefGoogle Scholar
  58. Vivian JA, Miczek KA (1993) Morphine attenuates ultrasonic vocalization during agonistic encounters in adult male rats. Psychopharmacology (Berl) 111:367–375CrossRefGoogle Scholar
  59. Williams SN, Undieh AS (2010) Brain-derived neurotrophic factor signaling modulates cocaine induction of reward-associated ultrasonic vocalization in rats. J Pharmacol Exp Ther 332:463–468PubMedCrossRefGoogle Scholar
  60. Wohr M, Schwarting RK (2009) Ultrasonic communication in rats: effects of morphine and naloxone on vocal and behavioral responses to playback of 50-kHz vocalizations. Pharmacol Biochem Behav 94:285–295PubMedCrossRefGoogle Scholar
  61. Wohr M, Schwarting RK (2010) Rodent ultrasonic communication and its relevance for models of neuropsychiatric disorders. e-Neuroforum 1:71–80CrossRefGoogle Scholar
  62. Wohr M, Houx B, Schwarting RK, Spruijt B (2008) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93:766–776PubMedCrossRefGoogle Scholar
  63. 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) 211:1–13CrossRefGoogle Scholar
  64. Wright JM, Dobosiewicz MR, Clarke PB (2012) Alpha- and beta-adrenergic receptors differentially modulate the emission of spontaneous and amphetamine-induced 50-kHz ultrasonic vocalizations in adult rats. Neuropsychopharmacology 37:808–821PubMedCrossRefGoogle Scholar
  65. Zacny JP, Lichtor JL, Flemming D, Coalson DW, Thompson WK (1994) A dose–response analysis of the subjective, psychomotor and physiological effects of intravenous morphine in healthy volunteers. J Pharmacol Exp Ther 268:1–9PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Jennifer M. Wright
    • 1
  • Lan Deng
    • 1
  • Paul B. S. Clarke
    • 1
  1. 1.Department of Pharmacology and TherapeuticsMcGill UniversityMontrealCanada

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