Artificial rearing alters the response of rats to natural and drug-mediated rewards

Developmental Psychobiology

Volumn 48, Issue 4, 2006, Pages 301-314

  Lomanowska, Anna M ^a   Rana, Shadna A ^b   McCutcheon, Dawn ^a   Parker, Linda A ^b   Wainwright, Patricia E ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b WILFRID LAURIER UNIVERSITY   (Canada)

Author keywords

Artificial rearing; Conditioned place response; Development; Early experience; Morphine; Rat; Reward; Sucrose preference

Indexed keywords

MORPHINE; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONDITIONED REFLEX; CONTROLLED STUDY; EMOTIONALITY; MALE; NONHUMAN; OPEN FIELD BEHAVIOR; RAT; REARING; REWARD; SUGAR INTAKE;

AFFECT; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CONDITIONING (PSYCHOLOGY); FEMALE; FOOD PREFERENCES; GASTROSTOMY; MALE; MORPHINE; NARCOTICS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SOCIAL ENVIRONMENT; SUCROSE;

ANIMALIA;

EID: 33646537506     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20139     Document Type: Article

References (81)

1. Barnett, S. A., Smart, J. L., & Widdowson, E. M. (1971). Early nutrition and the activity and feeding of rats in an artificial environment. Developmental Psychobiology, 4, 1-15.
2. Barrot, M., Olivier, J. D., Perrotti, L. I., DiLeone, R. J., Berton, O., Eisch, A. J., Impey, S., Storm, D. R., Neve, R. L., Yin, J. C., Zachariou, V., & Nestler, E. J. (2002). CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proceeding of the National Academy of Sciences of the United States of America, 99, 11435-11440.
3. Barrot, M., Wallace, D. L., Bolanos, C. A., Graham, D. L., Perrotti, L. I., Neve, R. L., Chambliss, H., Yin, J. C., & Nestler, E. J. (2005). Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proceeding of the National Academy of Sciences of the United States of America, 102, 8357-8362.
4. Bassareo, V., & Di Chiara, G. (1997). Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum. Journal of Neuroscience, 17, 851-861.
5. Berridge, K. C., & Robinson, T. E. (2003). Parsing reward. Trends in Neuroscience, 26, 507-513.
6. Bowlby, J. (1988). A secure base: Parent-child attachments and healthy human development. New York: Basic Books.
7. Brake, W. G., Zhang, T. Y., Diorio, J., Meaney, M. J., & Gratton, A. (2004). Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioral responses to psychostimulants and stressors in adult rats. European Journal of Neuroscience, 19, 1863-1874.
8. Brown, E. J. (2003). Child physical abuse: Risk for psychopathology and efficacy of interventions. Current Psychiatry Reports, 5, 87-94.
9. Burns, L. H., Annett, L., Kelley, A. E., Everitt, B. J., & Robbins, T. W. (1996). Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: Implication for limbic-striatal interactions. Behavioral Neuroscience, 110, 60-73.
10. Caldji, C., Diorio, J., & Meaney, M. J. (2000). Variations in maternal care in infancy regulate the development of stress reactivity. Biological Psychiatry, 48, 1164-1174.
11. Camp, L. L., & Rudy, J. W. (1988). Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Developmental Psychobiology, 21, 25-42.
12. Canadian Council on Animal Care (1993). Guide to the care and use of experimental animals, Vol 1, 2nd Edn. CCAC, Ottawa, Ontario.
13. Cassidy, J., & Shaver, P. R. (1999). Handbook of attachment: Theory, research, and clinical applications. New York: Guilford.
14. DeSousa, N. J., Bush, D. E., & Vaccarino, F. J. (2000). Self-administration of intravenous amphetamine is predicted by individual differences in sucrose feeding in rats. Psychopharmacology (Berl), 148, 52-58.
15. Field, T. (1998). Maternal depression effects on infants and early interventions. Preventive Medicine, 27, 200-203.
16. Fleming, A. S., Korsmit, M., & Deller, M. (1994). Rats pups are potent reinforcers to the maternal animal: Effects of experience, parity, hormones and dopamine function. Psychobiology, 22, 44-53.
17. Flory, G. S., Langley, C. M., Pfister, J. F., & Alberts, J. R. (1997). Instrumental learning for a thermal reinforcer in 1-day-old rats. Developmental Psychobiology, 30, 41-47.
18. Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science, 286, 1155-1158.
19. Francis, D. D., & Meaney, M. J. (1999). Maternal care and the development of stress responses. Current Opinion in Neurobiology, 9, 128-134.
20. Galef, B. G., Jr., & Smith, M. A. (1994). Susceptibility of artificially reared rat pups to social influences on food choice. Developmental Psychobiology, 27, 85-92.
21. Gentsch, C., Lichtsteiner, M., Frischknecht, H. R., Feer, H., & Siegfried, B. (1988). Isolation-induced locomotor hyperactivity and hypoalgesia in rats are prevented by handling and reversed by resocialization. Physiology and Behavior, 43, 13-16.
22. Girard, T. A., Xing, H., Ward, G. R., Nguyen, H., & Wainwright, P. E. (2001). Exposure to ethanol and nicotine during the brain growth spurt: Spatial DMP performance in male rats. Pharmacology Biochemisty and Behavior, 68, 515-523.
23. Girard, T. A., & Wainwright, P. E. (2002). Testing the spatial-versus object-learning distinction: Water-maze performance of male rats exposed to ethanol during the brain growth spurt. Behavioural Brain Research, 134, 493-503.
24. Girard, T. A., Hung, V., Patel, S., Ward, G. R., & Wainwright, P. E. (2003). Developmental binge exposure to ethanol and artificial rearing do not affect the social transfer of diet preference. Alcoholism-Clinical and Experimental Research, 27, 686-694.
25. Glaser, D. (2000). Child abuse and neglect and the brain-a review. Journal of Child Psychology and Psychiatry, 41, 97-116.
26. Gonzalez, A., Lovic, V., Ward, G. R., Wainwright, P. E., & Fleming, A. S. (2001). Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Developmental Psychobiology, 38, 11-32.
27. Gonzalez, A., & Fleming, A. S. (2002). Artificial rearing causes changes in maternal behavior and c-fos expression in juvenile female rats. Behavioral Neuroscience, 116, 999-1013.
28. Gosnell, B. A. (2000). Sucrose intake predicts rate of acquisition of cocaine self-administration. Psychopharmacology (Berl), 149, 286-292.
29. Grill, H. J., & Norgren, R. (1978). The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Research, 143, 263-279.
30. Hall, F. S. (1998). Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Critical Reviews in Neurobiology, 12, 129-162.
31. Hall, W. G. (1975). Weaning and growth of artificially reared rats. Science, 190, 1313-1315.
32. Hansen, S. (1994). Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: Characterization of the pup retrieval deficit. Physiology and Behavior, 55, 615-620.
33. Hashimoto, H., Saito, T. R., Furudate, S., & Takahashi, K. W. (2001). Prolactin levels and maternal behavior induced by ultrasonic vocalizations of the rat pup. Experimental Animals, 50, 307-312.
34. Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023-1039.
35. Hofer, M. A. (1973). The role of nutrition in the physiological and behavioral effects of early maternal separation on infant rats. Psychosomatic Medicine, 35, 350-359.
36. Hofer, M. A. (1994). Early relationships as regulators of infant physiology and behavior. Acta Paediatrica Supplement, 397, 9-18.
37. Hogg, S. (1996). A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacology Biochemistry and Behavior, 54, 21-30.
38. Hsu, F. C., Zhang, G. J., Raol, Y. S., Valentino, R. J., Coulter, D. A., & Brooks-Kayal, A. R. (2003). Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proceedings of the National Academy of Sciences of the United States of America, 100, 12213-12218.
39. Insel, T. R. (2003). Is social attachment an addictive disorder? Physiology and Behavior, 79, 351-357.
40. Jans, J. E., & Leon, M. (1983). Determinants of mother-young contact in Norway rats. Physiology and Behavior, 30, 919-935.
41. Johanson, I. B., Hall, W. G., & Polefrone, J. M. (1984). Appetitive conditioning in neonatal rats: Conditioned ingestive responding to stimuli paired with oral infusions of milk. Developmental Psychobiology, 17, 357-381.
42. Kaneko, W. M., Riley, E. P., & Ehlers, C. L. (1996). Effects of artificial rearing on electrophysiology and behavior in adult rats. Depression and Anxiety, 4, 279-288.
43. Kelly, S. J., Mahoney, J. C., Randich, A., & West, J. R. (1991). Indices of stress in rats: Effects of sex, perinatal alcohol and artificial rearing. Physiology and Behavior, 49, 751-756.
44. Kelly, S. J., Ostrowski, N. L., & Wilson, M. A. (1999). Gender differences in brain and behavior: Hormonal and neural bases. Pharmacology Biochemistry and Behavior, 64, 655-664.
45. Kuhn, C. M., & Schanberg, S. M. (1998). Responses to maternal separation: Mechanisms and mediators. International Journal of Developmental Neuroscience, 16, 261-270.
46. Levine, S. (1960). Stimulation in infancy. Scientific American, 202, 81-86.
47. Levy, F., Melo, A. I., Galef, B. G., Jr., Madden, M., & Fleming, A. S. (2003). Complete maternal deprivation affects social, but not spatial, learning in adult rats. Developmental Psychobiology, 43, 177-191.
48. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary- adrenal responses to stress. Science, 277, 1659-1662.
49. Liu, D., Caldji, C., Sharma, S., Plotsky, P. M., & Meaney, M. J. (2000). Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. Journal of Neuroendocrinology, 12, 5-12.
50. Lomanowska, A. (2005). Behavioural responses of artificially reared rats to reward and novelty. Master's Thesis. University of Waterloo, Department of Health Studies and Gerontology.
51. Lovic, V., & Fleming, A. S. (2004). Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behavioural Brain Research, 148, 209-219.
52. Macri, S., Mason, G. J., & Wurbel, H. (2004). Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. European Journal of Neuroscience, 20, 1017-1024.
53. Marinelli, M., & Piazza, P. V. (2002). Interaction between glucocorticoid hormones, stress and psychostimulant drugs. European Journal of Neuroscience, 16, 387-394.
54. Marmendal, M., Roman, E., Eriksson, C. J., Nylander, I., & Fahlke, C. (2004). Maternal separation alters maternal care, but has minor effects on behavior and brain opioid peptides in adult offspring. Developmental Psychobiology, 45, 140-152.
55. Matthews, K., & Robbins, T. W. (2003). Early experience as a determinant of adult behavioral responses to reward: The effects of repeated maternal separation in the rat. Neuroscience and Biobehavioral Reviews, 27, 45-55.
56. McEwen, B. S. (2003). Early life influences on life-long patterns of behavior and health. Mental Retardation and Developmental Disabilities Research Reviews, 9, 149-154.
57. Meaney, M. J., Aitken, D. H., Viau, V., Sharma, S., & Sarrieau, A. (1989). Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology, 50, 597-604.
58. Meaney, M. J., Brake, W., & Gratton, A. (2002). Environmental regulation of the development of mesolimbic dopamine systems: A neurobiological mechanism for vulnerability to drug abuse? Psychoneuroendocrinology, 27, 127-138.
59. Palanza, P. (2001). Animal models of anxiety and depression: How are females different? Neuroscience and Biobehavioral Reviews, 25, 219-233.
60. Parker, L. A. (1992). Place conditioning in a three-or four-choice apparatus: Role of stimulus novelty in drug-induced place conditioning. Behavioral Neuroscience, 106, 294-306.
61. Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985). Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. Journal of Neuroscience Methods, 14, 149-167.
62. Plotsky, P. M., & Meaney, M. J. (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research, 18, 195-200.
63. Pryce, C. R., & Feldon, J. (2003). Long-term neurobehavioral impact of the postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neuroscience and Biobehavioral Reviews, 27, 57-71.
64. Reboucas, R. C., & Schmidek, W. R. (1997). Handling and isolation in three strains of rats affect open field, exploration, hoarding and predation. Physiology and Behavior, 62, 1159-1164.
65. Sills, T. L., & Vaccarino, F. J. (1994). Individual differences in sugar intake predict the locomotor response to acute and repeated amphetamine administration. Psychopharmacology (Berl), 116, 1-8.
66. Simons, D. J., & Land, P. W. (1987). Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature, 326, 694-697.
67. Smart, J. L., Stephens, D. N., Tonkiss, J., Auestad, N. S., & Edmond, J. (1984). Growth and development of rats artificially reared on different milk-substitutes. British Journal of Nutrition, 52, 227-237.
68. Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417-463.
69. Stern, J. M. (1996). Somatosensation and maternal care in Norway rats. In J. S. Rosenblatt & C. T. Snowdon (Eds.), Parental care: Evolution, mechanisms, and adaptive significance (pp. 243-294). San Diego: Academic Press.
70. Swanson, H. H., Bolwerk, E., & Brenner, E. (1984). Effects of cooling in infant rats on growth, maturation, sleep patterns and responses to food deprivation. British Journal of Nutrition, 52, 139-148.
71. Teicher, M. H. (2002). Scars that won't heal: The neurobiology of child abuse. Scientific American, 286, 68-75.
72. Tonkiss, J., Smart, J. L., & Massey, R. F. (1987). Effects of early life undernutrition in artificially-reared rats. 2. Subsequent behavior. Physiology and Behavior, 41, 555-562.
73. Vezina, P., & Stewart, J. (1987). Conditioned locomotion and place preference elicited by tactile cues paired exclusively with morphine in an open field. Psychopharmacology, 91, 375-380.
74. Wainwright, P. E., Xing, H. C., Ward, G. R., Huang, Y. S., Bobik, E., Auestad, N., & Montalto, M. (1999). Water maze performance is unaffected in artificially reared rats fed diets supplemented with arachidonic acid and docosahexaenoic acid. Journal of Nutrition, 129, 1079-1089.
75. Wainwright, P. E. (2001). The role of nutritional factors in behavioral development in laboratory mice. Behavioural Brain Research, 125, 75-80.
76. Ward, G., Xing, H. C., Carnide, N., Slivchak, J., & Wainwright, P. (2004). Adrenocortical response to stress in fasted and unfasted artificially reared 12-day-old rat pups. Developmental Psychobiology, 45, 245-250.
77. Ward, G. R., Huang, Y. S., Bobik, E., Xing, H. C., Mutsaers, L., Auestad, N., Montalto, M., & Wainwright, P. (1998). Long-chain polyunsaturated fatty acid levels in formulae influence deposition of docosahexaenoic acid and arachidonic acid in brain and red blood cells of artificially reared neonatal rats. Journal of Nutrition, 128, 2473-2487.
78. Weiss, I. C., Pryce, C. R., Jongen-Relo, A. L., Nanz-Bahr, N. I., & Feldon, J. (2004). Effect of social isolation on stress-related behavioral and neuroendocrine state in the rat. Behavioural Brain Research, 152, 279-295.
79. Wilson, C., Nomikos, G. G., Collu, M., & Fibiger, H. C. (1995). Dopaminergic correlates of motivated behavior: Importance of drive. Journal of Neuroscience, 15, 5169-5178.
80. Yagil, R., Etzion, Z., & Berlyne, G. M. (1976). Changes in rat milk quantity and quality due to variations in litter size and high ambient temperature. Laboratory Animal Science, 26, 33-37.
81. Young, A. A., & Dawson, N. J. (1988). Effects of environmental temperature on the development of a noradrenergic thermoregulatory mechanism in the rat. Pflugers Archiv, 412, 141-146.