Ameliorative effects of brief daily periods of social interaction on isolation-induced behavioral and hormonal alterations

Physiology and Behavior

Volumn 116-117, Issue , 2013, Pages 13-22

  Raz, Sivan ^a,b  

^a THE MAX STERN YEZREEL VALLEY COLLEGE   (Israel)

^b TEL HAI COLLEGE   (Israel)

Author keywords

Behavioral alterations; Brief social interaction; Corticosterone; Social isolation

Indexed keywords

CORTICOSTERONE; SUCROSE;

ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL HOUSING; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR CHANGE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EVOKED AUDITORY RESPONSE; FOOD PREFERENCE; HORMONAL REGULATION; LEARNING; MALE; NONHUMAN; OPEN FIELD TEST; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; SOCIAL INTERACTION; SOCIAL ISOLATION; STARTLE REFLEX; TASK PERFORMANCE;

EID: 84876310771     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.03.009     Document Type: Article

References (100)

1. Lukkes J.L., Watt M.J., Lowry C.A., Forster G.L. Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front Behav Neurosci 2009, 3:1-12.
2. Garattini S., Valzelli L. Is the isolated animal a possible model for phobia and anxiety?. Prog Neuropsychopharmacol 1981, 5:159-165.
3. Pryce C.R., Rüedi-Bettschen D., Dettling A.C., Weston A., Russig H., Ferger B., et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev 2005, 29:649-674.
4. Geyer M.A., Moghaddam B. Animal models relevant to schizophrenia disorders. Neuropsychopharmacology: the fifth generation of progress 2002, 689-701. Lippincott Williams and Wilkins, Philadelphia. K.L. Davis, D.S. Charney, J.T. Coyle, C. Nemeroff (Eds.).
5. Lu L., Shepard J.D., Hall F.S., Shaham Y. Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 2003, 27:457-491.
6. Brain P., Benton D. The interpretation of physiological correlates of differential housing in laboratory rats. Life Sci 1979, 24:99-115.
7. Hall F.S. Social deprivation of neonatal, adolescent and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 1998, 12:129-162.
8. Valzelli L., Garattini S. Biochemical and behavioural changes induced by isolation in rats. Neuropharmacology 1972, 11:17-22.
9. Bakshi V.P., Geyer M.A. Ontogeny of isolation rearing-induced deficits in sensorimotor gating in rats. Physiol Behav 1999, 67:385-392.
10. Domeney A., Feldon J. The disruption of prepulse inhibition by social isolation in the Wistar rat: how robust is the effect?. Pharmacol Biochem Behav 1998, 59:883-890.
11. Wilkinson L.S., Killcross S.S., Humby T., Hall F.S., Geyer M.A., Robbins T.W. Social isolation in the rat produces developmentally specific deficits in prepulse inhibition of the acoustic startle response without disrupting latent inhibition. Neuropsychopharmacology 1994, 10:61-72.
12. Brenes J.C., Rodriguez O., Fornaguera J. Differential effect of environmental enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacol Biochem Behav 2008, 89:85-93.
13. Brenes Sáenz J.C., Villagra O.R., Fornaguera Trías J. Factor analysis of forced swimming test, sucrose preference test and open field test on enriched, social and isolated reared rats. Behav Brain Res 2008, 169:57-65.
14. Hall F.S., Humby T., Wilkinson L.S., Robbins T.W. The effects of isolation-rearing on preference by rats for a novel environment. Physiol Behav 1997, 62:299-303.
15. Nunes Mamede Rosa M.L., Nobre M.J., Ribeiro Oliveira A., Brandao M.L. Isolation-induced changes in ultrasonic vocalization, fear-potentiated startle and prepulse inhibition in rats. Neuropsychobiology 2005, 51:248-255.
16. Serra M., Pisu M.G., Mostallino M.C., Sanna E., Biggio G. Changes in neuroactive steroid content during social isolation stress modulates GABAA receptor plasticity and function. Brain Res Rev 2007, 57:520-530.
17. Weiss I.C., Pryce C.R., Jongen-Relo A.L., Nanz-Bahr N.I., Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 2004, 152:279-295.
18. Whittaker-Azmitia P., Zhou F., Hobin J., Borella A. Isolation-rearing of rats produces deficit as adults in the serotonergic innervation of hippocampus. Peptides 2000, 21:1755-1759.
19. Hall S.F., Perona M.T.G. Have studies of the developmental regulation of behavioral phenotypes revealed the mechanisms of gene-environment interactions?. Physiol Behav 2012, 107:623-640.
20. Thorsell A., Slawecki C.J., El Khoury A., Mathe A.A., Ehlers C.L. The effects of social isolation on neuropeptide Y levels, exploratory and anxiety-related behaviors in rats. Pharmacol Biochem Behav 2006, 83:28-34.
21. Arakawa H. The effects of isolation rearing on open-field behavior in male rats depends on developmental stages. Dev Psychobiol 2003, 43:11-19.
22. Grippo A.J., Lamb D.G., Carter C.S., Porges S.W. Social isolation disrupts autonomic regulation of the heart and influences negative affective behaviors. Biol Psychiatry 2007, 62:1162-1170.
23. Westenbroek C., Snijders T.A.B., den Boer J.A., Gerrits M., Fokkema D.S., Ter Host G.R. Pair-housing of male and female rats during chronic stress exposure results in gender-specific behavioral responses. Horm Behav 2005, 47:620-628.
24. Willner P. The validity of animal models of depression. Psychopharmacol 1984, 83:1-16.
25. Ahmed S.H., Stinus L., Le Moal M., Cador M. Social deprivation enhances the vulnerability of male Wistar rats to stressor- and amphetamine-induced behavioral sensitization. Psychopharmacology 1995, 117:116-124.
26. Barrot M., Wallace D.L., Bolan C.A., Graham D.L., Perrotti L.I., Neve R.L., et al. Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. PNAS 2005, 102:8357-8362.
27. Maisonnette S., Morato S., Brandao M.L. Role of resocialization and of 5HT1A receptor activation on the anxiogenic effects induced by isolation in the elevated plus-maze test. Physiol Behav 1993, 54:573-578.
28. Jankowska E., Pucilowski O., Kostowski W. Chronic oral treatment with diltiazem or verapamil decreases isolation-induced activity impairment in elevated plus maze. Behav Brain Res 1991, 43:15-18.
29. Miachon S., Jouvenet M., Vallon J.J. Cholesterol and triglyceride levels in the serum of muricidal male Wistar rats: indices of mitochondrial benzodiazepine receptors?. Brain Res Bull 2000, 51:57-61.
30. Rilke O., Will K., Jaehkel M., Oehler J. Behavioral and neurochemical effects of anpirtoline and citalopram in isolated and group housed mice. Prog Neuropsychopharmacol Biol Psychiatry 2001, 25:1125-1144.
31. Schuster R., Berger B.D., Swanson H.H. Cooperative social coordination and aggression: II. Effects of sex and housing among three strains of intact laboratory rats differing in aggressiveness. Q J Exp Psychol B 1993, 46:367-390.
32. Swanson H.H., Schuster R. Cooperative social coordination and aggression in male laboratory rats: effects of housing and testosterone. Horm Behav 1987, 21:310-330.
33. Valzelli L. Aggression in rats and mice, behavioral and biochemical aspects. Actual Pharmacol 1971, 24:133-152.
34. Willner P., Sampson D., Phillips G., Fichera R., Foxlow P., Muscat R. Effects of isolated housing and chronic antidepressant treatment on cooperative social behaviour in rats. Behav Pharmacol 1989, 1:85-90.
35. Malkesman O., Maayan R., Weizman A., Weller A. Aggressive behavior and HPA axis hormones after social isolation in adult rats of two different genetic animal models for depression. Behav Brain Res 2006, 175:408-414.
36. Gadek-Michalska A., Boryez J., Bugajski J. Effect of social isolation on corticosterone secretion elicited by histaminergic stimulation. Agents Actions 1994, 41:77-79.
37. Nagaraja H.S., Jeganathan P.S. Influence of different types of stress on selected cardiovascular parameters in rats. Indian J Physiol Pharmacol 1999, 43:296-304.
38. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006, 9:526-533.
39. Wright R.C., Ingenito A.J. Blockade of dorsal hippocampal kappa-opioid receptors increases blood pressure in normotensive and isolation-induced hypertensive rats. Neuropeptides 2003, 37:127-132.
40. Miura H., Qiao H., Kitagami T., Ohta T., Ozaki N. Effects of fluvoxamine on levels of dopamine, serotonin, and their metabolites in the hippocampus elicited by isolation housing and novelty stress in adult rats. Int J Neurosci 2005, 115:367-378.
41. Nilsson M., Perfilieva E., Johansson U., Orwar O. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. Dev Neurobiol 1999, 39:569-578.
42. Deroche V., Piazza P.V., Le Moal M., Simon H. Social isolation-induced enhancement of the psychomotor effects of morphine depends on corticosterone secretion. Brain Res 1994, 640:136-139.
43. Van den Berg C.L., Pijlman F.T.L., Koning H.A.M., Diergaarde L., Van Ree J.M., Spruijt B.M. Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behav Brain Res 1999, 106:133-142.
44. Doremus T.L., Brunell S.C., Rajendran P., Spear L.P. Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 2005, 29:1796-1808.
45. Wolffgramm J. Free choice ethanol intake of laboratory rats under different social conditions. Psychopharmacology 1990, 101:233-239.
46. Cheeta S., Irvine E., File S.E. Social isolation modifies nicotine's effects in animal tests of anxiety. Br J Pharmacol 2001, 132:1389-1395.
47. Raz S., Berger B.D. Social isolation increases morphine intake: behavioral and psychopharmacological aspects. Behav Pharmacol 2010, 39:21-46.
48. Einon D.F., Morgan M.J., Kibbler C.C. Brief periods of socialization and later behavior in the rat. Dev Psychobiol 1978, 11:213-225.
49. Berger B.D., Schuster R. Pharmacological aspects of social cooperation. Ethopharmacology of agonistic behavior in animals and humans 1987, 14-32. Martinus Nijhoff publishers. B. Olivier, J. Mos, P.F. Brain (Eds.).
50. Schuster R., Berger B.D. An animal model for studying the behavior of cooperating. Tasks and techniques: a sampling of the methodologies for the investigation of animal learning, behavior and cognition 2006, 189-208. Nova Science, Hauppauge, NY. M.J. Anderson (Ed.).
51. Berger B.D., Schuster R. An animal model of social interaction: implications for the analysis of drug action. Behavioral models and the analysis of drug action 1982, 415-428. Elsevier, Amsterdam. M.Y. Spiegelstein, A. Levy (Eds.).
52. Schuster R.H., Rachlin H., Rom M., Berger B.D. An animal model of dyadic social interaction: influence of isolation, competition, and shock-induced aggression. Aggress Behav 1982, 8:116-121.
53. Tsoory M.M., Youdim M.B., Schuster R. Social-cooperation differs from individual behavior in hypothalamic and striatal monoamine function: evidence from a laboratory rat model. Behav Brain Res 2012, 232:252-263.
54. Raz S., Teucher D., Berger B.D. Reversal of isolation induced aggression and increased morphine consumption by sixty-minutes per day of social interaction. Isr J Psychiatry 2005, 41-43.
55. Weiss I.C., Feldon J. Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology 2001, 156:305-326.
56. Tamashiro K.L.K., Nguyen M.M.N., Sakai R.R. Social stress: from rodents to primates. Front Neuroendocrinol 2005, 26:27-40.
57. Brenes J.C., Fornaguera J. The effect of chronic fluoxetine on social isolation-induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral stiatum. Behav Brain Res 2009, 198:199-205.
58. Brenes J.C., Fornaguera J. Effects of environmental enrichment and social isolation on sucrose consumption and preference: associations with depressive-like behavior and ventral striatum dopamine. Neurosci Lett 2008, 436:278-282.
59. Hall F.S., Huang S., Fong G.W., Pert A., Linnoila M. Effects of isolation rearing on voluntary consumption of ethanol, sucrose and saccharin solutions in Fawn Hooded and Wistar rats. Psychopharmacology 1998, 139:210-216.
60. Howes S.R., Dalley J.W., Morrison C.H., Robbins T.W., Everitt B.J. Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology 2000, 151:55-63.
61. Jones G.H., Marsden C.A., Robbins T.W. Increased sensitivity to amphetamine and reward-related stimuli following social isolation in rats: possible disruption of dopamine-dependent mechanisms of the nucleus accumbens. Psychopharmacology 1990, 102:364-372.
62. Deehan G.A., Cain M.E., Kiefer S.W. Differential rearing conditions alter operant responding for ethanol in outbred rats. Alcohol Clin Exp Res 2007, 31:1692-1698.
63. Morgan M.J., Einon D.F., Nicholas D. The effects of isolation rearing on behavioural inhibition in the rat. Q J Exp Psychol 1975, 27:615-634.
64. Fone K.C.F., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 2008, 32:1087-1102.
65. Kretschmer B.D., Schelling P., Beier N., Liebscher C., Treutel S., Kruger N., et al. Modulatory role of food, feeding regime and physical exercise on body weight and insulin resistance. Life Sci 2005, 76:1553-1573.
66. Thorsell A., Slawecki C.J., El Khoury A., Mathe A.A., Ehlers C.L. Effects of social isolation on ethanol consumption and substance P/neurokinin expression in Wistar rats. Alcohol 2005, 36:91-97.
67. Bourin M., Petit-Demoouliere B., Dhonnchadha B.N., Hascoet M. Animal models of anxiety in mice. Fundam Clin Pharmacol 2007, 21:567-574.
68. Grillon C. Models and mechanisms of anxiety: evidence from startle studies. Psychopharmacology 2008, 199:421-437.
69. Grillon C. Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology. Biol Psychiatry 2002, 52:958-975.
70. Rodgers R.J. Animal models of 'anxiety': where next?. Behav Pharmacol 1997, 8:477-496.
71. Davis M., Walker D.L., Lee Y. Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos Trans R Soc Lond 1997, B352:1657-1687.
72. Gewirtz J.C., McNish K.A., Davis M. Lesions of the bed nucleus of the stria terminalis block sensitization of the acoustic startle reflex produced by repeated stress, but not fear potentiated startle. Prog Neuropsychopharmacol 1998, 22:625-648.
73. Grillon C., Baas J. A review of the modulation of the startle reflex by affective states and its application in psychiatry. Clin Neurophysiol 2003, 114:1557-1579.
74. Koch M. The neurobiology of startle. Prog Neurobiol 1999, 59:107-128.
75. Viveros M.P., Hernandez R., Gallego A. Effects of social isolation and crowding upon active-avoidance performance in the rat. Anim Learn Behav 1990, 18:90-96.
76. Will B.E., Kelche C.R. Effects of different postoperative environments on the avoidance behavior of rats with hippocampal lesions: recovery or improvement of function?. Behav Neural Biol 1979, 27:96-106.
77. Choi J.S., Cain C.K., LeDoux J.E. The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem 2010, 17:139-147.
78. Gentsch C., Lichtsteiner M., Frischknecht H.R., Feer H., Siegfried B. Isolation-induced locomotor hyperactivity and hypoalgesia in rats are prevented by handling and reversed by resocialisation. Physiol Behav 1988, 43:13-16.
79. Meng Q., Lia N., Hana X., Shaoa F., Wang W. Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neurosci Lett 2010, 480:25-29.
80. Hellemans K.G.C., Benge L.C., Olmstead M.C. Adolescent enrichment partially reverses the social isolation syndrome. Dev Brain Res 2004, 150:103-115.
81. Serra M., Pisu M.G., Floris I., Biggio G. Social isolation-induced changes in the hypothalamic-pituitary-adrenal axis in the rat. Stress 2005, 8:259-264.
82. Morinan A., Leonard B.E. Some anatomical and physiological correlates of social isolation in the young rat. Physiol Behav 1980, 24:637-640.
83. Viveros M.P., Hernandez R., Martinez I., Gonzalez P. Effects of social isolation and crowding upon adrenocortical reactivity and behavior in the rat. Rev Esp Fisiol 1988, 44:315-321.
84. Haller J., Hala'sz J. Mild social stress abolished the effects of isolation on anxiety and chlordiazepoxide reactivity. Psychopharmacology 1999, 144:311-315.
85. Rivier C., Vale W. Diminished responsiveness of the hypothalamic-pituitary-adrenal axis of the rat during exposure to prolonged stress: a pituitary-mediated mechanism. Endocrinology 1987, 121:1320-1328.
86. Greco A.M., Gambardella P., Sticchi R., D'Aponte D., De Franciscis P. Chronic administration of imipramine antagonizes deranged circadian rhythm phases in individually housed rats. Physiol Behav 1990, 8:67-72.
87. Sandstrom N.J., Hart S.R. Isolation stress during the third postnatal week alters radial arm maze performance and corticosterone levels in adulthood. Behav Brain Res 2005, 56:289-296.
88. Miachon S., Rochet T., Marthian B., Barbagli B., Claustrat B. Long-term isolation of Wistar rats alters brain monoamine turnover, blood corticosterone, and ACTH. Brain Res Bull 1993, 32:611-614.
89. Sanchez M.M., Aguado F., Sanchez-Toscano F., Saphier D. Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 1998, 139:579-587.
90. Gentsch C., Lichtsteiner M., Feer H. Locomotor activity, defecation score and corticosterone levels during an openfield exposure: a comparison among individually and group-housed rats, and genetically selected rat lines. Physiol Behav 1981, 27:183-186.
91. Brain P.F., Nowell N.W. Isolation versus grouping effects on adrenal and gonadal function in albino mice I. The male. Gen Comp Endocrinol 1971, 16:149-154.
92. Tomazini F.M., Reimer A., Albrechet-Souza L., Brand̃ao M.L. Opposite effects of short- and long-duration isolation on ultrasonic vocalization, startle and prepulse inhibition in rats. J Neurosci Methods 2006, 153:114-120.
93. Stevens K.E., Johnson R.G., Rose G.M. Rats reared in social isolation show schizophrenia-like changes in auditory gating. Pharmacol Biochem Behav 1997, 58:1031-1036.
94. Varty G.B., Higgins G.A. Examination of drug-induced and isolation-induced disruptions of prepulse inhibition as models to screen antipsychotic drugs. Psychopharmacology 1995, 122:15-26.
95. Varty G.B., Braff D.L., Geyer M.A. Is there a critical developmental 'window' for isolation rearing-induced changes in prepulse inhibition of the acoustic startle response?. Behav Brain Res 1999, 100:177-183.
96. Varty G.B., Paulus M.P., Braff D.L., Geyer M.A. Environmental enrichment and isolation rearing in the rat: effects on locomotor behavior and startle response plasticity. Biol Psychiatry 2000, 47:864-873.
97. Weiss I., Domeney A., Feldon J. Dissociation between isolation-induced disruption of prepulse inhibition and hyperactivity as a function of caging condition. Behav Pharmacol 1998, 9:S93.
98. Garzon J., Fuentes J.A., Del Rio J. Antidepressants selectively antagonize the hyperactivity induced in rats by long-term isolation. Eur J Pharmacol 1979, 59:293-296.
99. Gentsch C., Lichtsteiner M., Kraeuchi K., Feer H. Different reaction patterns in individually and socially reared rats during exposures to novel environments. Behav Brain Res 1982, 4:45-54.
100. Heidbreder C.A., Weiss I.C., Domeney A.M., Pryce C., Homberg J., Hedou G., et al. Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 2000, 100:749-768.