Advertisement

Psychopharmacology

, Volume 114, Issue 3, pp 441–448 | Cite as

Ultrasounds emitted by female rats during agonistic interactions: effects of morphine and naltrexone

  • Margaret Haney
  • Klaus A. Miczek
Original Investigations

Abstract

Ultrasonic vocalizations may be an expression of the affective pain response in laboratory rodents. The present experiment compared morphine's effects on high (33–60 kHz) and low (20–32 kHz) frequency ultrasonic vocalizations to its effects on a range of unconditioned behavioral responses to aversive stimuli; the influence of estrous cyclicity on morphine sensitivity was also investigated. In experiment 1, naive female Long-Evans rats, selected during estrus or diestrus, received cumulative morphine (1, 3, 6, 10 mg/kg SC) or saline, and in experiment 2, rats were pretreated with naltrexone (0.1 mg/kg IP) 5 min before morphine (17, 30, 60, 100 mg/kg SC). The following endpoints were measured 20–25 min post-injection: (1) tail flick latency; (2) ultrasonic and audible vocalizations; (3) the behavioral response to aggressive attack; and (4) locomotor activity. Following a brief exposure to an attack, rats were threatened by an aggressor but protected from further attack by a wire mesh cage (30×21.5×20 cm), thereby allowing for continued behavioral and vocal measurement without the risk of physical injury; video and audio recordings were made of the attack encounter and a subset of the protected encounter (1 min). The endpoint most potently and specifically modulated by morphine was high frequency ultrasounds. The rate of high frequency calling varied as a function of the estrous cycle, supporting gonadal hormone modulation of ultrasonic vocalizations. Low frequency ultrasounds, by contrast, were relatively insensitive to opiate manipulation and were less influenced by estrous cyclicity. High frequency vocalizations may be a more sensitive indication of the affective response to an attacking conspecific than low frequency calls. The attenuation of high frequency ultrasonic calls at doses that do not affect any other behavioral or vocal responses may correspond to human descriptions of morphine analgesia, in which the affective component to pain is more potently modulated than the sensory component.

Key words

Ultrasound Rats Morphine Naltrexone Aggression Pain Opiate Defense 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bandler R (1988) Brain mechanisms of aggression as revealed by electrical and chemical stimulation: suggestion of a central role for the midbrain periaqueductal grey region. In: Epstein AN, Morrison AR (eds) Progress in psychobiology and physiological psychology. Academic Press, New York, pp 67–154Google Scholar
  2. Beatty WW, Fessler RG (1976) Ontogeny of sex differences in open-field behavior and sensitivity to electric shock in the rat. Physiol Behav 16:413–417Google Scholar
  3. Beatty WW, Fessler RG (1977) Gonadectomy and sensitivity to electric shock in the rat. Physiol Behav 19:1–6Google Scholar
  4. Berg DS, Baenninger R (1973) Hissing by laboratory rats during fighting encounters. Behav Biol 8:733–741Google Scholar
  5. Blanchard DC, Blanchard RJ, Rodgers RJ (1990) Pharmacological and neural control of anti-predator defense in the rat. Aggress Behav 16:165–175Google Scholar
  6. Blanchard RJ, Blanchard DC, Agullana R, Weiss S (1991a) Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav 50:967–972Google Scholar
  7. Blanchard DC, Weatherspoon A, Shepherd J, Rodgers RJ, Weiss SM, Blanchard RJ (1991b) “Paradoxical” effects of morphine on antipredator defense reactions in wild and laboratory rats. Pharmacol Biochem Behav 40:819–828Google Scholar
  8. Blanchard RJ, Agullana R, McGee L, Weiss S, Blanchard DC (1992a) Sex differences in the incidence and sonographic characteristics of antipredator ultrasonic cries in the laboratory rat (Rattus norvegicus). J Comp Psychol 106:270–277Google Scholar
  9. Blanchard RJ, Weiss SM, Yudko EB, Taukulis HK (1992b) Social encounters with conspecifics elicit selective high frequency (35–70 kHz) ultrasonic vocalizations in rats. Soc Neurosci Abstr 18:872Google Scholar
  10. Blumberg MS (1992) Ultrasonic short calls: locomotion, biomechanics and communication. J Comp Psychol 106:360–365Google Scholar
  11. Bornschein RL, Crockett RS, Smith RP (1977) Diurnal variations in the analgesic effectiveness of morphine in mice. Pharmacol Biochem Behav 6:621–626Google Scholar
  12. Brudzynski SM, Ociepa D (1992) Ultrasonic vocalization of laboratory rats in response to handling and touch. Physiol Behav 52:655–660Google Scholar
  13. Candido J, Lutfy K, Billings B, Sierra V, Duttaroy A, Inturrisi CE, Yoburn BC (1992) Effect of adrenal and sex hormones on opioid analgesia and receptor regulation. Pharmacol Biochem Behav 42:685–692Google Scholar
  14. Cuomo V, Cagiano R, Desalvia MA, Restani P, Galimberti R, Racagni G, Galli CL (1988) Ultrasonic vocalization in rat pups as a marker of behavioral development: an investigation of the effects of drugs influencing brain opioid systems. Neurotoxicol Teratol 10:465–469Google Scholar
  15. D'Amour F, Smith D (1941) A method for determining loss of pain sensation. J Pharmacol Exp Ther 72:74–79Google Scholar
  16. Depaulis A, Keay K, Bandler R (1992) Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp Brain Res 90:307–318Google Scholar
  17. Dewey WL, Harris LS (1975) The tail-flick test. In: Neidle A, Ehrenpress S (eds) Methods in narcotics research. Dekker, New York, pp 101–109Google Scholar
  18. Floody OR, Pfaff DW (1977) Communication among hamsters by high-frequency acoustic signals: I. Physical characteristics of hamster calls. J Comp Physiol Psychol 91:794–806Google Scholar
  19. Franklin KBJ (1989) Analgesia and the neural substrate of reward. Neurosci Biobehav Rev 18:149–154Google Scholar
  20. Haney M, Miczek KA (1993) Ultrasounds during agonistic interactions between female rats (Rattus norvegicus). J Comp Psychol (in press)Google Scholar
  21. Innes DG, Kavaliers M (1987) Opiates and deer mouse behavior: differences between island and mainland populations. Can J Zool 65:2504–2512Google Scholar
  22. Jürgens U, Pratt R (1979) Role of the periaqueductal gray in vocal expression of emotion. Brain Res 167:367–378Google Scholar
  23. Kafka MS, Wirz-Justice A, Naber D, Moore RY, Benedito MA (1983) Circadian rhythms in rat brain neurotransmitter receptors. Fed Proc 42:2796–2801Google Scholar
  24. Kaltwasser MT (1990) Acoustic signaling in the black rat (Rattus rattus). J Comp Psychol 104:227–232Google Scholar
  25. Kasson BG, George R (1984) Endocrine influences on the actions of morphine IV. Effects of sex and strain. Life Sci 34:1627–1634Google Scholar
  26. Kepler KL, Kest B, Kiefel JM, Cooper ML, Bodnar RJ (1989) Roles of gender, gonadectomy and estrous phase in the analgesic effects of intraventricular morphine in rats. Pharmacol Biochem Behav 34:119–127Google Scholar
  27. Kepler KL, Standifer KM, Paul D, Kest B, Pasternak GW, Bodnar RJ (1991) Gender effects and central opioid analgesia. Pain 45:87–94Google Scholar
  28. King FA (1986) Philosophical and practical issues in animal research involving pain and stress. Ann NY Acad Sci 467:405–409Google Scholar
  29. Kirk RE (1982) Experimental design. Wadsworth, Belmont, Ca., pp 95–97Google Scholar
  30. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson HJ (1988) Anatomy of CNS opioid receptors. Trends Neurosci 7:308–314Google Scholar
  31. Miczek KA (1982) Ethological analysis of drug action on aggression, defense and defect. In: Spiegelstein Y, Levy A (eds) Behavioral models and the analysis of drug action. Amsterdam: Elsevier, pp 225–239Google Scholar
  32. Miczek KA, Vivian JA (1993) Automatic quantification of withdrawal from 5-day diazepam in rats: ultrasonic distress vocalizations and hyperreflexia to acoustic startle stimuli. Psychopharmacology 110:379–382Google Scholar
  33. Miczek KA, Tornatzky W, Vivian J (1991) Ethology and neuropharmacology: rodent ultrasounds. In: Olivier B, Mos J, Slangen J (eds) Animal models in psychopharmacology: advances in pharmacological sciences. Birkhauser, Basel, pp 409–427Google Scholar
  34. Miczek KA, Weerts EM, Tornatzky W, DeBold JF, Vatne TM (1992) Alcohol and “bursts” of aggressive behavior: ethological analysis of individual differences in rats. Psychopharmacology 107:551–563Google Scholar
  35. Nyby J, Whitney G (1978) Ultrasonic communication of adult myomorph rodents. Neurosci Biobehav Rev 2:1–14Google Scholar
  36. Sales GD (1972) Ultrasound and aggressive behavior in rats and other small mammals. Anim Behav 20:88–100Google Scholar
  37. Schmauss C (1987) Spinal k-opioid receptor-mediated antinociception is stimulus-specific. Eur J Pharmacol 137:197–205Google Scholar
  38. Schmauss C, Yaksh TL (1984) In vivo studies on spinal opiate receptor systems mediating antinociception. II. Pharmacological profiles suggesting a differential association of mu, delta and kappa receptors with visceral chemical and cutaneous thermal stimuli in the rat. J Pharmacol Exp Ther 228:1–12Google Scholar
  39. Shepherd JK, Blanchard DC, Weiss SM, Rodgers RJ, Blanchard RJ (1992) Morphine attenuates antipredator ultrasonic vocalizations in mixed-sex rat colonies. Pharmacol Biochem Behav 41:551–558Google Scholar
  40. Sewell GD (1967) Ultrasound in adult rodents. Nature 215:512Google Scholar
  41. Takahashi LK, Thomas DA, Barfield R (1983) Analysis of ultrasonic vocalizations emitted by residents during aggressive encounters among rats (Rattus norvegicus). J Comp Psychol 97:207–212Google Scholar
  42. Tallarida RJ, Murray RB (1987) Manual of pharmacologic calculations with computer programs. Springer, New York, pp 19–22, 153–159Google Scholar
  43. Thomas DA, Takahashi LK, Barfield RJ (1983) Analysis of ultrasonic vocalization emitted by intruders during aggressive encounters among rats (Rattus norvegicus). J Comp Psychol 97:201–206Google Scholar
  44. Tonoue T, Ashida Y, Makinott H, Hata H (1986) Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: a psychotropic effect. Psychoneuroendocrinology 11:177–184Google Scholar
  45. 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 119:127–142Google Scholar
  46. Van der Poel AM, Noach EJK, Miczek KA (1989) Temporal patterning of ultrasonic distress calls in the adult rat: effects of morphine and benzodiazepines. Psychopharmacology 97:147–148Google Scholar
  47. Vivian JA, Miczek KA (1991) Ultrasounds during morphine withdrawal in rats. Psychopharmacology 104:187–193Google Scholar
  48. Vivian JA, Miczek KA (1993a) Morphine attenuates ultrasonic vocalizations during agonistic encounters in adult rats. Psychopharmacology 111:66–73Google Scholar
  49. Vivian JA, Miczek KA (1993b) Diazepam and gepirone selectively attenuate either 20–32 or 32–64 kHz ultrasonic vocalizations during aggressive encounters. Psychopharmacology 112:66–73Google Scholar
  50. Wenger GR (1980) Cumulative dose-response curves in behavioral pharmacology. Pharmacol Biochem Behav 13:647–651Google Scholar
  51. Wetzel DM, Kelley DB, Campbell BA (1980) Central control of ultrasonic vocalizations in neonatal rats: I. Brain stem motor nuclei. J Comp Physiol Psychol 94:596–605Google Scholar
  52. Wikler A (1950) Sites and mechanisms of action of morphine and related drugs in the central nervous system. Pharmacol Rev 2:435–506Google Scholar
  53. Wilkinson LO, Dourish CT (1991) Serotonin and animal behavior. In: Peroutka SR (ed) Serotonin receptor subtypes: basic and clinical aspects. Wiley-Liss, New York, pp 147–210Google Scholar
  54. Yajima Y, Hayashi Y, Yoshii N (1980) The midbrain central gray substance as a highly sensitive neural structure for the production of ultrasonic vocalization in the rat. Brain Res 198:446–452Google Scholar
  55. Yaksh TL, Rudy TA (1978) Narcotic analgetics: CNS sites and mechanisms of action as revealed by intracerebral injection techniques. Pain 4:299–359Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Margaret Haney
    • 1
  • Klaus A. Miczek
    • 1
  1. 1.Department of PsychologyTufts UniversityMedfordUSA

Personalised recommendations