The modulation of play fighting in rats: Role of the motor cortex

Behavioral Neuroscience

Volumn 121, Issue 1, 2007, Pages 164-176

  Kamitakahara, Holly ^a   Monfils, Marie H ^a,b   Forgie, Margaret L ^a   Kolb, Bryan ^a   Pellis, Sergio M ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Dominance; Motor cortex; Orbital frontal cortex; Play fighting; Social cognition

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; DEFENSE MECHANISM; FEMALE; FIGHTING; MALE; MONITORING; MOTOR CORTEX; NEUROMODULATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PLAY; RAT; SOCIAL BEHAVIOR; SOCIAL STATUS;

AGE FACTORS; AGONISTIC BEHAVIOR; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CONFLICT (PSYCHOLOGY); FEMALE; MALE; MOTOR CORTEX; PLAY AND PLAYTHINGS; RATS; RATS, LONG-EVANS; SEX FACTORS;

EID: 33847308641     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.121.1.164     Document Type: Article

References (90)

1. Adams, N., & Boice, R. (1989). Development of dominance in rats in laboratory and semi-natural environments. Behavioural Processes, 19, 127-142.
2. Aldridge, J. W., & Berridge, K. C. (1998). Coding for serial order by neostriatal neurons: A "natural action" approach to movement sequence. Journal of Neuroscience, 18, 2777-2787.
3. Arakawa, H. (2002). The effects of age and isolation period on two phases of behavioral response to foot shock in isolation-reared rats. Developmental Psychobiology, 41, 15-24.
4. Arakawa, H. (2003). The effects of isolation rearing on open-field behavior in male rats depends on developmental stages. Developmental Psychobiology, 43, 11-19.
5. Berdoy, M., Smith, P., & MacDonald, D. W. (1995). Stability of social status in wild rats: Age and the role of settled dominance. Behaviour, 132, 193-212.
6. Berridge, K. C., & Whishaw, I. Q. (1992). Cortex, striatum and cerebellum: Control of serial order in a grooming sequence. Experimental Brain Research, 90, 275-290.
7. Biben, M. (1998). Squirrel monkey play fighting: Making the case for a cognitive training function for play. In M. Bekoff & J. A. Byers (Eds.), Animal play: Evolutionary, comparative, and ecological aspects (pp. 161-182). Cambridge, England: Cambridge University Press.
8. Blanchard, R. J., & Blanchard, D. C. (1990). The colony model of aggression and defense. In D. A. Dewsbury (Ed.), Contemporary issues in comparative psychology (pp. 410-430). Sunderland, MA: Sinauer.
9. Blanchard, R. J., Blanchard, D. C., Takahashi, L. K., & Kelley, M. J. (1977). Attack and defense behaviour in the albino rat. Animal Behaviour, 25, 622-634.
10. Blanchard, R. J., Flannelly, K. J., & Blanchard, D. C. (1988). Life-span studies of dominance and aggression in established colonies of laboratory rats. Physiology & Behavior, 43, 1-7.
11. Bolles, R. C., & Woods, P. J. (1964). The ontogeny of behavior in the albino rat. Animal Behaviour, 12, 427-441.
12. Burghardt, G. M. (2001). Play: Attributes and neural substrates. In E. M. Blass (Ed.), Handbook of behavioral neurobiology: Vol. 15. Developmental psychobiology, developmental neurobiology and behavioral ecology: Mechanisms and early principles (pp. 317-356). New York: Kluwer Academic/Plenum.
13. Burghardt, G. M. (2005). The genesis of play. Cambridge, MA: MIT Press.
14. Byrd, K. R., & Briner, W. E. (1999). Fighting, nonagonistic social behavior, and exploration in isolation-reared rats. Aggressive Behavior, 25, 211-223.
15. Calhoun, J. B. (1963). The ecology and sociology of the Norway rat. Washington, DC: U.S. Department of Health, Education, and Welfare, Public Health Service.
16. Canadian Council for Animal Care. (1993). Guide to the care and use of experimental animals. Ottawa, Canada: Author.
17. da Silva, N. L., Ferreria, V. N. M., de Padua Gorabrez, A., & Morato, G. S. (1996). Individual housing from weaning modifies the performance of young rats on elevated plus-maze apparatus. Physiology & Behavior, 60, 1391-1396.
18. Einon, D. F., Humphreys, A. P., Chivers, S. M., Field, S., & Naylor, V. (1981). Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Developmental Psychobiology, 14, 343-355.
19. Einon, D. F., & Potegal, M. (1991). Enhanced defense in adult rats deprived of playfighting experience as juveniles. Aggressive Behavior, 17, 27-40.
20. Fagen, R. (1981). Animal play behavior. New York: Oxford University Press.
21. Field, E. F., & Pellis, S. M. (1994). Differential effects of amphetamine on the attack and defense components of play fighting in rats. Physiology & Behavior, 56, 325-330.
22. Flannelly, K., & Lore, R. (1977). The influence of females upon aggression in domesticated male rats (Rattus norvegicus). Animal Behaviour, 25, 654-659.
23. Foroud, A., & Pellis, S. M. (2002). The development of anchoring in the play fighting of rats: Evidence for an adaptive age-reversal in the juvenile phase. International Journal of Comparative Psychology, 15, 11-20.
24. Foroud, A., & Pellis, S. M. (2003). The development of roughness in the play fighting of rats: A Laban Movement Analysis perspective. Developmental Psychobiology, 42, 35-43.
25. Foroud, A., Whishaw, I. Q., & Pellis, S. M. (2004). Experience and cortical control over the pubertal transition to rougher play fighting in rats. Behavioural Brain Research, 149, 69-76.
26. Fox, M. W. (1969). The anatomy of aggression and its ritualization in Canidae: A developmental and comparative study. Behaviour, 35, 242-258.
27. Hikosaka, O. (1998). Neural systems for control of voluntary action: A hypothesis. Advances in Biophysics, 35, 81-102.
28. Hol, T., van den Berg, C. L., van Ree, J. M., & Spruijt, B. M. (1999). Isolation during the play period in infancy decreases adult social interactions in rats. Behavioural Brain Research, 100, 91-97.
29. Kolb, B. (1984). Functions of the frontal cortex of the rat: A comparative review. Brain Research, 320, 65-98.
30. Kolb, B. (1987). Recovery from early cortical damage in rats. I. Differential behavioral and anatomical effects of frontal lesions at different ages of neural maturation. Behavioural Brain Research, 25, 205-220.
31. Kolb, B., Cioe, J., & Whishaw, I. Q. (2000). Is there an optimal age for recovery from motor cortex lesions? I. Behavioral and anatomical sequelae of bilateral motor cortex lesions in rats on postnatal days 1, 10, and in adulthood. Brain Research, 882, 62-74.
32. Kolb, B., & Holmes, C. (1983). Neonatal motor cortex lesions in the rat: Absence of sparing of motor behaviors and impaired spatial learning concurrent with abnormal cerebral morphogenesis. Behavioral Neuroscience, 97, 697-709.
33. Kolb, B., & Whishaw, I. Q. (1989). Plasticity in the neocortex: Mechanisms underlying recovery from early brain damage. Progress in Neurobiology, 32, 235-276.
34. Leyhausen, P. (1979). Cat behavior: The predatory and social behavior of domestic and wild cats. New York: Garland STPM Press.
35. Martin, P., & Caro, T. M. (1985). On the functions of play and its role in behavioural development. Advances in the Study of Behavior, 15, 59-103.
36. Martinez, M., Calvo-Torrent, A., Pico-Alfonso, M. A., & Angeles, M. (1998). Social defeat and subordination as models of social stress in laboratory rodents: A review. Aggressive Behavior, 24, 241-256.
37. Mink, J. W. (1996). The basal ganglia: Focused selection and inhibition of competing motor programs. Progress in Neurobiology, 50, 381-425.
38. Monfils, M. H., Driscoll, I., Danka, D., VandenBerg, P. M., Thomas, N., Kleim, J. A., & Kolb, B. (2005). FGF-2 stimulates functional recovery after neonatal lesions of motor cortex in rats. Neuroscience, 134, 1-8.
39. Moore, C. L. (1985). Development of mammalian sexual behavior. In E. S. Gollin (Ed.), The comparative development of adaptive skills (pp. 19-56). Hillsdale, NJ: Erlbaum.
40. Niesink, R. J. M., & van Ree, J. M. (1982). Short-term isolation increases social interactions of male rats: A parametric analysis. Physiology & Behavior, 29, 819-825.
41. Panksepp, J. (1998). Affective neuroscience. New York: Oxford University Press.
42. Panksepp, J., & Beatty, W. W. (1980). Social deprivation and play in rats. Behavioral and Neural Biology, 30, 197-206.
43. Panksepp, J., Normansell, L., Cox, J. F., & Siviy, S. M. (1994). Effects of neonatal decortication on the social play of juvenile rats. Physiology & Behavior, 56, 429-443.
44. Pellis, S. M. (1988). Agonistic versus amicable targets of attack and defense: Consequences for the origin, function and descriptive classification of play-fighting. Aggressive Behavior, 14, 85-104.
45. Pellis, S. M. (1993). Sex and the evolution of play fighting: A review and a model based on the behavior of muroid rodents. The Journal of Play Theory & Research, 1, 56-77.
46. Pellis, S. M. (2002). Sex differences in play fighting revisited: Traditional and nontraditional mechanisms of sexual differentiation in rats. Archives of Sexual Behavior, 31, 17-26.
47. Pellis, S. M., Castaneda, E., McKenna, M. M., Tran-Nguyen, L. T. L., & Whishaw, I. Q. (1993). The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats. Neuroscience Letters, 158, 13-15.
48. Pellis, S. M., Field, E. F., Smith, L. K., & Pellis, V. C. (1997). Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neuroscience and Biobehavioral Reviews, 21, 105-120.
49. Pellis, S. M., Field, E. F., & Whishaw, I. Q. (1999). The development of a sex-differentiated defensive motor-pattern in rats: A possible role for juvenile experience. Developmental Psychobiology, 35, 156-164.
50. Pellis, S. M., Hastings, E., Shimizu, T., Kamitakahara, H., Komorowska, J., Forgie, M. L., & Kolb, B. (2006). The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and non-playful social contexts. Behavioral Neuroscience, 120, 72-84.
51. Pellis, S. M., & Iwaniuk, A. N. (2004). Evolving a playful brain: A levels of control approach. International Journal of Comparative Psychology, 17, 90-116.
52. Pellis, S. M., & McKenna, M. M. (1992). Intrinsic and extrinsic influences on play fighting in rats: Effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate. Behavioural Brain Research, 50, 135-145.
53. Pellis, S. M., & Pellis, V. C. (1987). Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggressive Behavior, 13, 227-242.
54. Pellis, S. M., & Pellis, V. C. (1988a). Identification of the possible origin of the body target which differentiates play fighting from serious fighting in Syrian golden hamsters Mesocricetus auratus. Aggressive Behavior, 14, 437-449.
55. Pellis, S. M., & Pellis, V. C. (1988b). Play-fighting in the Syrian golden hamster Mesocricetus auratus Waterhouse and its relationship to serious fighting during post-weaning development. Developmental Psychobiology, 21, 323-337.
56. Pellis, S. M., & Pellis, V. C. (1990). Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Developmental Psychobiology, 23, 215-231.
57. Pellis, S. M., & Pellis, V. C. (1991). Role reversal changes during the ontogeny of play fighting in male rats: Attack versus defense. Aggressive Behavior, 17, 179-189.
58. Pellis, S. M., & Pellis, V. C. (1992). Juvenilized play fighting in subordinate male rats. Aggressive Behavior, 18, 449-457.
59. Pellis, S. M., & Pellis, V. C. (1997). The prejuvenile onset of play fighting in laboratory rats (Rattus norvegicus). Developmental Psychobiology, 31, 193-205.
60. Pellis, S. M., & Pellis, V. C. (1998a). The play fighting of rats in comparative perspective: A schema for neurobehavioral analyses. Neuroscience & Biobehavioral Reviews, 23, 87-101.
61. Pellis, S. M., & Pellis, V. C. (1998b). The structure-function interface in the analysis of play fighting. In M. Bekoff & J. A. Byers (Eds.), Animal play: Evolutionary, comparative, and ecological aspects (pp. 115-140). Cambridge, England: Cambridge University Press.
62. Pellis, S. M., & Pellis, V. C. (2006). Play and the development of social engagement: A comparative perspective. In P. J. Marshall & N. A. Fox (Eds.), The development of social engagement: Neurobiological perspectives (pp. 247-274). Oxford, England: Oxford University Press.
63. Pellis, S. M., Pellis, V. C., & Dewsbury, D. A. (1989). Different levels of complexity in the playfighting by muroid rodents appear to result from different levels of intensity of attack and defense. Aggressive Behavior, 15, 297-310.
64. Pellis, S. M., Pellis, V. C., & Foroud, A. (2005). Play fighting: Aggression, affiliation and the development of nuanced social skills. In R. Tremblay, W. W. Hartup, & J. Archer (Eds.), Developmental origins of aggression (pp. 47-62). New York: Guilford Press.
65. Pellis, S. M., Pellis, V. C., & McKenna, M. M. (1993). Some subordinates are more equal than others: Play fighting amongst adult subordinate male rats. Aggressive Behavior, 19, 385-393.
66. Pellis, S. M., Pellis, V. C., & McKenna, M. M. (1994). A feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens. Journal of Comparative Psychology, 108, 68-73.
67. Pellis, S. M., Pellis, V. C., & Whishaw, I. Q. (1992). The role of the cortex in play fighting by rats: Developmental and evolutionary implications. Brain, Behavior, and Evolution, 39, 270-284.
68. Pierce, J. D., Jr., Pellis, V. C., Dewsbury, D. A., & Pellis, S. M. (1991). Targets and tactics of agonistic and precopulatory behavior in montane and prairie voles: Their relationship to juvenile play fighting. Aggressive Behavior, 17, 337-349.
69. Reinhart, C. J., McIntyre, D. C., Metz, G., & Pellis, S. M. (2006). Play fighting between kindling-prone (FAST) and kindling-resistant (SLOW) rats. Journal of Comparative Psychology, 120, 19-30.
70. Reinhart, C. J., McIntyre, D. C., & Pellis, S. M. (2004). The development of play fighting in kindling-prone (FAST) and kindling-resistant (SLOW) rats: How does the retention of phenotypic juvenility affect the complexity of play? Developmental Psychobiology, 45, 83-92.
71. Siviy, S. M. (1998). Neurobiological substrates of play behavior: Glimpses into the structure and function of mammalian playfulness. In M. Bekoff & J. A. Byers (Eds.), Animal play: Evolutionary, comparative, and ecological aspects (pp. 221-242). Cambridge, England: Cambridge University Press.
72. Siviy, S. M., Baliko, C. N., & Bowers, K. S. (1997). Rough-and-tumble play behavior in Fischer-344 and buffalo rats: Effects of social isolation. Physiology & Behavior, 61, 597-602.
73. Siviy, S. M., Love, N. J., DeCicco, B. M., Giordano, S. B., & Seifert, T. L. (2003). The relative playfulness of juvenile Lewis and Fischer-344 rats. Physiology & Behavior, 80, 385-394.
74. Siviy, S. M., & Panksepp, J. (1987). Sensory modulation of juvenile play in rats. Developmental Psychobiology, 20, 29-55.
75. Small, W. S. (1899). Notes on the psychic development of the young white rat. The American Journal of Psychology, 11, 80-100.
76. Smith, L. K., Fantella, S-L., & Pellis, S. M. (1999). Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent. Aggressive Behavior, 25, 141-152.
77. Smith, L. K., Field, E. F., Forgie, M. L., & Pellis, S. M. (1996). Dominance and age-related changes in the play fighting of intact and post-weaning castrated male rats (Rattus norvegicus). Aggressive Behavior, 22, 215-226.
78. Smith, L. K., Forgie, M. L., & Pellis, S. M. (1998a). Mechanisms underlying the absence of the pubertal shift in the playful defense of female rats. Developmental Psychobiology, 33, 147-156.
79. Smith, L. K., Forgie, M. L., & Pellis, S. M. (1998b). The post-pubertal change in the playful defense of male rats depends upon neonatal exposure to gonadal hormones. Physiology & Behavior, 63, 151-155.
80. Spinka, M., Newberry, R. C., & Bekoff, M. (2001). Mammalian play: Can training for the unexpected be fun? Quarterly Review of Biology, 76, 141-176.
81. Symons, D. (1978). Play and aggression: A study of rhesus monkeys. New York: Columbia University Press.
82. Takahashi, L. K. (1986). Postweaning environmental and social factors influence the onset of agonistic behavior in Norway rats. Behavioural Processes, 12, 237-260.
83. Takahashi, L. K., & Lore, R. K. (1982). Intermale and maternal aggression in adult rats tested at different ages. Physiology & Behavior, 29, 1013-1018.
84. Takahashi, L. K., & Lore, R. K. (1983). Play fighting and the development of agonistic behavior in male and female rats. Aggressive Behavior, 9, 217-227.
85. Thor, D. H., & Holloway, W. R., Jr. (1984). Developmental analysis of social play behavior in juvenile rats. Bulletin of the Psychonomic Society, 22, 587-590.
86. van den Berg, C. L., Hol, T., van Ree, J. M., Spruijt, B. M., Everts, H., & Koolhas, J. M. (1999). Play is indispensable for an adequate development of coping with social challenges in the rat. Developmental Psychobiology, 34, 129-138.
87. Vanderschuren, L. F. M., Niesink, R. J. M., & van Ree, J. M. (1997). The neurobiology of social play behavior in rats. Neuroscience and Biobehavioural Reviews, 21, 309-326.
88. von Frijtag, J. C., Schot, M., van den Bos, R., & Spruijt, B. M. (2002). Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. Developmental Psychobiology, 41, 58-69.
89. Whishaw, I. Q., Pellis, S. M., Gorny, B. P., & Pellis, V. C. (1991). The impairments in reaching and the movements of compensation in rats with motor cortex lesions: A video recording and movement notation analysis. Behavioural Brain Research, 42, 77-91.
90. Whishaw, I. Q., & Whishaw, G. E. (1996). Conspecific aggression influences food carrying: Studies on a wild population of Rattus norvegicus. Aggressive Behavior, 22, 47-66.