Rats selectively bred for low levels of 50 kHz ultrasonic vocalizations exhibit alterations in early social motivation

Developmental Psychobiology

Volumn 50, Issue 4, 2008, Pages 322-331

  Harmon, K M ^a   Cromwell, H C ^a   Burgdorf, J ^b   Moskal, J R ^b   Brudzynski, S M ^c   Kroes, R A ^b   Panksepp, J ^a,b,d  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

^b Northwestern University   (United States)

^c BROCK UNIVERSITY   (Canada)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Attachment; Conditioning; Emotion; Reward; Vocalizations

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUTISM; AVERSION; BEHAVIOR DISORDER; BREEDING; COMMUNICATION DISORDER; CONDITIONING; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMOTIONAL ATTACHMENT; EMOTIONALITY; EPIGENETICS; MATERNAL BEHAVIOR; MOTIVATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPIC VARIATION; PLACE PREFERENCE; RAT; REWARD; SOCIAL BEHAVIOR; ULTRASOUND; VOCALIZATION; AFFECT; ANIMAL; ANIMAL COMMUNICATION; FEMALE; GENETIC SELECTION; GENOTYPE; LOCOMOTION; MALE; ODOR; PHENOTYPE; PHYSIOLOGY; SOCIAL ISOLATION;

ANIMALIA; RATTUS;

AFFECT; ANIMAL COMMUNICATION; ANIMALS; CONDITIONING (PSYCHOLOGY); FEMALE; GENOTYPE; LOCOMOTION; MALE; MOTIVATION; ODORS; PHENOTYPE; RATS; REWARD; SELECTION (GENETICS); SOCIAL BEHAVIOR; SOCIAL ISOLATION; ULTRASONICS; VOCALIZATION, ANIMAL;

EID: 48949120027     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20294     Document Type: Article

References (60)

1. Bardo, M. T., & Bevins, R. A. (2000). Conditioned place preference: What does it add to our preclinical understanding of drug reward. Psychopharmacology, 153, 31-43.
2. Barfield, R. J., & Geyer, L. A. (1972). Sexual behavior: Ultrasonic postejaculatory song of the male rat. Science, 176, 1349-1350.
3. Blanchard, R. J., Blanchard, D. C., Agullana, R., & Weiss, S. M. (1991). Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiology and Behavior, 50, 967-972.
4. Blanchard, R. J., Yudko, R. B., Blanchard, D. C., & Taukulis, H. K. (1993). High-frequency (35-70 kHz) ultrasonic vocalizations in rats confronted with anesthetized conspecifics: Effects of gepirone ethanol, and diazepam. Pharmacology, Biochemistry and Behavior, 44, 313-319.
5. Blumberg, M. S., & Alberts, J. R. (1991). On the significance of similarities between ultrasonic vocalizations of infant and adult rats. Neuroscience & Biobehavioral Reviews, 15, 383-390.
6. Blumberg, M. S., & Sokoloff, G. (2000). Do infants cry? Psychological Review, 108, 83-95.
7. Brudzynski, S. M. (2001). Pharmacological and behavioral characteristics of 22 kHz alarm calls in rats. Neuroscience Biobehavioral Review, 25, 611-617.
8. Brudzynski, S. M., Bihara, F., Ociepa, D., & Fu, X. (1993). Analysis of 22 kHz ultrasonic vocalization in laboratory rats: Long and short calls. Physiology and Behavior, 54, 215-221.
9. Brudzynski, S. M., Kehoe, P., & Callahan, M. (1999). Sonographic structure of isolation-induced ultrasonic calls of rat pups. Developmental Psychobiology, 34, 195-204.
10. Brudzynski, S. M., & Pniak, A. (2002). Social contacts and production of 50 kHz short ultrasonic calls in adult rats. Journal of Comparative Psychology, 116, 73-82.
11. Brunelli, S. A. (2005). Selective breeding for an infant phenotype: Rat pup ultrasonic vocalization (USV). Behavior Genetics, 35, 53-65.
12. Brunelli, S. A., Keating, C. C., Hamilton, N. A., & Hofer, M. A. (1996). Development of ultrasonic vocalization responses in genetically heterogeneous National Institute of Health (N: NIH) rats. I. Influence of age, testing experience, and associated factors. Developmental Psychobiology, 29, 507-516.
13. Brunelli, S. A., Vinocur, D. D., Soo Hoo, D., & Hofer, M. A. (1997). Five Generations of selective breeding for ultrasonic vocalization (USV) responses in N: NIH strain rats. Developmental Psychobiology 31, 255-265.
14. Burgdorf, J., & Panksepp, J. (2006). The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews, 30, 173-187.
15. Burgdorf, J., Panksepp, J., Brudzynski, S. M., Kroes, R., & Moskal, J. R. (2005). Breeding for 50-kHz positive affective vocalization in rats. Behavior Genetics, 35, 67-72.
16. Burgdorf, J., Panksepp, J., Kroes, R. A., & Moskal, J. R. (2007). The effect of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Developmental Psychobiology, (in press).
17. Carter, C. S. (2003). Developmental consequences of oxytocin. Physiology & Behavior, 79, 383-397.
18. Cromwell, H. C., Johnson, A., McKnight, L., Horinek, M., Asbrock, C., Burt, S., Jolous-Jamsjidi, C., & Meserve, L. A. (2007). Effects of polychlorinated biphenyls on maternal odor conditioning in rat pups. Physiology & Behavior, 91, 658-666.
19. Costantini, F., & D'Amato, F. R. (2006). Ultrasonic vocalizations in mice and rats: Social contexts and functions. Acta Zoologica Sinica, 52, 619-633.
20. Dichter, G. S., Brunelli, S. A., & Hofer, M. A. (1996). Elevated plus-maze behavior in adult offspring of selectively bred rats. Physiology and Behavior, 60, 299-304.
21. Gammie, S. C. (2005). Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behavior and Cognitive Neuroscience Reviews, 4, 119-135.
22. Harmon, K. M., Burgdorf, J., Moskal, J. R., Kroes, R. A., Panksepp, J., & Cromwell, H. C. (2006). Behavioral phenotyping of rats selectively bred for differential levels of 50 kHz ultrasonic vocalizations. Thirty-Sixth Annual Meeting of the Society for Neuroscience, Atlanta, Georgia, Neuroscience Meeting Planner, Abstract 578.10.
23. Hofer, M. A. (1995). An evolutionary perspective on anxiety. In: S. P. Roose, & R. A. Glick (Eds.), Anxiety as symptom and signal (pp. 17-38). London: Analytic Press.
24. Hofer, M. A. (1996). Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology, 21, 203-217.
25. Hofer, M. A., & Shair, H. N. (1993). Ultrasonic vocalization, laryngeal braking, and thermogenesis in rat pups: A reappraisal. Behavioral Neuroscience, 107, 354-362.
26. Hofer, M. A., Shair, H. N., Masmela, J., & Brunelli, S. A. (2001). Developmental effects of selective breeding for an infantile trait: The rat pup ultrasonic isolation call. Developmental Psychobiology, 39, 231-246.
27. Insel, T. (1997). A neurobiological basis of social attachment. American Journal of Psychiatry, 154, 726-735.
28. Kalin, N. H., Shelton, S. R., & Barksdale, C. M. (1988). Opiate modulation of separation-induced distress in non-human primates. Brain Research, 440, 285-292.
29. Knutson, B., Burgdorf, J., & Panksepp, J. (1998). Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. Journal of Comparative Psychology, 112, 65-73.
30. Knutson, B., Burgdorf, J., & Panksepp, J. (1999). High-frequency ultrasonic vocalizations index conditioned pharmacological rewards in rats. Physiological Behavior, 66, 639-643.
31. Knutson, B., Burgdorf, J., & Panksepp, J. (2002). Ultrasonic vocalizations as indices of affective states in rats. Psychological Bulletin, 128, 961-977.
32. McGinnis, M. Y., & Vakulenko, M. (2003). Characterization of 50-kHz ultrasonic vocalizations in male and female rats. Physiology & Behavior, 80, 81-88.
33. McIntosh, T. K., & Barfield, R. J. (1980). The temporal patterning of 40-60 kHz ultrasonic vocalizations compulation in the rat (Rattus norvegicus). Behavior and Neural Biology, 29, 349-358.
34. Miczek, K. A., Tornatzky, W., & Vivian, J. (1991). Ethology and neuropharmacology: Rodent ultrasounds. In: B. Olivier, & J. Mos (Eds.), Animal models in psychopharmacology (pp. 409-427). Boston: Birkhäuser.
35. Nelson, E., & Panksepp, J. (1996). Oxytocin mediate acquisition of maternally associated odor preferences in preweanling rat pups. Behavioral Neuroscience, 110, 583-592.
36. Nelson, E., & Panksepp, J. (1998). Brain substrates of infant-mother attachment: Contributions of opioids, oxytocin, and norepinephrine. Neuroscience Biobehavioral Review, 22, 437-452.
37. Newman, J. D. (1988). The physiological control of mammalian vocalizations. New York: Plenum.
38. Newman, J. D. (1991). Vocal manifestations of anxiety and their pharmacological control. In: S. E. File (Ed.), Psychopharmacology of anxiolytics and antidepressants (pp 251-260). New York: Pergamon Press.
39. Panksepp, J. (1988). Posterior pituitary hormones and separation distress in chicks. Neuroscience Abstracts, 14, 287.
40. Panksepp, J. (1992). Oxytocin effects on emotional processes: Separation distress, social bonding, and relationships to psychiatric disorders. Annals of the New York Academy of Sciences, 652, 243-252.
41. Panksepp, J. (1998). Affective neuroscience: The foundations of human and animal emotions. New York: Oxford University Press.
42. Panksepp, J. (2003). Can anthropomorphic analyses of "separation cries" in other animals inform us about the emotional nature of social loss in humans? Psychological Reviews, 110, 376-388.
43. Panksepp, J., & Burgdorf, J. (1999). Laughing rats? Playful tickling arouses high frequency ultrasonic chirping in young rodents. In: S. Hameroff, D. Chalmers, & A. Kadzniak (Eds.), Toward a science of consciousness III (pp 231-244). Cambridge, MA: MIT Press.
44. 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. Behavioral Brain Research, 115, 25-38.
45. Panksepp, J., & Burgdorf, J. (2003). "Laughing" rats and the evolutionary antecedents of human joy? Physiology & Behavior, 73, 533-547.
46. Panksepp, J., Gordon, N., & Burgdorf, J. (2002). Empathy and the action-perception resonances of socio-emotional systems of the brain. Behavior Brain Science, 25, 43.
47. Panksepp, J., Herman, B. H., Vilberg, T., Bishop, P., & DeEskinazi, F. G. (1990). Endogenous opioids and social behavior. Neuroscience and Biobehavioral Reviews, 4, 473-487.
48. Panksepp, J., Knutson, B., & Burgdorf, J. (2002). The role of brain emotional systems in addictions: A neuro-evolutionary perspective and new self-report animal model. Addiction, 97, 459-469.
49. Panksepp, J., Normansell, L. A., Herman, B., Bishop, P., & Crepeau, L. (1988). Neural and neurochemical control of the separation distress call. In: J. D. Newman (Ed.), The physiological control of mammalian vocalizations (pp 263-300). New York: Plenum.
50. Panksepp, J., Yates, G., Ikemoto, S., & Nelson, E. (1991). Simple ethological models of depression; social-isolation induced "despair" in chicks and mice. In: B. Olivier, J. Mos, & J. L. Slangen (Eds.), Animal models in psychopharmacology (pp 161-181). Basel: Birkhauser-Verlag.
51. Sales, G. D., & Pye, D. (1974). Ultrasonic communication by animals. London: Chapman & Hall.
52. Shair, H. N., & Jasper, A. (2003). Decreased venous return is neither sufficient nor necessary to elicit ultrasonic vocalizations of infant rat pups. Behavioral Neuroscience, 117, 840-853.
53. Shields, L. E. S., & Brudzynski, S. M. (2007). Ontogenetic development of acoustic features of isolation calls in Wistar rats. Canadian Journal of Neurological Sciences, 34(Suppl. 3), S11.
54. Thomas, D. A., Takahashi, L. K., & Barfield, R. J. (1983). Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus). Journal of Comparative Psychology, 97, 201-206.
55. Tonoue, T., Ashida, Y., Makino, H., & Hata, H. (1996). Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: A psychotropic effect. Psychoneuroendocrinology, 11, 177-184.
56. Tzschentke, T. M. (1998). Measuring reward with the conditioned place preference paradigm: A comprehensive review of drug effects, recent progress, and new issues. Progress in Neurobiology, 56, 613-672.
57. van der Poel, A. M., & Miczek, K. A. (1991). Long ultrasonic calls in male rats following mating, defeat, and aversive stimulation: Frequency modulation and bout structure. Behaviour 119, 127-142.
58. Vivian, J. A., Barros, H. M., Manitiu, A., & Miczek, K. A. (1997). Ultrasonic vocalizations in rat pups: Modulation at the gamma-aminobutyric acid. A receptor complex and the neurosteroid recognition site. Journal of Pharmacology Experiment Therapy, 282, 318-325.
59. Winslow, J. T., Hearn, E. F., Ferguson, J., Young, L. J., Matsuk, M. M., & Insel, T. R. (2000). Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Hormone Behavior, 37, 145-155.
60. Winslow, J. T., & Insel, T. R. (1991). The infant rat separation paradigm: A novel test for novel anxiolytics. Trends in Pharmacological Science, 12, 402-404.