Effects of pre-pubertal social experiences on the responsiveness of juvenile rats to predator odors

Neuroscience and Biobehavioral Reviews

Volumn 32, Issue 7, 2008, Pages 1249-1258

  Siviy, Stephen M ^a  

^a GETTYSBURG COLLEGE   (United States)

Author keywords

Adolescent; Anxiety; Conditioning; Fear; Juvenile; Play; Social; Social buffer

Indexed keywords

ANIMAL EXPERIMENT; CAT; CONTROLLED STUDY; EXPERIENCE; FEAR; MALE; NONHUMAN; PRE PUBERTAL SOCIAL EXPERIENCE; PREDATION; PREDATOR ODOR; PRIORITY JOURNAL; RAT; REVIEW; RISK ASSESSMENT; SPECIES EXTINCTION;

ADAPTATION, PSYCHOLOGICAL; AGE FACTORS; ANIMALS; CATS; CRITICAL PERIOD (PSYCHOLOGY); DISCRIMINATION (PSYCHOLOGY); ESCAPE REACTION; FEAR; MALE; ODORS; RATS; RATS, LONG-EVANS; RISK ASSESSMENT; SMELL; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT;

EID: 50849127826     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2008.05.004     Document Type: Review

References (92)

1. Adamec R.E., Head D., Blundell J., Burton P., and Berton O. Lasting anxiogenic effects of feline predator stress in mice: sex differences in vulnerability to stress and predicting severity of anxiogenic response from the stress experience. Physiology and Behavior 88 (2006) 12-29
2. Adamec R.E., and Shallow T. Lasting effects on rodent anxiety of a single exposure to a cat. Physiology and Behavior 54 (1993) 101-109
3. Adamec R.E., Walling S., and Burton P. Long-lasting, selective, anxiogenic effects of feline predator stress in mice. Physiology and Behavior 54 (2004) 401-410
4. Angulo J.A., Printz D., Ledoux M., and McEwen B.S. Isolation stress increases tyrosine hydroxylase mRNA in the locus coeruleus and midbrain and decreases proenkephalin mRNA in the striatum and nucleus accumbens. Molecular Brain Research 11 (1991) 301-308
5. Anisman H., Zaharia M.D., Meaney M.J., and Merali Z. Do early-life events permanently alter behavioral and hormonal responses to stressors. International Journal of Developmental Neuroscience 16 (1998) 149-164
6. Apfelbach R., Blanchard D.C., Blanchard R.J., Hayes R.A., and McGregor I.S. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neuroscience and Biobehavioral Reviews 29 (2005) 1123-1144
7. Arakawa H. The effects of isolation rearing on open-field behavior in male rats depends on developmental stages. Developmental Psychobiology 43 (2003) 11-19
8. Armario A., Luna G., and Balasch J. The effect of conspecifics on corticoadrenal response of rats to a novel environment. Behavioral and Neural Biology 37 (1983) 332-337
9. Armario A., Ortiz R., and Balasch J. Corticoadrenal and behavioral response to open field in pairs of male rats either familiar or non-familiar to each other. Experientia 39 (1983) 1316-1317
10. Baldwin J.D., and Baldwin J.I. Effects of food ecology on social play: a laboratory simulation. Zeitschrift fur Tierpsychologie 40 (1976) 1-14
11. Blanchard R.J., Blanchard D.C., Rodgers J., and Weiss S.M. The characterization and modeling of antipredator defensive behavior. Neuroscience and Biobehavioral Reviews 14 (1990) 463-472
12. Blanchard D.C., Blanchard R.J., Tom P., and Rodgers R.J. Diazepam changes risk assessment in an anxiety/defense test battery. Psychopharmacology 101 (1990) 511-518
13. Blanchard D.C., Griebel G., Rodgers R.J., and Blanchard R.J. Benzodiazepine and serotonergic modulation of antipredator and conspecific defense. Neuroscience and Biobehavioral Reviews 22 (1998) 597-612
14. Blanchard D.C., Hori K., Rodgers R.J., Hendrie C.A., and Blanchard R.J. Attenuation of defensive threat and attack in wild rats (Rattus rattus) by benzodiazepines. Psychopharmacology 97 (1989) 392-401
15. Blanchard R.J., and Blanchard D.C. Antipredator defensive behaviors in a visible burrow system. Journal of Comparative Psychology 103 (1989) 70-82
16. Blanchard R.J., and Blanchard D.C. Attack and defense in rodents as ethoexperimental models for the study of emotion. Progress in Neuro-Psychopharmacology and Biological Psychiatry 13 (1989) S3-S14
17. Blanchard R.J., Yang M., Li C.-I., Gervacio A., and Blanchard D.C. Cue and context conditioning of defensive behaviors to cat odor stimuli. Neuroscience and Biobehavioral Reviews 25 (2001) 587-595
18. Blanchard R.J., Yudko E.B., Rodgers R.J., and Blanchard D.C. Defense system psychopharmacology: an ethological approach to the pharmacology of fear and anxiety. Behavioural Brain Research 58 (1993) 155-165
19. Boccia M.L., and Pedersen C. Animal models of critical and sensitive periods in social and emotional development. In: Bailey D.B., and Symons F.J. (Eds). Critical Thinking About Critical Periods (2001), Paul H. Brookes Publishing Company, Baltimore 107-127
20. Brunson K.L., Avishai-Eliner S., Hatalski C.G., and Baram T.Z. Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone. Molecular Psychiatry 6 (2001) 647-656
21. Burghardt G.M. The Genesis of Animal Play: Testing the Limits (2005), MIT Press, Cambridge, MA
22. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., and Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Science of the United States of America 95 (1998) 5335-5340
23. Champagne F.A., and Curley J.P. How social experiences influence the brain. Current Opinion in Neurobiology 15 (2005) 704-709
24. Champagne F.A., Francis D.D., Mar A., and Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiology and Behavior 79 (2003) 359-371
25. Champagne F.A., Weaver I.C.G., Diorio J., Sharma S., and Meaney M.J. Natural variations in maternal care are associated with estrogen receptor α expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144 (2003) 4720-4724
26. Davitz J.R., and Mason D.J. Socially facilitated reduction of a fear response in rats. Journal of Comparative and Physiological Psychology 48 (1955) 149-151
27. De Vries A.C., Glasper E.R., and Detillion C.E. Social modulation of stress responses. Physiology and Behavior 79 (2003) 399-407
28. Denenberg V.H., and Karas G.G. Effects of infantile handling upon weight gain and mortality in the rat and mouse. Science 130 (1959) 629-630
29. Dielenberg R.A., Arnold J.C., and McGregor I.S. Low-dose midazolam attenuates predatory odor avoidance in rats. Pharmacology Biochemistry and Behavior 62 (1999) 197-201
30. Dielenberg R.A., Carrive P., and McGregor I.S. The cardiovascular and behavioral response to cat odor in rats: unconditioned and conditioned effects. Brain Research 897 (2001) 228-237
31. Dielenberg R.A., and McGregor I.S. Habituation of the hiding response to cat odor in rats (Rattus norvegicus). Journal of Comparative Psychology 113 (1999) 376-387
32. Dielenberg R.A., and McGregor I.S. Defensive behavior in rats towards predatory odors: a review. Neuroscience and Biobehavioral Reviews 25 (2001) 597-609
33. Doremus T.L., Brunell S.C., Varlinskaya E.I., and Spear L.P. Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats. Pharmacology Biochemistry and Behavior 75 (2003) 411-418
34. Doremus T.L., Varlinskaya E.I., and Spear L.P. Factor analysis of elevated plus-maze behavior in adolescent and adult rats. Pharmacology Biochemistry and Behavior 83 (2006) 570-577
35. Elliott B.M., Faraday M.M., Phillips J.M., and Grunberg N.E. Effects of nicotine on elevated plus maze and locomotor activity in male and female adolescent and adult rats. Pharmacology Biochemistry and Behavior 77 (2004) 21-28
36. Fox N.A., Hane A.A., and Pine D.S. Plasticity for affective neurocircuitry: how the environment affects gene expression. Current Directions in Psychological Science 16 (2007) 1-5
37. Fox N.A., Nichols K.E., Henderson H.A., Rubin K., Schmidt L., Hamer D., Ernst M., and Pine D.S. Evidence for a gene-environment interaction in predicting behavioral inhibition in middle childhood. Psychological Science 16 (2005) 921-926
38. Frisone D.F., Frye C.A., and Zimmerberg B. Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behavioural Brain Research 128 (2002) 153-160
39. Heim C., and Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biological Psychiatry 49 (2001) 1023-1039
40. Hol T., Koolhaas J.M., and Spruijt B.M. Consequences of short term isolation after weaning on later adult behavioural and neuroendocrine reaction to social stress. Behavioural Pharmacology 5 (1994) 88-89
41. Holmes A., le Guisquet A.M., Vogel E., Millstein R.A., Leman S., and Belzung C. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neuroscience and Biobehavioral Reviews 29 (2005) 1335-1346
42. Hubbard D.T., Blanchard D.C., Yang M., Markham C.M., Gervacio A., Chun-I L., and Blanchard R.J. Development of defensive behavior and conditioning to cat odor in the rat. Physiology and Behavior 80 (2004) 525-530
43. Kagan J. Emotional development and psychiatry. Biological Psychiatry 49 (2001) 973-979
44. Kiyokawa Y., Kikusui T., Takeuchi Y., and Mori Y. Partner's stress status influences social buffering effects in rats. Behavioral Neuroscience 118 (2004) 798-804
45. Kiyokawa Y., Takeuchi Y., and Mori Y. Two types of social buffering differentially mitigate conditioned fear responses. European Journal of Neuroscience 26 (2007) 3606-3613
46. Knutson B., Burgdorf J., and Panksepp J. Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. Journal of Comparative Psychology 112 (1998) 65-73
47. Latane B. Gregariousness and fear in laboratory rats. Journal of Experimental Social Psychology 5 (1969) 61-69
48. Laviola G., Adriani W., Terranova M.L., and Gerra G. Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neuroscience and Biobehavioral Reviews 23 (1999) 883-1010
49. Levine S., Alpert M., and Lewis G.W. Infantile experience and the maturation of the pituitary adrenal axis. Science 126 (1957) 1347
50. MacLean P.D. The Triune Brain in Evolution: Role in Paleocerebral Functions (1990), Plenum Press, New York
51. Maughan B., and McCarthy G. Childhood adversities and psychosocial disorders. British Medical Bulletin 53 (1997) 156-169
52. McGregor I.S., Schrama L., Ambermoon P., and Dielenberg R.A. Not all 'predator odours' are equal: cat odour but not 2,4,5-trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behavioural Brain Research 129 (2002) 1-16
53. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 24 (2001) 1161-1192
54. Meaney M.J., Aitken D.H., Bodnoff S.R., Iny L.J., and Sapolsky R.M. The effects of postnatal handling on the development of the glucocorticoid receptor systems and stress recovery in the rat. Progress in Neuro-Psychopharmacology and Biological Psychiatry 9 (1985) 731-734
55. Meaney M.J., Mitchell J.B., Aitken D.H., Bhatnagar S., Bodnoff S.R., Iny L.J., and Sarrieau A. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits later in life. Psychoneuroendocrinology 16 (1991) 85-103
56. Meerlo P., Horvath K.M., Nagy G.M., Bohus B., and Koolhaas J.M. The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. Journal of Neuroendocrinology 11 (1999) 925-933
57. Menard J.L., Champagne D.L., and Meaney M.J. Variations of maternal care differentially influence 'fear' reactivity and regional patterns of cFos immunoreactivity in response to the shock-probe burying test. Neuroscience 129 (2004) 297-308
58. Nemeroff C.B. Early-life adversity, CRF dysregulation, and vulnerability to mood and anxiety disorders. Psychopharmacology Bulletin 38 (2004) 14-20
59. Niesink R.J.M., and Van Ree J.M. Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology 28 (1989) 411-418
60. Panksepp J. Affective Neuroscience: The Foundations of Human and Animal Emotions (1998), Oxford University Press, New York
61. Panksepp J., Siviy S.M., and Normansell L. The psychobiology of play: theoretical and methodological considerations. Neuroscience and Biobehavioral Reviews 8 (1984) 465-492
62. Parent C., Zhang T.-Y., Caldji C., Bagot R., Champagne F.A., Pruessner J., and Meaney M.J. Maternal care and individual differences in defensive responses. Current Directions in Psychological Science 14 (2005) 229-233
63. Pellis S.M., and Pellis V.C. Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neuroscience and Biobehavioral Reviews 23 (1998) 87-101
64. Pellis S.M., and Pellis V.C. Rough-and-tumble play and the development of the social brain. Current Directions in Psychological Science 16 (2007) 95-98
65. Repetti R.L., Taylor S.E., and Seeman T.E. Risky families: family social environments and the mental and physical health of offspring. Psychological Bulletin 128 (2002) 330-366
66. Romeo R.D., Karatsoreos I.N., and McEwen B.S. Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Hormones and Behavior 50 (2006) 463-468
67. Siviy S.M. Neurobiological substrates of play behavior: glimpses into the structure and function of mammalian playfulness. In: Bekoff M., and Byers J.A. (Eds). Animal Play: Evolutionary, Comparative, and Ecological Perspectives (1998), Cambridge University Press, Cambridge 221-242
68. Siviy S.M., and Baliko C.N. A further characterization of alpha-2 adrenoceptor involvement in the rough-and-tumble play of juvenile rats. Developmental Psychobiology 37 (2000) 24-34
69. Siviy S.M., Baliko C.N., and Bowers K.S. Rough-and-tumble play behavior in Fischer-344 and Buffalo rats: effects of social isolation. Physiology and Behavior 61 (1997) 597-602
70. Siviy S.M., and Harrison K.A. Effects of neonatal handling on play behavior and fear towards a predator odor in juvenile rats (Rattus norvegicus). Journal of Comparative Psychology 122 (2008) 1-8
71. Siviy S.M., Harrison K.A., and McGregor I.S. Fear, risk assessment, and playfulness in the juvenile rat. Behavioral Neuroscience 120 (2006) 49-59
72. Siviy S.M., and Panksepp J. Energy balance and juvenile play in rats. Physiology and Behavior 35 (1985) 435-441
73. Siviy S.M., and Panksepp J. Sensory modulation of juvenile play in rats. Developmental Psychobiology 20 (1987) 39-55
74. Slawecki C.J. Comparison of anxiety-like behavior in adolescent and adult Sprague-Dawley rats. Behavioral Neuroscience 119 (2005) 1477-1483
75. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews 24 (2000) 417-463
76. Suomi S.J. Early determinants of behaviour: evidence from primate studies. British Medical Bulletin 53 (1997) 170-184
77. Taylor G.T. Fear and affiliation in domesticated male rats. Journal of Comparative and Physiological Psychology 95 (1981) 685-693
78. Twenge J.M. The age of anxiety? Birth cohort change in anxiety and neuroticism, 1952-1993. Journal of Personality and Social Psychology 79 (2000) 1007-1021
79. Van den Berg C.L., Hol T., Van Ree J.M., Spruijt B.M., Everts H., and Koolhaas J.M. Play is indispensable for an adequate development of coping with social challenges in the rat. Developmental Psychobiology 34 (1999) 129-138
80. Van den Berg C.L., Pijlman F.T.A., Koning H.A.M., Diergaarde L., Van Ree J.M., and Spruijt B.M. Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behavioural Brain Research 106 (1999) 133-142
81. Vanderschuren L.J.M.J., Niesink R.J.M., and Van Ree J.M. The neurobiology of social play behavior in rats. Neuroscience and Biobehavioral Reviews 21 (1997) 3090-3326
82. Varlinskaya E.I., Spear L.P., and Spear N.E. Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiology and Behavior 67 (1999) 475-482
83. Von Frijtag J.C., Schot M., van den Bos R., and Spruijt B.M. Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. Developmental Psychobiology 41 (2002) 58-69
84. Weiss I.C., Pryce C.R., Jongen-Relo A.L., Nanz-Bahr N.I., and Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behavioural Brain Research 152 (2004) 279-295
85. Wiedenmayer C.P., and Barr G.A. Developmental changes in responsivity to threat are stimulus-specific in rats. Developmental Psychobiology 39 (2001) 1-7
86. Williams T.P., and Miller B.D. Pharmacologic management of anxiety disorders in children and adolescents. Current Opinion in Pediatrics 15 (2003) 483-490
87. Wilson J.H. A conspecific attenuates prolactin responses to open-field exposure in rats. Hormones and Behavior 38 (2000) 39-43
88. Wilson J.H. Prolactin in rats is attenuated by conspecific touch in a novel environment. Cognitive, Affective, and Behavioral Neuroscience 1 (2001) 199-205
89. Zangrossi H., and File S.E. Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor. Brain Research Bulletin 29 (1992) 381-388
90. Zangrossi H., and File S.E. Chlordiazepoxide reduces the generalized anxiety, but not the direct responses, of rats exposed to cat odor. Pharmacology Biochemistry and Behavior 43 (1992) 1195-1200
91. Zhang J., Engel J.A., Soderpalm B., and Svensson L. Repeated administration of amphetamine induces sensitization to its disruptive effect on prepulse inhibition in the rat. Psychopharmacology 135 (1998) 401-406
92. Zhang T.Y., Chretien P., Meaney M.J., and Gratton A. Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. The Journal of Neuroscience 25 (2005) 1493-1502