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Bisaz R, Sullivan RM. Developmental neurobiology of the rat attachment system and its modulation by stress. Behav Sci (Basel). 2012;2(2):79-102doi: 10.3390/bs2020079.
Bisaz, R., & Sullivan, R. M. (2012). Developmental neurobiology of the rat attachment system and its modulation by stress. Behavioral sciences (Basel, Switzerland), 2(2), 79-102. https://doi.org/10.3390/bs2020079
Bisaz, Reto, and Sullivan, Regina M. "Developmental neurobiology of the rat attachment system and its modulation by stress." Behavioral sciences (Basel, Switzerland) vol. 2,2 (2012): 79-102. doi: https://doi.org/10.3390/bs2020079
Bisaz R, Sullivan RM. Developmental neurobiology of the rat attachment system and its modulation by stress. Behav Sci (Basel). 2012 Jun 01;2(2):79-102. doi: 10.3390/bs2020079. PMID: 23626910; PMCID: PMC3635149.
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Behav Sci (Basel). 2012 Jun 01;2(2):79-102. doi: 10.3390/bs2020079.

Developmental neurobiology of the rat attachment system and its modulation by stress.

Behavioral sciences (Basel, Switzerland)

Reto Bisaz, Regina M Sullivan

Affiliations

  1. Emotional Brain Institute, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, New York, NY 10962, USA ; Child & Adolescent Psychiatry, New York University School of Medicine, 215 Lexington Avenue, New York, NY 10016, USA ; Center for Neural Science, New York University, 4 Washington Place, New York, NY 10003, USA.

PMID: 23626910 PMCID: PMC3635149 DOI: 10.3390/bs2020079

Abstract

Stress is a powerful modulator of brain structure and function. While stress is beneficial for survival, inappropriate stress dramatically increases the risk of physical and mental health problems, particularly when experienced during early developmental periods. Here we focus on the neurobiology of the infant rat's odor learning system that enables neonates to learn and approach the maternal odor and describe the unique role of the stress hormone corticosterone in modulating this odor approach learning across development. During the first nine postnatal days, this odor approach learning of infant rats is supported by a wide range of sensory stimuli and ensures attachment to the mother's odor, even when interactions with her are occasionally associated with pain. With maturation and the emergence of a stress- or pain-induced corticosterone response, this odor approach learning terminates and a more adult-like amygdala-dependent fear/avoidance learning emerges. Strikingly, the odor approach and attenuated fear learning of older pups can be re-established by the presence of the mother, due to her ability to suppress her pups' corticosterone release and amygdala activity. This suggests that developmental changes in stress responsiveness and the stimuli that produce a stress response might be critically involved in optimally adapting the pup's attachment system to its respective ecological niche.

Keywords: amygdala; attachment; corticosterone; fear; locus coeruleus; maternal odor; norepinephrine; pup; rat; stress; trauma

References

  1. J Clin Psychiatry. 2004;65 Suppl 1:18-28 - PubMed
  2. Neurobiol Aging. 2002 Sep-Oct;23(5):921-39 - PubMed
  3. Physiol Behav. 1994 Apr;55(4):717-21 - PubMed
  4. Physiol Behav. 1976 Sep;17(3):373-82 - PubMed
  5. Endocrinology. 1986 Apr;118(4):1445-51 - PubMed
  6. Genetica. 1998-1999;104(3):199-205 - PubMed
  7. Dev Psychobiol. 1975 Mar;8(2):151-64 - PubMed
  8. J Child Psychol Psychiatry. 1995 May;36(4):549-71 - PubMed
  9. Brain Res Dev Brain Res. 1990 May 1;53(2):215-21 - PubMed
  10. Neuroscience. 2002;112(4):901-6 - PubMed
  11. Horm Behav. 2006 Nov;50(4):623-31 - PubMed
  12. Biol Psychiatry. 2000 Oct 15;48(8):778-90 - PubMed
  13. Science. 1967 Apr 14;156(3772):258-60 - PubMed
  14. Dev Psychobiol. 2009 Sep;51(6):488-504 - PubMed
  15. Pharmacol Biochem Behav. 1989 Feb;32(2):569-72 - PubMed
  16. Physiol Behav. 1982 Nov;29(5):769-71 - PubMed
  17. Dev Cogn Neurosci. 2011 Jan;1(1):77-87 - PubMed
  18. Behav Brain Res. 2001 Sep 28;124(1):29-32 - PubMed
  19. Neuroscience. 1997 Jan;76(1):261-72 - PubMed
  20. Physiol Behav. 2001 Jun;73(3):255-60 - PubMed
  21. Neuron. 1999 Jun;23(2):227-8 - PubMed
  22. J Neurosci. 1994 Jul;14(7):4252-68 - PubMed
  23. Ann N Y Acad Sci. 1999 Jun 29;877:756-9 - PubMed
  24. Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):73-82 - PubMed
  25. J Neuroendocrinol. 2001 Sep;13(9):799-807 - PubMed
  26. Biol Psychiatry. 2009 May 1;65(9):760-9 - PubMed
  27. Science. 1972 Aug 11;177(4048):522-4 - PubMed
  28. Dev Psychobiol. 1990 Jul;23(5):411-26 - PubMed
  29. Annu Rev Neurosci. 2001;24:1161-92 - PubMed
  30. Brain Res Dev Brain Res. 1992 Dec 18;70(2):279-82 - PubMed
  31. Dev Psychobiol. 1982 Jul;15(4):349-55 - PubMed
  32. Annu Rev Neurosci. 1988;11:329-52 - PubMed
  33. Endocrinology. 1998 Jun;139(6):2838-46 - PubMed
  34. Neuroendocrinology. 1996 Apr;63(4):305-17 - PubMed
  35. Nat Rev Neurosci. 2002 Jun;3(6):453-62 - PubMed
  36. Nat Neurosci. 2000 Aug;3(8):799-806 - PubMed
  37. Horm Behav. 2007 Sep;52(3):391-400 - PubMed
  38. J Comp Psychol. 1987 Jun;101(2):190-6 - PubMed
  39. Behav Neurosci. 1997 Feb;111(1):49-56 - PubMed
  40. Neuropsychopharmacology. 2003 Nov;28(11):1950-9 - PubMed
  41. Psychother Psychosom. 1993;60(1):33-8 - PubMed
  42. Pediatr Neurol. 1996 Sep;15(2):114-9 - PubMed
  43. Brain Res. 2008 Mar 20;1200:58-65 - PubMed
  44. Dev Psychobiol. 2011 Dec;53(8):813-27 - PubMed
  45. Annu Rev Psychol. 1992;43:377-98 - PubMed
  46. Dev Psychobiol. 1995 Mar;28(2):103-15 - PubMed
  47. Neuron. 2005 Oct 20;48(2):175-87 - PubMed
  48. Mol Psychiatry. 2001 Jan;6(1):13-34 - PubMed
  49. Biol Neonate. 1998 Dec;74(6):402-8 - PubMed
  50. Eur J Pharmacol. 2009 Jun 10;612(1-3):48-53 - PubMed
  51. J Neurosci. 1999 Oct 1;19(19):8696-703 - PubMed
  52. Chem Senses. 2001 Jun;26(5):551-76 - PubMed
  53. Brain Res Dev Brain Res. 1995 Apr 18;85(2):187-91 - PubMed
  54. J Comp Neurol. 1987 Sep 1;263(1):113-25 - PubMed
  55. Biol Psychiatry. 2007 Nov 15;62(10):1070-9 - PubMed
  56. J Dev Behav Pediatr. 1987 Jun;8(3):171-6 - PubMed
  57. J Child Psychol Psychiatry. 2007 Mar-Apr;48(3-4):224-44 - PubMed
  58. Behaviour. 1971;40(1):100-34 - PubMed
  59. Ann N Y Acad Sci. 2003 Dec;1008:122-31 - PubMed
  60. J Neurosci. 2006 Jun 21;26(25):6737-48 - PubMed
  61. J Psychiatry Neurosci. 2005 Sep;30(5):315-8 - PubMed
  62. Neuroendocrinology. 2007;85(3):158-76 - PubMed
  63. Dev Psychobiol. 1986 Nov;19(6):615-23 - PubMed
  64. J Comp Physiol Psychol. 1972 Nov;81(2):281-90 - PubMed
  65. J Comp Physiol Psychol. 1967 Aug;64(1):114-20 - PubMed
  66. Neuropharmacology. 2007 Jan;52(1):215-27 - PubMed
  67. Physiol Behav. 1992 Oct;52(4):787-91 - PubMed
  68. Dev Psychobiol. 2010 Jul;52(5):453-64 - PubMed
  69. Behav Brain Res. 2001 Nov 29;126(1-2):147-57 - PubMed
  70. Dev Psychobiol. 1993 Jul;26(5):261-77 - PubMed
  71. Curr Opin Neurobiol. 2002 Apr;12(2):205-10 - PubMed
  72. Behav Neural Biol. 1980 May;29(1):132-6 - PubMed
  73. Psychoneuroendocrinology. 1995;20(2):169-82 - PubMed
  74. Learn Mem. 2001 May-Jun;8(3):148-55 - PubMed
  75. J Comp Physiol Psychol. 1980 Aug;94(4):650-63 - PubMed
  76. Behav Neurosci. 1996 Jun;110(3):583-92 - PubMed
  77. Cell Mol Neurobiol. 1993 Aug;13(4):321-47 - PubMed
  78. Learn Mem. 2000 Nov-Dec;7(6):413-21 - PubMed
  79. Nat Rev Neurosci. 2005 Jun;6(6):463-75 - PubMed
  80. Braz J Med Biol Res. 2010 Oct;43(10):914-9 - PubMed
  81. Dev Psychobiol. 1985 May;18(3):215-27 - PubMed
  82. Science. 2003 Jul 18;301(5631):386-9 - PubMed
  83. J Comp Physiol Psychol. 1973 Jun;83(3):374-8 - PubMed
  84. Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15716-21 - PubMed
  85. Br Med Bull. 1997 Jan;53(1):170-84 - PubMed
  86. Physiol Behav. 1975 Mar;14(3):311-9 - PubMed
  87. Physiol Rev. 2003 Jul;83(3):803-34 - PubMed
  88. Ann N Y Acad Sci. 1994 Nov 30;746:275-88; discussion 289-93 - PubMed
  89. Prog Brain Res. 2000;122:81-103 - PubMed
  90. Brain Res Dev Brain Res. 1990 May 1;53(2):243-7 - PubMed
  91. Psychoneuroendocrinology. 2005 Nov;30(10):939-46 - PubMed
  92. Front Behav Neurosci. 2009 Sep 01;3:22 - PubMed
  93. Int J Psychophysiol. 1999 Nov;34(2):147-62 - PubMed
  94. J Clin Psychiatry. 2003 Feb;64(2):202-7 - PubMed
  95. Dev Psychobiol. 1999 Mar;34(2):87-99 - PubMed
  96. NIDA Res Monogr. 1995;158:172-201 - PubMed
  97. Brain Res. 1986 May;391(2):289-92 - PubMed
  98. J Neurosci. 2009 Dec 16;29(50):15745-55 - PubMed
  99. Learn Mem. 2003 Jan-Feb;10(1):1-4 - PubMed
  100. Learn Mem. 2009 Jan 29;16(2):114-21 - PubMed
  101. Brain Res. 1996 Apr 15;716(1-2):149-56 - PubMed
  102. J Neurophysiol. 1987 Sep;58(3):510-24 - PubMed
  103. Ann N Y Acad Sci. 2006 Jul;1071:521-4 - PubMed
  104. J Neurosci. 2012 May 30;32(22):7758-65 - PubMed
  105. Ann N Y Acad Sci. 1994 Nov 30;746:294-304; discussion 304-7 - PubMed
  106. Dev Psychobiol. 2009 Jan;51(1):95-105 - PubMed
  107. Neuropharmacology. 1998 Apr-May;37(4-5):623-32 - PubMed
  108. Nat Neurosci. 2006 Aug;9(8):1004-6 - PubMed
  109. Endocrinology. 1991 Mar;128(3):1385-95 - PubMed
  110. Biol Psychiatry. 2003 May 15;53(10):854-62 - PubMed
  111. Brain Res. 1969 Jul;14(2):427-45 - PubMed
  112. Physiol Behav. 2009 Mar 23;96(4-5):532-9 - PubMed
  113. Biol Psychiatry. 2010 Jun 15;67(12):1137-45 - PubMed
  114. Neuroscience. 2008 Jun 26;154(3):1132-42 - PubMed
  115. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7261-5 - PubMed
  116. Psychosom Med. 1995 Sep-Oct;57(5):468-74 - PubMed
  117. Behav Neurosci. 1993 Apr;107(2):254-63 - PubMed
  118. Learn Mem. 2008 Aug 26;15(9):649-56 - PubMed
  119. Endocrinology. 2008 Oct;149(10):4892-900 - PubMed
  120. Dev Psychobiol. 1988 Jan;21(1):25-42 - PubMed
  121. Ind Health. 1999 Apr;37(2):143-56 - PubMed
  122. J Comp Physiol Psychol. 1980 Aug;94(4):588-95 - PubMed
  123. Endocrinology. 2000 May;141(5):1590-2 - PubMed
  124. Mol Neurobiol. 2003 Apr;27(2):121-36 - PubMed
  125. Adv Exp Med Biol. 1990;265:269-76 - PubMed
  126. J Neurosci. 2004 Feb 4;24(5):1182-9 - PubMed
  127. Behav Neural Biol. 1988 Jul;50(1):16-23 - PubMed
  128. Nat Neurosci. 2009 Nov;12(11):1367-9 - PubMed
  129. Behav Neurosci. 1991 Dec;105(6):843-9 - PubMed
  130. Prog Neurobiol. 1997 Nov;53(4):399-430 - PubMed
  131. J Neurosci. 1987 Oct;7(10):3154-62 - PubMed
  132. Acta Pharmacol Sin. 2000 Jun;21(6):481-93 - PubMed
  133. Brain Res. 2000 May 19;865(1):45-58 - PubMed
  134. Ann N Y Acad Sci. 2003 Apr;985:125-34 - PubMed
  135. J Neurosci. 2007 Apr 18;27(16):4482-91 - PubMed
  136. Dev Psychobiol. 1980 Sep;13(5):513-8 - PubMed
  137. Physiol Behav. 1976 Jul;17(1):131-6 - PubMed
  138. Brain Res. 1986 Jun;392(1-2):278-82 - PubMed
  139. Nat Rev Neurosci. 2005 Jul;6(7):507-20 - PubMed
  140. Brain Res Dev Brain Res. 1997 Sep 20;102(2):291-3 - PubMed
  141. Pediatr Res. 2009 Sep;66(3):272-7 - PubMed
  142. Am J Prev Med. 2006 Dec;31(6 Suppl 1):S175-81 - PubMed
  143. Neuron. 1999 Jun;23(2):229-32 - PubMed
  144. Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6741-6 - PubMed
  145. Annu Rev Neurosci. 1992;15:353-75 - PubMed
  146. Synapse. 1999 Apr;32(1):37-43 - PubMed
  147. J Comp Physiol Psychol. 1962 Oct;55:819-20 - PubMed
  148. Dev Psychobiol. 1980 Mar;13(2):141-50 - PubMed
  149. J Neurosci. 2006 Mar 1;26(9):2434-42 - PubMed
  150. Dev Psychobiol. 2001 Jul;39(1):8-18 - PubMed
  151. Neurogastroenterol Motil. 2007 Sep;19(9):761-8 - PubMed
  152. Neurosci Biobehav Rev. 1992 Winter;16(4):553-68 - PubMed
  153. Prog Neurobiol. 1990;34(6):505-26 - PubMed
  154. Cell Mol Neurobiol. 1993 Aug;13(4):295-319 - PubMed
  155. J Neurophysiol. 2002 Jun;87(6):3156-9 - PubMed
  156. Dev Psychopathol. 2001 Summer;13(3):419-49 - PubMed
  157. J Neurosci. 1993 Sep;13(9):3839-47 - PubMed
  158. Biol Psychiatry. 2010 Aug 15;68(4):314-9 - PubMed
  159. J Neuroendocrinol. 1999 Dec;11(12):925-33 - PubMed
  160. Dev Psychobiol. 1984 Mar;17(2):161-81 - PubMed
  161. Science. 1980 Oct 3;210(4465):15-22 - PubMed
  162. Behav Neurosci. 1991 Apr;105(2):307-12 - PubMed
  163. Sci Am. 1963 Jun;208:138-46 - PubMed
  164. Behav Neurosci. 2007 Dec;121(6):1293-305 - PubMed
  165. Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):33-44 - PubMed
  166. J Comp Neurol. 1991 Feb 15;304(3):467-77 - PubMed
  167. Ann N Y Acad Sci. 2003 Dec;1008:132-9 - PubMed
  168. Biol Psychiatry. 2005 Apr 15;57(8):823-31 - PubMed
  169. Brain Res Mol Brain Res. 1993 May;18(3):195-200 - PubMed
  170. Brain Res. 1994 Apr 18;643(1-2):306-9 - PubMed
  171. Prog Brain Res. 1970;32:79-85 - PubMed
  172. Horm Behav. 2002 Aug;42(1):42-52 - PubMed
  173. Behav Brain Res. 2000 Jun 1;110(1-2):25-37 - PubMed
  174. Behav Brain Res. 2010 Dec 25;214(2):268-76 - PubMed
  175. Physiol Behav. 2003 Aug;79(3):399-407 - PubMed
  176. Biol Psychiatry. 2001 Jun 15;49(12):1023-39 - PubMed
  177. Behav Neurosci. 1998 Dec;112(6):1430-7 - PubMed
  178. Physiol Behav. 1979 Sep;23(3):615-8 - PubMed
  179. Science. 1981 Jan 30;211(4481):506-8 - PubMed
  180. Brain Res Mol Brain Res. 1994 Jan;21(1-2):133-49 - PubMed
  181. Behav Neurosci. 1993 Oct;107(5):860-6 - PubMed
  182. Annu Rev Psychol. 2007;58:145-73 - PubMed
  183. Neuron. 2011 Nov 17;72(4):506-19 - PubMed
  184. Endocrinology. 1994 Dec;135(6):2549-57 - PubMed
  185. Psychiatr Clin North Am. 2002 Jun;25(2):397-426, vii-viii - PubMed
  186. Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):57-71 - PubMed
  187. Behav Neural Biol. 1993 Sep;60(2):152-62 - PubMed
  188. Psychoneuroendocrinology. 1983;8(4):401-9 - PubMed
  189. Ann N Y Acad Sci. 2003 Apr;985:106-13 - PubMed
  190. Horm Behav. 2005 Feb;47(2):139-50 - PubMed
  191. Neurosci Biobehav Rev. 2003 Sep;27(4):307-28 - PubMed
  192. Nat Neurosci. 2004 Aug;7(8):791-2 - PubMed
  193. Int J Psychiatry. 1965 Jan;1:43-51 - PubMed
  194. Neurosci Biobehav Rev. 2010 May;34(6):835-44 - PubMed
  195. Ann N Y Acad Sci. 2003 Dec;1008:304-7 - PubMed
  196. J Comp Neurol. 2004 Aug 30;476(4):414-28 - PubMed
  197. Science. 1977 Nov 11;198(4317):635-6 - PubMed
  198. J Comp Neurol. 1984 Feb 20;223(2):177-202 - PubMed
  199. Behav Neurosci. 2000 Oct;114(5):957-62 - PubMed
  200. Endocrinology. 1984 Oct;115(4):1364-70 - PubMed
  201. Nature. 2000 Sep 7;407(6800):38-9 - PubMed
  202. J Comp Neurol. 1991 Jan 22;303(4):637-57 - PubMed
  203. J Neurosci. 1998 Nov 15;18(22):9529-38 - PubMed
  204. Annu Rev Neurosci. 2000;23:155-84 - PubMed
  205. Physiol Behav. 1981 Nov;27(5):811-7 - PubMed
  206. Curr Opin Neurobiol. 2010 Aug;20(4):441-9 - PubMed
  207. Brain Res. 1995 Nov 20;699(2):192-200 - PubMed
  208. Trends Neurosci. 1998 Aug;21(8):323-31 - PubMed
  209. Brain Res. 1985 Oct;354(2):314-7 - PubMed
  210. Behav Neurosci. 1991 Jun;105(3):450-8 - PubMed
  211. Dev Psychobiol. 2001 Nov;39(3):188-98 - PubMed
  212. Eur J Neurosci. 2003 Oct;18(7):2031-6 - PubMed
  213. Philos Trans R Soc Lond B Biol Sci. 2006 Dec 29;361(1476):2215-28 - PubMed
  214. Neurosci Lett. 1995 Jun 2;192(1):49-52 - PubMed
  215. Behav Neural Biol. 1994 Jan;61(1):1-18 - PubMed
  216. Front Behav Neurosci. 2009 Sep 24;3:27 - PubMed
  217. Psychol Rev. 1972 May;79(3):215-36 - PubMed
  218. Trends Cogn Sci. 2006 Aug;10(8):345-7 - PubMed
  219. Behav Neurosci. 1986 Jun;100(3):359-67 - PubMed
  220. Science. 1962 Mar 9;135(3506):795-6 - PubMed
  221. J Neurosci. 2011 Apr 6;31(14):5348-52 - PubMed

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