Skip to main content

Advertisement

SpringerLink
Log in

Dose-dependent differences in short ultrasonic vocalizations emitted by rats during cocaine self-administration

  • original investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

The motivational impetuses underlying self-administration of cocaine and other drugs of abuse are not fully understood. One emerging factor is affect. Both positive and negative affective states have been hypothesized to influence drug seeking and drug taking. In parallel, it has been posited that the ultrasonic vocalizations (USVs) of Rattus norvegicus provide insight into the animals’ affective reactions. Furthermore, it has been shown that mesolimbic dopamine (DA) plays a key role in cocaine self-administration and in USV production. Thus, affective processing as measured by rodent USVs likely coincides with cocaine self-administration, but to date has not been studied.

Objective

The present study examined USVs in both the negative affective (18–32.99 kHz) and positive affective (38–80 kHz) ranges of rats during self-administration of a low (0.355 mg/kg/infusion) or high (0.71 mg/kg/infusion) dose of cocaine.

Results

USVs in both ranges were observed in both dose groups. Vocalizations of the low-dose animals occurred primarily in the 22-kHz range (18–32.99 kHz), but exhibited shorter durations (10–500 ms) than those traditionally observed for 22-kHz calls in aversive situations. In contrast, USVs of the high-dose group were primarily observed in the 50-kHz frequency range (38–80 kHz), typically associated with appetitive outcomes.

Conclusions

These results provide evidence for the presence of USVs during cocaine self-administration. The observed dose-dependent difference in USVs provides novel support for the view that affect is one potential motivational factor influencing human drug use and relapse behaviors. Rodent USVs may provide a powerful tool for understanding the role of affect in addiction.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

USV:

Ultrasonic vocalization

SD :

Discriminative stimulus

FM:

Frequency-modulated

FF:

Fixed frequency

ITI:

Inter-trial interval

VTA:

Ventral tegmental area

VI:

Variable interval

NAcc:

Nucleus accumbens

DA:

Dopamine

References

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

    Article  PubMed  CAS  Google Scholar 

  • Baker TB, Piper ME, McCarthy DE, Majeskie MR, Fiore MC (2004) Addiction motivation reformulated: an affective processing model of negative reinforcement. Psychol Rev 111:33–51

    Article  PubMed  Google Scholar 

  • Barfield RJ, Thomas DA (1986) The role of ultrasonic vocalizations in the regulation of reproduction in rats. Ann N Y Acad Sci 474:33–43

    Article  PubMed  CAS  Google Scholar 

  • Barros HMT, Miczek KA (1996) Withdrawal from oral cocaine in rats: ultrasonic vocalizations and tactile startle. Psychopharmacology 125:379–384

    Article  PubMed  CAS  Google Scholar 

  • 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 50:967–972

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM (2005) Principles of rat communication: quantitative parameters of ultrasonic calls in rats. Behav Genet 35:85–92

    Article  PubMed  Google Scholar 

  • Brudzynski SM (2008) Communication of adult rats by ultrasonic vocalization: Biological, sociobiological, and neuroscience approaches. ILAR J 50:43–50

    Google Scholar 

  • Brudzynski SM, Holland G (2005) Acoustic characteristics of air-puff induced 22-kHz alarm calls in direct recordings. Neurosci Biobehav Rev 29:1169–1180

    Article  PubMed  Google Scholar 

  • Brudzynski SM, Pniak A (2002) Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J Comp Psychol 116:73–82

    Article  PubMed  Google Scholar 

  • Brudzynski SM, Ociepa D, Bihari F (1991) Comparison between cholinergically and naturally induced ultrasonic vocalization in the rat. J Psychiatry Neurosci 16:221–226

    PubMed  CAS  Google Scholar 

  • Brudzynski SM, Bihari F, Ociepa D, Fu X (1993) Analysis of 22 kHz ultrasonic vocalizations in laboratory rats: long and short calls. Physiol Behav 54:215–221

    Article  PubMed  CAS  Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J (2000) Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behav Neurosci 114:320–327

    Article  PubMed  CAS  Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J, Ikemoto S (2001) Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. Behav Neurosci 115:940–944

    Article  PubMed  CAS  Google Scholar 

  • Childress AR, Ehrman RN, Wang Z, Li Y, Sciortino N, Hakun J et al (2008) Prelude to passion: limbic activation by “unseen” drug and sexual cues. PLoS ONE 3:e1506

    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 

  • Covington HE III, Miczek KA (2003) Vocalizations during withdrawal from opiates and cocaine: possible expressions of affective distress. Eur J Pharmacol 467:1–13

    Article  PubMed  CAS  Google Scholar 

  • Fox HC, Axelrod SR, Paliwal P, Sleeper J, Sinha R (2007) Difficulties in emotion regulation and impulse control during cocaine abstinence. Drug Alcohol Depend 89:298–301

    Article  PubMed  CAS  Google Scholar 

  • Francis RL (1977) 22-kHz calls by isolated rats. Nature 265:236–238

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Brudzynski SM (1994) High-frequency ultrasonic vocalization induced by intracerebral glutamate in rats. Pharmacol Biochem Behav 49:835–841

    Article  PubMed  CAS  Google Scholar 

  • Ghitza UE, Fabbricatore AT, Prokopenko V, Pawlak AP, West MO (2003) Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J Neurosci 23:7239–7245

    PubMed  CAS  Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (1998) Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol 112:65–73

    Article  PubMed  CAS  Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (1999) High frequency ultrasonic vocalizations index conditioned pharmacological reward in rats. Physiol Behav 66:639–643

    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 

  • Koob GF, Moal L (2005) Plasticity of reward neurocircuitry and the ‘dark side’ of drug addiction. Nat Neurosci 8(11):1442–1444

    Article  PubMed  CAS  Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  • Koob GF, Caine B, Markou A, Pulvirenti L, Weiss F (1994) Role for the mesocortical dopamine system in the motivating effects of cocaine. NIDA Res Monogr 145:1–18

    PubMed  CAS  Google Scholar 

  • Mark GP, Hajnal A, Kinney AE, Keys AS (1999) Self-administration of cocaine increases the release of acetylcholine to a greater extent than response-independent cocaine in the nucleus accumbens of rats. Psychopharmacology 143:47–53

    Article  PubMed  CAS  Google Scholar 

  • McKay JR, Rutheford MJ, Alterman AI, Cacciola JS, Kaplan MR (1995) An examination of the cocaine relapse process. Drug Alcohol Depend 38:35–43

    Article  PubMed  CAS  Google Scholar 

  • Mu P, Fuchs T, Saal DB, Sorg BA, Dong Y, Panksepp J (2009) Repeated cocaine exposure induces sensitization of ultrasonic vocalizations in rats. Neurosci Lett 453:31–35

    Article  PubMed  CAS  Google Scholar 

  • Mutschler NH, Miczek KA (1998a) Withdrawal from IV cocaine “binges” in rats: ultrasonic distress calls and startle. Psychopharmacology 135:161–168

    Article  PubMed  CAS  Google Scholar 

  • Mutschler NH, Miczek KA (1998b) Withdrawal from a self-administered or non-contingent cocaine binge: differences in ultrasonic distress vocalizations in rats. Psychopharmacology 136:402–408

    Article  PubMed  CAS  Google Scholar 

  • Nicolaysen LC, Pan H, Justice JB Jr (1988) Extracellular cocaine and dopamine concentrations are linearly related in rat striatum. Brain Res 456:317–323

    Article  PubMed  CAS  Google Scholar 

  • Norman AB, Tsibulsky VL (2006) The compulsion zone: a pharmacological theory of acquired cocaine self-administration. Brain Res 1116:143–152

    Article  PubMed  CAS  Google Scholar 

  • Pettit HO, Justice JB Jr (1991) Effect of dose on cocaine self-administration behavior and dopamine levels in the nucleus accumbens. Brain Res 539:94–102

    Article  PubMed  CAS  Google Scholar 

  • Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 46:28–34

    PubMed  CAS  Google Scholar 

  • Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237:1219–23

    Article  PubMed  CAS  Google Scholar 

  • Root DH, Fabbricatore AT, Barker DJ, Ma S, Pawlak AP, West MO (2009) Evidence for habitual and goal-directed behavior following devaluation of cocaine: a multifaceted interpretation of relapse. PLoS ONE 4:e7170

    Article  PubMed  CAS  Google Scholar 

  • Stuber GD, Roitman MF, Phillips PE, Carelli RM, Wightman RM (2005) Rapid dopamine signaling in the nucleus accumbens during contingent and noncontingent cocaine administration. Neuropsychopharmacol 30:853–63

    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 

  • Tonoue T, Ashida Y, Makino H, Hata H (1986) Inhibition of shock-elicited ultrasonic vocalizations by opioid peptides in the rat: a psychotropic effect. Psychoneuroendocrinology 11:177–184

    Article  PubMed  CAS  Google Scholar 

  • Weiss F, Markou A, Lorang MT, Koob GF (1992) Basal extracellular dopamine levels in the nucleus accumbens are decreased during cocaine withdrawal after unlimited-access self-administration. Brain Res 593:314–318

    Article  PubMed  CAS  Google Scholar 

  • Wheeler RA, Twining RC, Jones JL, Slater JM, Grigson PS, Carelli RM (2008) Behavioral and electrophysiological indices of negative affect predict cocaine self-administration. Neuron 57:774–785

    Article  PubMed  CAS  Google Scholar 

  • Wikler A (1948) Recent progress in research on the neurophysiologic basis of morphine addiction. Am J Psychiatry 105:329–338

    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 

  • Yokel AR, Pickens R (1974) Drug level of d- and l-amphetamine during intravenous self-administration. Psychopharmacologia 34:255–264

    Article  PubMed  CAS  Google Scholar 

  • You Z, Wang B, Zitman D, Wise RA (2008) Acetylcholine release in the mesocorticolimbic dopamine system during cocaine seeking: conditioned and unconditioned contributions to reward and motivation. J Neurosci 28:9021–9029

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Linda King, Thomas Grace Sr., Trishala Parthasarathy, Smruti Patel, Dana Silagi, Alyssa Ames, Mark Kogan, and Karina Gotliboym for their excellent assistance.

Author information

Authors and Affiliations

  1. Department of Psychology, Rutgers University, New Brunswick, NJ, 08903, USA

    David J. Barker, David H. Root, Sisi Ma, Shaili Jha, Laura Megehee, Anthony P. Pawlak & Mark O. West

  2. Department of Psychology, Rutgers University, 152 Frelinghuysen Road, Piscataway, NJ, 08854, USA

    Mark O. West

Authors
  1. David J. Barker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David H. Root
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sisi Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shaili Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laura Megehee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anthony P. Pawlak
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mark O. West
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark O. West.

Additional information

This study was supported by the National Institute on Drug Abuse Grants DA 006886, DA 029873 and DA 026252. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barker, D.J., Root, D.H., Ma, S. et al. Dose-dependent differences in short ultrasonic vocalizations emitted by rats during cocaine self-administration. Psychopharmacology 211, 435–442 (2010). https://doi.org/10.1007/s00213-010-1913-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-010-1913-9

Keywords

Search

Navigation