Selective breeding for 50kHz ultrasonic vocalization emission produces alterations in the ontogeny and regulation of rough-and-tumble play

Behavioural Brain Research

Volumn 229, Issue 1, 2012, Pages 138-144

  Webber, E S ^a   Harmon, K M ^a   Beckwith, T J ^a   Pena S ^a   Burgdorf, J ^b   Panksepp, J ^c   Cromwell, H C ^a  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

^b Northwestern University   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Fear conditioning; Predator odor; Rough and tumble play; Selective breeding; Ultrasonic vocalizations; Unconditioned fear

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; AVERSIVE BEHAVIOR; BEHAVIOR CHANGE; BEHAVIOR CONTROL; CAT; CONTROLLED STUDY; CROSS BREEDING; DEVELOPMENTAL STAGE; EMOTIONALITY; FEMALE; INHIBITION (PSYCHOLOGY); INSTRUMENTAL CONDITIONING; INVESTIGATIVE PROCEDURES; MALE; NONHUMAN; ONTOGENY; PHENOTYPE; PLAY; PREDATOR STRESS; PRIORITY JOURNAL; RAT; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; ULTRASONIC VOCALIZATION; AGE; ANIMAL; BREEDING; EMOTION; LONG EVANS RAT; NEWBORN; NONPARAMETRIC TEST; PHYSIOLOGY; RECREATION; REINFORCEMENT; SOCIAL BEHAVIOR; ULTRASOUND; VIDEORECORDING; VOCALIZATION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BREEDING; CATS; EMOTIONS; EXTINCTION, PSYCHOLOGICAL; FEMALE; INHIBITION (PSYCHOLOGY); MALE; PLAY AND PLAYTHINGS; RATS; RATS, LONG-EVANS; SOCIAL BEHAVIOR; STATISTICS, NONPARAMETRIC; ULTRASONICS; VIDEO RECORDING; VOCALIZATION, ANIMAL;

EID: 84856259328     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.01.012     Document Type: Article

References (50)

1. Brudzynski S.M., McCormick C.M., Burgdorf J., Panksepp J., Kroes R., Moskal J.R. Differences in corticosterone response to stress in rats bred for 50kHz vocalization. Abstracts viewer/Itinerary Planner Washington DC Society for Neuroscience 2008, [Abstract].
2. Brunelli S.A. Selective breeding for an infant phenotype: rat pup ultrasonic vocalization (USV). Behavior Genetics 2005, 35(1):53-65. 10.1007/s10519-004-0855-6.
3. Burgdorf J., Knutson B., Panksepp J. Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behavioral Neuroscience 2000, 114(2):320-327.
4. Burman O.H.P., Ilvat A., Jones G., Mendl M. Ultrasonic vocalizations as indicators of welfare of laboratory rats (Rattus norvegicus). Applied Animal Behaviour Science 2007, 104(1-2):116-129.
5. Harmon K.M., Cromwell H.C., Burgdorf J., Moskal J.R., Brudzynski S.M., Kroes R.A., et al. Rats selectively bred for low levels of 50kHz ultrasonic vocalizations exhibit alterations in early social motivation. Developmental Psychobiology 2008, 50(4):322-331. 10.1002/dev.20294.
6. Wintink A.J., Brudzynski S.M. The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats. Pharmacology, Biochemistry, and Behavior 2001, 70(2-3):317-323.
7. Burgdorf J., Knutson B., Panksepp J., Shippenberg T.S. Evaluation of rat ultrasonic vocalizations as predictors of the conditioned aversive effects of drugs. Psychopharmacology 2001, 155(1):35-42.
8. Panksepp J., Burgdorf J. 50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables. Behavioural Brain Research 2000, 115(1):25-38.
9. Panksepp J. Neuroevolutionary sources of laughter and social joy: modeling primal human laughter in laboratory rats. Behavioural Brain Research 2007, 182(2):231-244. 10.1016/j.bbr.2007.02.015.
10. Sales G.D. Ultrasound and aggressive behaviour in rats and other small mammals. Animal Behaviour 1972, 20(1):88-100.
11. Panksepp J., Burgdorf J. Laughing rats and the evolutionary antecedents of human joy?. Physiology and Behavior 2003, 79:533-547. 10.1016/S0031-9384(03)00159-8.
12. Burgdorf J., Wood P.L., Kroes R.A., Moskal J.R., Panksepp J. Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies. Behavioural Brain Research 2007, 182(2):274-283. 10.1016/j.bbr.2007.03.010.
13. Knutson B., Burgdorf J., Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychological Bulletin 2002, 128(6):961-977.
14. Brandao M.L., Borelli K.G., Matos J.M., Oliveira L.C., Nobre M.J. Brainstem mechanisms in anxiety and panic. Focus on brain mapping research 2005, Nova Science Publishers, Inc, New York, NY, p. 137.
15. Kroes R.A., Burgdorf J., Otto N.J., Panksepp J., Moskal J.R. Social defeat, a paradigm of depression in rats that elicits 22-kHz vocalizations, preferentially activates the cholinergic signaling pathway in the periaqueductal gray. Behavioural Brain Research 2007, 182(2):290-300. 10.1016/j.bbr.2007.03.022.
16. Panksepp J. Affective neuroscience: the foundations of human and animal emotions 1998, Oxford University Press, New York.
17. Mällo T., Matrov D., Kõiv K., Harro J. Effect of chronic stress on behavior and cerebral oxidative metabolism in rats with high or low positive affect. Neuroscience 2009, 164(3):963-974. 10.1016/j.neuroscience.2009.08.041.
18. Burgdorf J., Panksepp J., Brudzynski S.M., Kroes R., Moskal J.R. Breeding for 50-kHz positive affective vocalization in rats. Behavior Genetics 2005, 35(1):67-72. 10.1007/s10519-004-0856-5.
19. Burgdorf J., Panksepp J. The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews 2006, 30(2):173-187. 10.1016/j.neubiorev.2005.06.001.
20. Blanchard R.J., Yang M., Li C.I., Gervacio A., Blanchard D.C. Cue and context conditioning of defensive behaviors to cat odor stimuli. Neuroscience and Biobehavioral Reviews 2001, 25(7-8):587-595.
21. Dielenberg R.A., Arnold J.C., McGregor I.S. Low-dose midazolam attenuates predatory odor avoidance in rats. Pharmacology, Biochemistry, and Behavior 1999, 62(2):197-201.
22. Takahashi L.K., Nakashima B.R., Hong H., Watanabe K. The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neuroscience and Biobehavioral Reviews 2005, 29(8):1157-1167. 10.1016/j.neubiorev.2005.04.008.
23. Siviy S.M., Harrison K.A., McGregor I.S. Fear, risk assessment, and playfulness in the juvenile rat. Behavioral Neuroscience 2006, 120(1):49-59. 10.1037/0735-7044.120.1.49.
24. Panksepp J., Siviy S., Normansell L. The psychobiology of play: theoretical and methodological perspectives. Neuroscience and Biobehavioral Reviews 1984, 8(4):465-492.
25. Panksepp J. The ontogeny of play in rats. Developmental Psychobiology 1981, 14(4):327-332. 10.1002/dev.420140405.
26. Burgdorf J., Panksepp J., Brudzynski S.M., Beinfeld M.C., Cromwell H.C., Kroes R.A., et al. The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Developmental Psychobiology 2009, 51(1):34-46. 10.1002/dev.20343.
27. Blanchard R.J., Blanchard D.C., Agullana R., Weiss S.M. Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiology & Behavior 1991, 50(5):967-972. 10.1016/0031-9384(91)90423-L.
28. Choi J.S., Brown T.H. Central amygdala lesions block ultrasonic vocalization and freezing as conditional but not unconditional responses. The Journal of Neuroscience 2003, 23(25):8713-8721.
29. Litvin Y., Blanchard D.C., Blanchard R.J. Rat 22kHz ultrasonic vocalizations as alarm cries. Behavioural Brain Research 2007, 182(2):166-172. 10.1016/j.bbr.2006.11.038.
30. Schwarting R.K.W., Jegan N., Wöhr M. Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult wistar rats. Behavioural Brain Research 2007, 182(2):208-222. 10.1016/j.bbr.2007.01.029.
31. Wohr M., Schwarting R.K. Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior?. PloS One 2007, 2(12):e1365. 10.1371/journal.pone.0001365.
32. Wohr M., Houx B., Schwarting R.K., Spruijt B. Effects of experience and context on 50-kHz vocalizations in rats. Physiology & Behavior 2008, 93(4-5):766-776. 10.1016/j.physbeh.2007.11.031.
33. Knutson B., Burgdorf J., Panksepp J. Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. Journal of Comparative Psychology (Washington, D.C.: 1983) 1998, 112(1):65-73.
34. Panksepp J., Burgdorf J. Laughing rats? Playful tickling arouses high frequency ultrasonic chirping in young rodents. Toward a Science of Consciousness 1999, III:231-244.
35. Pellis S.M., Pellis V.C. Locomotor-rotational movements in the ontogeny and play of the laboratory rat Rattus norvegicus. Developmental Psychobiology 1983, 16(4):269-286. 10.1002/dev.420160403.
36. Shimozuru M., Kikusui T., Takeuchi Y., Mori Y. Effects of isolation-rearing on the development of social behaviors in male mongolian gerbils (Meriones unguiculatus). Physiology & Behavior 2008, 94(3):491-500. 10.1016/j.physbeh.2008.03.003.
37. van den Berg C.L., Hol T., Van Ree J.M., Spruijt B.M., Everts H., Koolhaas J.M. Play is indispensable for an adequate development of coping with social challenges in the rat. Developmental Psychobiology 1999, 34(2):129-138.
38. Pellis S.M., Pellis V.C. Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Developmental Psychobiology 1990, 23(3):215-231. 10.1002/dev.420230303.
39. Pellis S.M., McKenna M. What do rats find rewarding in play fighting?-an analysis using drug-induced non-playful partners. Behavioural Brain Research 1995, 68(1):65-73.
40. Satterlee D.G., Marin R.H., Jonest R.B. Selection of Japanese quail for reduced adrenocortical responsiveness accelerates puberty in males. Poultry Science 2002, 81(7):1071-1076.
41. Kornblum S., Hasbroucq T., Osman A. Dimensional overlap: cognitive basis for stimulus-response compatibility-a model and taxonomy. Psychological Review 1990, 97(2):253-270.
42. Toates F. The interaction of cognitive and stimulus-response processes in the control of behaviour. Neuroscience and Biobehavioral Reviews 1998, 22(1):59-83.
43. Wöhr M., Borta A., Schwarting R.K.W. Overt behavior and ultrasonic vocalization in a fear conditioning paradigm: a dose-response study in the rat. Neurobiology of Learning and Memory 2005, 84(3):228-240. 10.1016/j.nlm.2005.07.004.
44. Bandler R., Keay K.A. Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. Progress in Brain Research 1996, 107:285-300.
45. Leman S., Dielenberg R.A., Carrive P. Effect of dorsal periaqueductal gray lesion on cardiovascular and behavioural responses to contextual conditioned fear in rats. Behavioural Brain Research 2003, 143(2):169-176. 10.1016/S0166-4328(03)00033-0.
46. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 2002, 26(3):321-352.
47. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 2006, 142(1):1-20. 10.1016/j.neuroscience.2006.06.027.
48. Davis M. Animal models of anxiety based on classical conditioning: the conditioned emotional response (CER) and the fear-potentiated startle effect. Pharmacology & Therapeutics 1990, 47(2):147-165.
49. LeDoux J.E. The emotional brain: the mysterious underpinnings of emotional life 1996, Simon & Schuster, New York.
50. Panksepp J. Toward a cross-species neuroscientific understanding of the affective mind: do animals have emotional feelings?. American Journal of Primatology 2011, 73(6):545-561. 10.1002/ajp.20929.