Psychopharmacology

, Volume 211, Issue 1, pp 1–13 | Cite as

Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context

  • Jennifer M. Wright
  • Jim C. Gourdon
  • Paul B. S. Clarke
Original Investigation

Abstract

Rationale

50-kHz ultrasonic vocalizations (USVs) emitted by adult rats are heterogeneous; they occur over a wide frequency range, show varying degrees of frequency modulation, and appear to differ in their behavioral significance. However, they have not been extensively categorized.

Objectives

The main objective of this study was to identify subtypes of 50-kHz USVs emitted by adult rats and to determine how amphetamine (AMPH) or social testing condition affects their relative and absolute production rate and acoustic characteristics. A second objective was to determine the extent of individual differences in call rate, call subtype profile, and acoustic parameters (i.e., duration, bandwidth, and mean peak frequency).

Methods

Adult male Long–Evans rats were administered systemic amphetamine (0.25–2 mg/kg, IP) and tested individually or with a cage mate for 20 min. Call categories were defined based on visual inspection of over 20,000 USV spectrograms. Surgical devocalization was performed on a subset of AMPH-tested rats in order to confirm the authenticity of call subtypes.

Results

Fourteen categories of 50-kHz USVs were recognized. Call subtypes were differentially affected by social context, AMPH dose, and time within session. In contrast, the acoustic characteristics of call subtypes were notably stable. Marked and stable inter-individual differences occurred with respect to overall 50-kHz call rate, acoustic parameters, and call profile.

Conclusions

The present findings, obtained under saline and amphetamine test conditions, provide the first detailed classification of adult rat 50-kHz USVs. Consideration of 50-kHz USV subtypes may advance our understanding of inter-rat communication and affective state.

Keywords

Ultrasonic vocalizations Amphetamine Reward Frequency-modulated Trill Dose–response Individual differences 

Notes

Acknowledgments

This study was supported by a Natural Science and Engineering Research Council of Canada discovery grant (155055, to P.B.S.C), a Canadian Institutes of Health Research of Canada operating grant (MOP-10516, to P.B.S.C), and a Master’s Research Scholarship from the Fonds Québécois de Recherche sur la Nature et les Technologies (to J.M.W). We would like to thank Diala Chehayeb for valuable discussions and Laura Desrochers for help with the reliability testing. The authors have no financial relationship with the organizations that sponsored this research. Declaration: all experiments comply with the current laws of Canada.

Supplementary material

213_2010_1859_MOESM1_ESM.pdf (58 kb)
Table S1 Correlation between the average proportion of each call subtype across all test conditions (PDF 57 kb)
213_2010_1859_MOESM2_ESM.pdf (76 kb)
Table S2 ANOVA results for the effect of AMPH, social testing condition, and call category on acoustic parameters (PDF 75 kb)
213_2010_1859_MOESM3_ESM.pdf (166 kb)
Figure S1 The mean ± SEM number of USVs (per minute) during each of the sampled time intervals during the 20-min session for each of the drug conditions (a), and for the AMPH-SAL difference scores for each AMPH dose (b). (PDF 165 kb)
213_2010_1859_MOESM4_ESM.pdf (1.1 mb)
Figure S2 Individual differences in call rate were maintained within test sessions and across AMPH doses. Each rat (panels a and b) or rat pair (panels b and d) was ranked with respect to the total number of USVs emitted, either during particular 1-min time intervals within test sessions (panels a and c) or at different AMPH doses (panels b and d). For the purposes of illustration, the time course data (panels a and c) are from AMPH 1 mg/kg test sessions only. Dose–response data are from numbers of calls averaged across minutes 3, 8, 13, and 18 of the session. Cronbach’s alpha = 0.844–0.979 (see text) (PDF 1114 kb)
213_2010_1859_MOESM5_ESM.pdf (99 kb)
Figure S3 Individual differences in call profile across test sessions. The number of flats, step-ups, trills, and flat–trill combinations as a percentage (+SEM) of the total number of calls (i.e. all subtypes) is shown for three singly-tested rats (n = 5 dose levels). Across test sessions, individual rats exhibit higher or lower proportions of the various subtypes compared to other rats. These rats were chosen to illustrate this phenomenon based on clear differences in tendency to emit the four most frequent call categories. (PDF 98 kb)
213_2010_1859_MOESM6_ESM.pdf (418 kb)
Figure S4 Amphetamine dose-dependently increased the proportion of trill calls and suppressed flat calls. The proportion (mean ± SEM) of each call category for singly- and pair-tested rats is plotted against increasing AMPH dose. Note also the overall higher proportion of trills and trills with jumps in the pair-tested rats compared to the singly-tested rats. Caveat: some call categories were emitted very infrequently, namely the upward and downward ramps, the split, and the inverted U. For example, 1% in the saline condition for singly-tested rats corresponds to approximately three calls. Amphetamine-induced changes with respect to flat, short, and trill calls were not significantly group-dependent (Table 1); pooling the two groups (i.e., single and pair-tested), significant differences from the saline condition are indicated by asterisks (*p < 0.05, **p < 0.01, ***p < 0.001, paired t tests, n = 16) (PDF 418 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 197:205–209CrossRefPubMedGoogle Scholar
  2. Blanchard RJ, Blanchard DC, Agullana R, Weiss SM (1991) Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav 50:967–972CrossRefPubMedGoogle Scholar
  3. Blumberg MS (1992) Rodent ultrasonic short calls: locomotion, biomechanics, and communication. J Comp Psychol 106:360–365CrossRefPubMedGoogle Scholar
  4. Blumberg MS, Moltz H (1987) Hypothalamic temperature and the 22 kHz vocalization of the male rat. Physiol Behav 40:637–640CrossRefPubMedGoogle Scholar
  5. Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50:43–50PubMedGoogle Scholar
  6. Brudzynski SM, Chiu EM (1995) Behavioural responses of laboratory rats to playback of 22 kHz ultrasonic calls. Physiol Behav 57:1039–1044CrossRefPubMedGoogle Scholar
  7. Brudzynski SM, Pniak A (2002) Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J Comp Psychol 116:73–82CrossRefPubMedGoogle Scholar
  8. Burgdorf J, Panksepp J (2006) The neurobiology of positive emotions. Neurosci Biobehav Rev 30:173–187CrossRefPubMedGoogle Scholar
  9. Burgdorf J, Knutson B, Panksepp J (2000) Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behav Neurosci 114:320–327CrossRefPubMedGoogle Scholar
  10. Burgdorf J, Knutson B, Panksepp J, Ikemoto S (2001a) Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. Behav Neurosci 115:940–944CrossRefPubMedGoogle Scholar
  11. Burgdorf J, Knutson B, Panksepp J, Shippenberg TS (2001b) Evaluation of rat ultrasonic vocalizations as predictors of the conditioned aversive effects of drugs. Psychopharmacology (Berl) 155:35–42CrossRefGoogle Scholar
  12. Burgdorf J, Panksepp J, Brudzynski SM, Kroes R, Moskal JR (2005) Breeding for 50-kHz positive affective vocalization in rats. Behav Genet 35:67–72CrossRefPubMedGoogle Scholar
  13. 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 182:274–283CrossRefPubMedGoogle Scholar
  14. Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J (2008a) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 122:357–367CrossRefPubMedGoogle Scholar
  15. Burgdorf J, Panksepp J, Brudzynski SM, Beinfeld MC, Cromwell HC, Kroes RA, Moskal JR (2008b) The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Dev Psychobiol 51:34–46CrossRefGoogle Scholar
  16. Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51:667–672CrossRefPubMedGoogle Scholar
  17. Calvino B, Besson JM, Boehrer A, Depaulis A (1996) Ultrasonic vocalization (22–28 kHz) in a model of chronic pain, the arthritic rat: effects of analgesic drugs. Neuroreport 7:581–584CrossRefPubMedGoogle 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 182:284–289CrossRefPubMedGoogle Scholar
  19. 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 123:328–336CrossRefPubMedGoogle Scholar
  20. Fendt M, Schwienbacher I, Schnitzler HU (2006) Carbachol injections into the nucleus accumbens induce 50 kHz calls in rats. Neurosci Lett 401:10–15CrossRefPubMedGoogle Scholar
  21. Fu XW, Brudzynski SM (1994) High-frequency ultrasonic vocalization induced by intracerebral glutamate in rats. Pharmacol Biochem Behav 49:835–841CrossRefPubMedGoogle Scholar
  22. Grilly DM, Loveland A (2001) What is a “low dose” of d-amphetamine for inducing behavioral effects in laboratory rats? Psychopharmacology (Berl) 153:155–169CrossRefGoogle Scholar
  23. Han JS, Bird GC, Li W, Jones J, Neugebauer V (2005) Computerized analysis of audible and ultrasonic vocalizations of rats as a standardized measure of pain-related behavior. J Neurosci Methods 141:261–269CrossRefPubMedGoogle Scholar
  24. Hodgson RA, Guthrie DH, Varty GB (2008) Duration of ultrasonic vocalizations in the isolated rat pup as a behavioral measure: sensitivity to anxiolytic and antidepressant drugs. Pharmacol Biochem Behav 88:341–348CrossRefPubMedGoogle Scholar
  25. Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386CrossRefPubMedGoogle Scholar
  26. Kaltwasser MT (1990) Acoustic signaling in the black rat (Rattus rattus). J Comp Psychol 104:227–232CrossRefPubMedGoogle Scholar
  27. Kaltwasser MT (1991) Acoustic startle induced ultrasonic vocalization in the rat: a novel animal model of anxiety? Behav Brain Res 43:133–137CrossRefPubMedGoogle Scholar
  28. Knutson B, Burgdorf J, Panksepp J (1998) Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol 112:65–73CrossRefPubMedGoogle Scholar
  29. Knutson B, Burgdorf J, Panksepp J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 128:961–977CrossRefPubMedGoogle Scholar
  30. Lin MT, Chandra A, Chern YF, Tsay BL (1980) Effects of intracerebroventricular injection of d-amphetamine on metabolic, respiratory, and vasomotor activities and body temperatures in the rat. Can J Physiol Pharmacol 58:903–908PubMedGoogle Scholar
  31. Litvin Y, Blanchard DC, Blanchard RJ (2007) Rat 22 kHz ultrasonic vocalizations as alarm cries. Behav Brain Res 182:166–172CrossRefPubMedGoogle Scholar
  32. Mallo T, Matrov D, Herm L, Koiv K, Eller M, Rinken A, Harro J (2007) Tickling-induced 50-kHz ultrasonic vocalization is individually stable and predicts behaviour in tests of anxiety and depression in rats. Behav Brain Res 184:57–71CrossRefPubMedGoogle Scholar
  33. Panksepp JB, Jochman KA, Kim JU, Koy JJ, Wilson ED, Chen Q, Wilson CR, Lahvis GP (2007) Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PLoS ONE 2:e351CrossRefPubMedGoogle Scholar
  34. Parsons S (2000) Advantages and disadvantages of techniques for transforming and analyzing chiropteran echolocation calls. J Mammal 81:927–938CrossRefGoogle Scholar
  35. Roberts LH (1975) Evidence for the laryngeal source of ultrasonic and audible cries of rodents. J Zool London 175:243–257CrossRefGoogle Scholar
  36. Sales GD (1972) Ultrasound and mating behaviour in rodents with some observations on other behavioural situations. J Zool London 168:149–164CrossRefGoogle Scholar
  37. Sales GD, Pye D (1974) Ultrasonic communication by animals. Chapman and Hall, LondonGoogle Scholar
  38. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN (2008) Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS ONE 3:e3067CrossRefPubMedGoogle Scholar
  39. Schwarting RK, Jegan N, Wohr M (2007) Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult Wistar rats. Behav Brain Res 182:208–222CrossRefPubMedGoogle Scholar
  40. 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 1–10Google Scholar
  41. Spyraki C, Fibiger HC, Phillips AG (1982) Dopaminergic substrates of amphetamine-induced place preference conditioning. Brain Res 253:185–193CrossRefPubMedGoogle Scholar
  42. Stevenson CW, Goodwin PE, Tunstall B, Spicer CH, Marsden CA, Mason R (2009) Neonatal maternal separation alters reward-related ultrasonic vocalizations in rat dams. Behav Brain Res 200:232–236CrossRefPubMedGoogle Scholar
  43. Thomas DA, Talalas L, Barfield RJ (1981) Effects of devocalization of the male on mating behavior in rats. J Comp Physiol Psychol 95:630–637CrossRefGoogle Scholar
  44. Thomas DA, Takahashi LK, Barfield RJ (1983) Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus). J Comp Psychol 97:201–206CrossRefPubMedGoogle Scholar
  45. 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 168:64–73CrossRefPubMedGoogle Scholar
  46. Ulus IH, Kiran BK, Ozkurt S (1975) Involvement of central dopamine in the hyperthermia in rats produced by d-amphetamine. Pharmacology 13:309–316CrossRefPubMedGoogle Scholar
  47. van der Poel AM, Miczek KA (1991) Long ultrasonic calls in male rats following mating, defeat and aversive stimulation: frequency modulation and bout structure. Behaviour 119:127–142CrossRefGoogle Scholar
  48. Vivian JA, Miczek KA (1993) Morphine attenuates ultrasonic vocalization during agonistic encounters in adult male rats. Psychopharmacology (Berl) 111:367–375CrossRefGoogle Scholar
  49. White NR, Barfield RJ (1990) Effects of male pre-ejaculatory vocalizations on female receptive behavior in the rat (Rattus norvegicus). J Comp Psychol 104:140–146CrossRefPubMedGoogle Scholar
  50. White NR, Cagiano R, Moises AU, Barfield RJ (1990) Changes in mating vocalizations over the ejaculatory series in rats (Rattus norvegicus). J Comp Psychol 104:255–262CrossRefPubMedGoogle Scholar
  51. 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 70:317–323CrossRefPubMedGoogle Scholar
  52. Wohr M, Schwarting RK (2007) Ultrasonic communication in rats: Can playback of 50-kHz Calls induce approach behavior? PLoS ONE 2:e1365CrossRefPubMedGoogle Scholar
  53. 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 94:285–295CrossRefPubMedGoogle Scholar
  54. Wohr M, Houx B, Schwarting RK, Spruijt B (2008) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93:766–776CrossRefPubMedGoogle Scholar
  55. Wohr M, Kehl M, Borta A, Schanzer A, Schwarting RK, Hoglinger GU (2009) New insights into the relationship of neurogenesis and affect: tickling induces hippocampal cell proliferation in rats emitting appetitive 50-kHz ultrasonic vocalizations. Neuroscience 163:1024–1030CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jennifer M. Wright
    • 1
  • Jim C. Gourdon
    • 2
  • Paul B. S. Clarke
    • 1
    • 3
  1. 1.Department of Pharmacology and TherapeuticsMcGill UniversityMontrealCanada
  2. 2.Comparative Medicine and Animal Resources CenterMcGill UniversityMontrealCanada
  3. 3.Center for Studies in Behavioral NeurobiologyConcordia UniversityMontrealCanada

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