Individual differences in novelty-seeking and emotional reactivity correlate with variation in maternal behavior

Hormones and Behavior

Volumn 51, Issue 5, 2007, Pages 655-664

  Clinton, Sarah M ^a   Vázquez, Delia M ^a   Kabbaj, Mohammed ^b   Kabbaj, Marie Helen ^b   Watson, Stanley J ^a   Akil, Huda ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Anxiety; High responder; Light Dark test; Low responder; Stress

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; EMOTION; ENVIRONMENTAL FACTOR; FEMALE; LIGHT DARK CYCLE; LOCOMOTION; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MOTHER CHILD RELATION; NEUROENDOCRINE SYSTEM; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PUERPERIUM; RAT; SEX DIFFERENCE; SPRAGUE DAWLEY RAT; STIMULATION;

AGE FACTORS; ANIMALS; EMOTIONS; EXPLORATORY BEHAVIOR; FEMALE; INDIVIDUALITY; MALE; MATERNAL BEHAVIOR; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; TEMPERAMENT;

EID: 34248642559     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2007.03.009     Document Type: Article

References (65)

1. Abraham A., Clinton S.M., Watson S.J., and Akil H. Individual Differences in Novelty-Seeking Correlate with Differences in Aggressive Behavior. Proceedings of the Society for Neuroscience 36th Annual Meeting, Atlanta, GA, pp (2006)
2. Altman J., and Sudarshan K. Postnatal development of locomotion in the laboratory rat. Anim. Behav. 23 (1975) 896-920
3. Arnold J.L., and Siviy S.M. Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat. Dev. Psychobiol. 41 (2002) 205-215
4. Ball S.A., Cobb-Richardson P., Connolly A.J., Bujosa C.T., and O'Neall T.W. Substance abuse and personality disorders in homeless drop-in center clients: symptom severity and psychotherapy retention in a randomized clinical trial. Comp. Psychiatry 46 (2005) 371-379
5. Bridges R.S., Robertson M.C., Shiu R.P., Friesen H.G., Stuer A.M., and Mann P.E. Endocrine communication between conceptus and mother: placental lactogen stimulation of maternal behavior. Neuroendocrinology 64 (1996) 57-64
6. Card J.P., Levitt P., Gluhovsky M., and Rinaman L. Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. J. Neurosci. 25 (2005) 9102-9111
7. Champagne F., Diorio J., Sharma S., and Meaney M.J. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 12736-12741
8. Champagne F.A., Weaver I.C., Diorio J., Sharma S., and Meaney M.J. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144 (2003) 4720-4724
9. Cloninger C.R. A systematic method for clinical description and classification of personality variants. A proposal. Arch. Gen. Psychiatry 44 (1987) 573-588
10. Dellu F., Piazza P.V., Mayo W., Le Moal M., and Simon H. Novelty-seeking in rats-biobehavioral characteristics and possible relationship with the sensation-seeking trait in man. Neuropsychobiology 34 (1996) 136-145
11. Denenberg V.H., Brumaghim J.T., Haltmeyer G.C., and Zarrow M.X. Increased adrenocortical activity in the neonatal rat following handling. Endocrinology 81 (1967) 1047-1052
12. Dietz D.M., Tapocik J., Gaval-Cruz M., and Kabbaj M. Dopamine transporter, but not tyrosine hydroxylase, may be implicated in determining individual differences in behavioral sensitization to amphetamine. Physiol. Behav. 86 (2005) 347-355
13. Eilam D., and Golani I. The ontogeny of exploratory behavior in the house rat (Rattus rattus): the mobility gradient. Dev. Psychobiol. 21 (1988) 679-710
14. Ferris C.F., Kulkarni P., Sullivan Jr. J.M., Harder J.A., Messenger T.L., and Febo M. Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J. Neurosci. 25 (2005) 149-156
15. Fleming A.S., and Rosenblatt J.S. Olfactory regulation of maternal behavior in rats. I. Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J. Comp. Physiol. Psychol. 86 (1974) 221-232
16. Fleming A.S., and Rosenblatt J.S. Olfactory regulation of maternal behavior in rats. II. Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins. J. Comp. Physiol. Psychol. 86 (1974) 233-246
17. Fleming A.S., and Anderson V. Affect and nurturance: mechanisms mediating maternal behavior in two female mammals. Prog. Neuro-psychopharmacol. Biol. Psychiatry 11 (1987) 121-127
18. Fleming A.S., and Sarker J. Experience-hormone interactions and maternal behavior in rats. Physiol. Behav. 47 (1990) 1165-1173
19. Fleming A.S., and Walsh C. Neuropsychology of maternal behavior in the rat: c-fos expression during mother-litter interactions. Psychoneuroendocrinology 19 (1994) 429-443
20. Fleming A.S., and Korsmit M. Plasticity in the maternal circuit: effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. Behav. Neurosci. 110 (1996) 567-582
21. Fleming A., Vaccarino F., Tambosso L., and Chee P. Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203 (1979) 372-374
22. Fleming A.S., Vaccarino F., and Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 25 (1980) 731-743
23. Fleming A.S., Cheung U., Myhal N., and Kessler Z. Effects of maternal hormones on 'timidity' and attraction to pup-related odors in female rats. Physiol. Behav. 46 (1989) 449-453
24. Fleming A.S., Suh E.J., Korsmit M., and Rusak B. Activation of Fos-like immunoreactivity in the medial preoptic area and limbic structures by maternal and social interactions in rats. Behav. Neurosci. 108 (1994) 724-734
25. Fleming A.S., O'Day D.H., and Kraemer G.W. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci. Biobehav. Rev. 23 (1999) 673-685
26. Francis D., Diorio J., Liu D., and Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286 (1999) 1155-1158
27. Francis D.D., Champagne F.C., and Meaney M.J. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J. Neuroendocrinol. 12 (2000) 1145-1148
28. Hofer M.A. Maternal separation affects infant rats' behavior. Behav. Biol. 9 (1973) 629-633
29. Hooks M.S., Jones G.H., Smith A.D., Neill D.B., and Justice Jr. J.B. Individual differences in locomotor activity and sensitization. Pharmacol. Biochem. Behav. 38 (1991) 467-470
30. Hooks M.S., Juncos J.L., Justice Jr. J.B., Meiergerd S.M., Povlock S.L., Schenk J.O., and Kalivas P.W. Individual locomotor response to novelty predicts selective alterations in D1 and D2 receptors and mRNAs. J. Neurosci. 14 (1994) 6144-6152
31. Hooks M.S., Sorg B.A., and Kalivas P.W. The relationship between MRNA levels and the locomotor response to novelty. Brain Res. 663 (1994) 312-316
32. Kabbaj M. Neurobiological bases of individual differences in emotional and stress responsiveness: high responders-low responders model. Arch. Neurol. 61 (2004) 1009-1012
33. Kabbaj M., and Akil H. Individual differences in novelty-seeking behavior in rats: a c-fos study. Neuroscience 106 (2001) 535-545
34. Kabbaj M., Devine D.P., Savage V.R., and Akil H. Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: differential expression of stress-related molecules. J. Neurosci. 20 (2000) 6983-6988
35. Kabbaj M., Evans S., Watson S.J., and Akil H. The search for the neurobiological basis of vulnerability to drug abuse: using microarrays to investigate the role of stress and individual differences. Neuropharmacology 47 Suppl 1 (2004) 111-122
36. Klebaur J.E., Bevins R.A., Segar T.M., and Bardo M.T. Individual differences in behavioral responses to novelty and amphetamine self-administration in male and female rats. Behav. Pharmacol. 12 (2001) 267-275
37. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., and Plotsky P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 122 (2000) 81-103
38. Lee A., Clancy S., and Fleming A.S. Mother rats bar-press for pups: effects of lesions of the mpoa and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav. Brain Res. 100 (1999) 15-31
39. Levine S. Plasma-free corticosteroid response to electric shock in rats stimulated in infancy. Science 135 (1962) 795-796
40. Levine S., Alpert M., and Lewis G.W. Infantile experience and the maturation of the pituitary adrenal axis. Science 126 (1957) 1347
41. Levine S., Haltmeyer G.C., Karas G.G., and Denenberg V.H. Physiological and behavioral effects of infantile stimulation. Physiol. Behav. 2 (1967) 55-59
42. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., and Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1659-1662
43. Mattson B.J., and Morrell J.I. Preference for cocaine- versus pup-associated cues differentially activates neurons expressing either Fos or cocaine- and amphetamine-regulated transcript in lactating, maternal rodents. Neuroscience 135 (2005) 315-328
44. Mattson B.J., Williams S., Rosenblatt J.S., and Morrell J.I. Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period. Behav. Neurosci. 115 (2001) 683-694
45. Mattson B.J., Williams S.E., Rosenblatt J.S., and Morrell J.I. Preferences for cocaine- or pup-associated chambers differentiates otherwise behaviorally identical postpartum maternal rats. Psychopharmacology (Berlin) 167 (2003) 1-8
46. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24 (2001) 1161-1192
47. Numan M. Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 87 (1974) 746-759
48. Numan M. Neural basis of maternal behavior in the rat. Psychoneuroendocrinology 13 (1988) 47-62
49. Numan M., Morrell J.I., and Pfaff D.W. Anatomical identification of neurons in selected brain regions associated with maternal behavior deficits induced by knife cuts of the lateral hypothalamus in rats. J. Comp. Neurol. 237 (1985) 552-564
50. Piazza P.V., Deminiere J.M., Le Moal M., and Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 245 (1989) 1511-1513
51. Piazza P.V., Maccari S., Deminiere J.M., Le Moal M., Mormede P., and Simon H. Corticosterone levels determine individual vulnerability to amphetamine self-administration. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 2088-2092
52. Piazza P.V., Rouge-Pont F., Deminiere J.M., Kharoubi M., Le Moal M., and Simon H. Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus accumbens of rats predisposed to develop amphetamine self-administration. Brain Res. 567 (1991) 169-174
53. Rinaman L., Levitt P., and Card J.P. Progressive postnatal assembly of limbic-autonomic circuits revealed by central transneuronal transport of pseudorabies virus. J. Neurosci. 20 (2000) 2731-2741
54. Rosenblatt J.S. The development of maternal responsiveness in the rat. Am. J. Orthop. 39 (1969) 36-56
55. Rosenblatt J.S., Wagner C.K., and Morrell J.I. Hormonal priming and triggering of maternal behavior in the rat with special reference to the relations between estrogen receptor binding and ER mRNA in specific brain regions. Psychoneuroendocrinology 19 (1994) 543-552
56. Russell P.A. Effects of maternal separation and maternal disturbance on offspring growth and behavior in rats. J. Gen. Psychol. 88 (1973) 127-133
57. Sanchez M.M., Ladd C.O., and Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 13 (2001) 419-449
58. Sapolsky R.M., and Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396 (1986) 64-76
59. Sell S.L., Dillon A.M., Cunningham K.A., and Thomas M.L. Estrous cycle influence on individual differences in the response to novelty and cocaine in female rats. Behav. Brain Res. 161 (2005) 69-74
60. Smart J.L., and Dobbing J. Vulnerability of developing brain. IV. Passive avoidance behavior in young rats following maternal undernutrition. Dev. Psychobiol. 5 (1972) 129-135
61. Stead J.D., Neal C., Meng F., Wang Y., Evans S., Vazquez D.M., Watson S.J., and Akil H. Transcriptional profiling of the developing rat brain reveals that the most dramatic regional differentiation in gene expression occurs postpartum. J. Neurosci. 26 (2006) 345-353
62. Stead J.D., Clinton S., Neal C., Schneider J., Jama A., Miller S., Vazquez D.M., Watson S.J., and Akil H. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36 5 (2006) 697-712
63. Wiedenmayer C.P., and Barr G.A. Ontogeny of defensive behavior and analgesia in rat pups exposed to an adult male rat. Physiol. Behav. 63 (1998) 261-269
64. Zarrow M.X., Campbell P.S., and Denenberg V.H. Handling in infancy: increased levels of the hypothalamic corticotropin releasing factor (CRF) following exposure to a novel situation. Proc. Soc. Exp. Biol. Med. 141 (1972) 356-358
65. Zuckerman M., and Neeb M. Sensation seeking and psychopathology. Psychiatry Res. 1 (1979) 255-264