Stress responses and the mesolimbic dopamine system: social contexts and sex differences.

Brian C Trainor
Author Information
  1. Brian C Trainor: Department of Psychology, University of California, 1 Shields Ave., Davis, CA 95616, USA.

Abstract

Organisms react to threats with a variety of behavioral, hormonal, and neurobiological responses. The study of biological responses to stress has historically focused on the hypothalamic-pituitary-adrenal axis, but other systems such as the mesolimbic dopamine system are involved. Behavioral neuroendocrinologists have long recognized the importance of the mesolimbic dopamine system in mediating the effects of hormones on species specific behavior, especially aspects of reproductive behavior. There has been less focus on the role of this system in the context of stress, perhaps due to extensive data outlining its importance in reward or approach-based contexts. However, there is steadily growing evidence that the mesolimbic dopamine neurons have critical effects on behavioral responses to stress. Most of these data have been collected from experiments using a small number of animal model species under a limited set of contexts. This approach has led to important discoveries, but evidence is accumulating that mesolimbic dopamine responses are context dependent. Thus, focusing on a limited number of species under a narrow set of controlled conditions constrains our understanding of how the mesolimbic dopamine system regulates behavior in response to stress. Both affiliative and antagonistic social interactions have important effects on mesolimbic dopamine function, and there is preliminary evidence for sex differences as well. This review will highlight the benefits of expanding this approach, and focus on how social contexts and sex differences can impact mesolimbic dopamine stress responses.

References

  1. Prog Neurobiol. 2004 Dec;74(5):301-20 [PMID: 15582224]
  2. Psychoneuroendocrinology. 2007 Sep-Nov;32(8-10):966-80 [PMID: 17825994]
  3. Brain Res. 2003 Dec 5;992(2):227-38 [PMID: 14625061]
  4. Neurosci Lett. 2001 Oct 5;311(3):189-92 [PMID: 11578826]
  5. Neuropsychopharmacology. 2005 Jan;30(1):17-26 [PMID: 15257308]
  6. Biol Lett. 2008 Jun 23;4(3):253-5 [PMID: 18397863]
  7. Synapse. 1998 May;29(1):80-3 [PMID: 9552177]
  8. Pharmacol Biochem Behav. 2011 Jun;98(4):575-82 [PMID: 21396951]
  9. Brain Res. 2005 Feb 28;1035(2):168-76 [PMID: 15722056]
  10. Neuroscience. 1988 Oct;27(1):1-39 [PMID: 3059226]
  11. Learn Mem. 2011 Feb 16;18(3):136-43 [PMID: 21325435]
  12. Proc Natl Acad Sci U S A. 2009 May 26;106(21):8737-42 [PMID: 19439662]
  13. Life Sci. 1982 Jun 21;30(25):2207-14 [PMID: 6180276]
  14. Horm Behav. 1997 Dec;32(3):143-54 [PMID: 9454665]
  15. Front Neuroendocrinol. 2003 Jul;24(3):151-80 [PMID: 14596810]
  16. Behav Neurosci. 1995 Apr;109(2):354-65 [PMID: 7619325]
  17. Biol Psychiatry. 2000 Dec 15;48(12):1157-63 [PMID: 11137057]
  18. Eur J Neurosci. 2003 Oct;18(7):1997-2001 [PMID: 14622232]
  19. Psychoneuroendocrinology. 2006 Feb;31(2):237-49 [PMID: 16157456]
  20. Brain Res. 1989 Jan 9;476(2):377-81 [PMID: 2702475]
  21. J Neurosci. 2011 Feb 23;31(8):3095-103 [PMID: 21414930]
  22. Primates. 1999 Jan;40(1):105-30 [PMID: 23179535]
  23. Psychopharmacology (Berl). 2006 Jun;186(3):362-72 [PMID: 16432684]
  24. Biol Psychiatry. 2009 May 1;65(9):760-9 [PMID: 19150054]
  25. J Neurochem. 2006 Jan;96(1):236-46 [PMID: 16300631]
  26. Behaviour. 1966;26(1):91-104 [PMID: 4955110]
  27. Brain Res. 2002 Feb 1;926(1-2):10-7 [PMID: 11814401]
  28. Horm Behav. 2005 Jun;48(1):64-74 [PMID: 15919386]
  29. Behav Neurosci. 1989 Feb;103(1):36-45 [PMID: 2493791]
  30. Psychopharmacology (Berl). 1985;87(1):43-50 [PMID: 3933036]
  31. Prog Neuropsychopharmacol Biol Psychiatry. 2003 Feb;27(1):21-30 [PMID: 12551722]
  32. Proc Natl Acad Sci U S A. 2005 Jun 7;102(23):8357-62 [PMID: 15923261]
  33. Brain Res. 1978 Mar 24;143(2):263-79 [PMID: 630409]
  34. Stress. 1996 Jul;1(1):21-32 [PMID: 9807059]
  35. Brain Behav Evol. 2007;70(4):218-26 [PMID: 17914253]
  36. Physiol Behav. 1979 Dec;23(6):1001-5 [PMID: 542507]
  37. Brain Res. 2010 Sep 24;1353:113-24 [PMID: 20633541]
  38. J Comp Neurol. 2001 Jul 16;436(1):64-81 [PMID: 11413547]
  39. Science. 2006 Feb 10;311(5762):864-8 [PMID: 16469931]
  40. Horm Behav. 2003 Jan;43(1):2-15 [PMID: 12614627]
  41. Behav Brain Res. 1999 Mar;99(2):169-79 [PMID: 10512583]
  42. J Comp Physiol Psychol. 1963 Jun;56:636-44 [PMID: 14001051]
  43. Neuroscience. 2005;135(3):703-14 [PMID: 16125862]
  44. Proc Natl Acad Sci U S A. 2009 Mar 24;106(12):4894-9 [PMID: 19261850]
  45. Psychoneuroendocrinology. 2002 Aug;27(6):683-91 [PMID: 12084661]
  46. Neuropsychobiology. 2005;52(2):90-110 [PMID: 16037678]
  47. Proc Natl Acad Sci U S A. 2008 Apr 8;105(14):5567-72 [PMID: 18391192]
  48. J Comp Psychol. 2005 Feb;119(1):111-6 [PMID: 15740435]
  49. Nat Neurosci. 2004 Oct;7(10):1040-7 [PMID: 15452575]
  50. Ann N Y Acad Sci. 1962 Dec 28;102:338-435 [PMID: 14012344]
  51. Pharmacol Biochem Behav. 1995 Jun-Jul;51(2-3):397-405 [PMID: 7667360]
  52. Nat Neurosci. 2006 Jan;9(1):133-9 [PMID: 16327783]
  53. PLoS One. 2008 Oct 01;3(10):e3281 [PMID: 18827927]
  54. J Neurosci. 2010 Dec 8;30(49):16453-8 [PMID: 21147984]
  55. Pharmacol Biochem Behav. 1998 Jun;60(2):585-92 [PMID: 9632244]
  56. Behav Neurosci. 1991 Oct;105(5):727-43 [PMID: 1840012]
  57. PLoS One. 2011 Feb 15;6(2):e17047 [PMID: 21347237]
  58. Psychoneuroendocrinology. 2005 Jul;30(6):550-7 [PMID: 15808924]
  59. J Neurochem. 1989 May;52(5):1655-8 [PMID: 2709017]
  60. Ann N Y Acad Sci. 2004 Dec;1032:63-84 [PMID: 15677396]
  61. Neuroscience. 1989;30(1):63-75 [PMID: 2664555]
  62. Prog Neuropsychopharmacol Biol Psychiatry. 2010 May 30;34(4):565-80 [PMID: 20206659]
  63. Horm Behav. 2010 Jun;58(1):1 [PMID: 20303970]
  64. Behav Brain Res. 1993 Jun 30;55(2):151-7 [PMID: 7689320]
  65. Neuron. 2010 Dec 9;68(5):815-34 [PMID: 21144997]
  66. Neuroscience. 1991;41(1):1-24 [PMID: 1676137]
  67. Nat Rev Neurosci. 2004 Jun;5(6):483-94 [PMID: 15152198]
  68. Neuroscience. 2010 May 19;167(3):598-607 [PMID: 20206238]
  69. Biol Psychiatry. 2009 May 15;65(10):874-80 [PMID: 19251249]
  70. Am J Primatol. 2000 Nov;52(3):115-31 [PMID: 11078026]
  71. Neurosci Lett. 1998 Sep 18;254(1):21-4 [PMID: 9780082]
  72. PLoS One. 2010 Dec 09;5(12):e15222 [PMID: 21151605]
  73. Physiol Behav. 2003 Nov;80(2-3):303-8 [PMID: 14637229]
  74. Neuroscience. 2011 Apr 14;179:104-19 [PMID: 21277950]
  75. Annu Rev Neurosci. 2006;29:565-98 [PMID: 16776597]
  76. J Endocrinol. 2009 Aug;202(2):223-36 [PMID: 19420011]
  77. Biol Psychiatry. 2006 Jun 15;59(12):1116-27 [PMID: 16631126]
  78. Eur J Neurosci. 2007 Apr;25(7):2201-13 [PMID: 17439498]
  79. Psychoneuroendocrinology. 2010 Jun;35(5):635-43 [PMID: 19857931]
  80. Pharmacopsychiatry. 2009 May;42 Suppl 1:S69-78 [PMID: 19434558]
  81. Physiol Behav. 1985 Dec;35(6):935-40 [PMID: 4095185]
  82. Psychopharmacology (Berl). 2007 Apr;191(3):461-82 [PMID: 17225164]
  83. Neurosci Biobehav Rev. 2010 May;34(6):845-52 [PMID: 19447133]
  84. J Neurochem. 1998 Jan;70(1):384-90 [PMID: 9422385]
  85. Cell. 2007 Oct 19;131(2):391-404 [PMID: 17956738]
  86. Behav Brain Res. 2010 Apr 2;208(2):528-34 [PMID: 20060017]
  87. Neuropsychopharmacology. 2005 Oct;30(10):1832-40 [PMID: 15886724]
  88. Neuroscience. 2002;113(2):395-400 [PMID: 12127096]
  89. Behav Neurosci. 2005 Feb;119(1):5-15 [PMID: 15727507]
  90. Biol Psychiatry. 1998 Nov 1;44(9):882-91 [PMID: 9807643]
  91. Biol Psychiatry. 1997 Apr 15;41(8):871-82 [PMID: 9099414]
  92. Brain Res Dev Brain Res. 1996 Apr 30;92(2):172-81 [PMID: 8738124]
  93. Neuroreport. 1997 Jul 28;8(11):2477-81 [PMID: 9261812]
  94. Behav Brain Res. 2008 Feb 11;187(1):109-15 [PMID: 17928072]
  95. Behav Brain Res. 2010 Jan 20;206(2):166-76 [PMID: 19747509]
  96. Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11435-40 [PMID: 12165570]
  97. Nat Neurosci. 2009 Feb;12(2):200-9 [PMID: 19151710]
  98. Neuroreport. 2004 Dec 22;15(18):2701-5 [PMID: 15597038]
  99. Physiol Behav. 2008 Feb 27;93(3):595-605 [PMID: 18031771]
  100. J Comp Neurol. 1973 Sep 15;151(2):121-58 [PMID: 4744471]
  101. Pharmacol Biochem Behav. 1995 Aug;51(4):681-6 [PMID: 7675843]
  102. Horm Behav. 2009 Jan;55(1):93-7 [PMID: 18835271]
  103. Behav Brain Res. 2000 Dec 20;117(1-2):137-46 [PMID: 11099767]
  104. Behav Brain Res. 2011 Mar 17;218(1):253-7 [PMID: 21129410]
  105. Am J Psychiatry. 1997 Feb;154(2):239-42 [PMID: 9016274]
  106. Horm Behav. 2002 Nov;42(3):294-306 [PMID: 12460589]
  107. Pharmacol Biochem Behav. 1999 Dec;64(4):803-12 [PMID: 10593204]
  108. Depress Anxiety. 2009;26(5):411-8 [PMID: 19180583]
  109. Pharmacol Ther. 2008 Nov;120(2):102-28 [PMID: 18789966]
  110. Nat Neurosci. 2002 Feb;5(2):169-74 [PMID: 11802171]
  111. J Physiol. 2006 Dec 15;577(Pt 3):907-24 [PMID: 16959856]
  112. Brain Res. 2000 May 2;864(1):146-51 [PMID: 10793199]
  113. J Comp Neurol. 1990 Dec 15;302(3):437-46 [PMID: 1702109]
  114. Behav Neurosci. 2005 Feb;119(1):224-32 [PMID: 15727527]
  115. Am J Psychiatry. 2000 Mar;157(3):457-9 [PMID: 10698826]
  116. J Neurosci. 1997 Jun 15;17(12):4849-55 [PMID: 9169543]
  117. Proc Biol Sci. 2005 May 7;272(1566):941-7 [PMID: 16024350]
  118. Neuroreport. 1997 Apr 14;8(6):1495-8 [PMID: 9172161]
  119. J Neuroendocrinol. 2009 Mar;21(4):415-20 [PMID: 19187468]
  120. Behav Brain Res. 1999 Dec;106(1-2):133-42 [PMID: 10595429]
  121. Neurosci Biobehav Rev. 2010 Nov;35(2):151-6 [PMID: 20438754]
  122. Psychoneuroendocrinology. 1988;13(6):515-20 [PMID: 3237947]
  123. Nat Neurosci. 2010 Nov;13(11):1351-3 [PMID: 20890295]
  124. Psychopharmacology (Berl). 1990;102(3):364-72 [PMID: 2251333]
  125. Neurosci Biobehav Rev. 2001 Jan;25(1):53-74 [PMID: 11166078]
  126. Horm Behav. 1989 Dec;23(4):473-502 [PMID: 2691387]
  127. Pharmacol Biochem Behav. 2006 Jan;83(1):28-34 [PMID: 16458953]
  128. Pharmacol Biochem Behav. 1991 Feb;38(2):315-20 [PMID: 2057501]
  129. Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12393-8 [PMID: 20616093]
  130. Pharmacol Biochem Behav. 1998 Apr;59(4):859-72 [PMID: 9586842]
  131. Front Psychiatry. 2011 May 09;2:24 [PMID: 21629841]
  132. J Neurosci. 2001 Sep 15;21(18):7397-403 [PMID: 11549750]
  133. Neuroscience. 2006 Dec;143(3):661-70 [PMID: 17027163]
  134. Physiol Behav. 2001 Jun;73(3):427-33 [PMID: 11438371]
  135. Psychopharmacology (Berl). 2007 Apr;191(3):391-431 [PMID: 17072591]
  136. J Neurosci. 2001 Aug 15;21(16):RC159 [PMID: 11459880]
  137. Physiol Behav. 1988;42(1):93-5 [PMID: 3387484]
  138. Nature. 1976 Sep 16;263(5574):242-4 [PMID: 958479]
  139. Learn Mem. 2010 Jun 28;17(7):337-43 [PMID: 20584920]
  140. Dev Psychobiol. 2009 Jul;51(5):417-28 [PMID: 19492363]
  141. Brain Res Bull. 1982 Jan;8(1):7-14 [PMID: 7055735]
  142. J Neurosci. 2003 Nov 26;23(34):10827-31 [PMID: 14645475]
  143. Science. 2004 Mar 26;303(5666):2040-2 [PMID: 15044807]
  144. Am J Psychiatry. 2012 Feb;169(2):205-12 [PMID: 22423352]
  145. Neuroscience. 2004;124(2):449-57 [PMID: 14980394]
  146. Neuropharmacology. 2004;47 Suppl 1:227-41 [PMID: 15464140]
  147. Brain Res Brain Res Rev. 1999 Dec;31(1):6-41 [PMID: 10611493]
  148. J Nucl Med. 2008 May;49(5):757-63 [PMID: 18413401]
  149. Psychopharmacology (Berl). 2005 Jun;179(4):769-80 [PMID: 15619113]
  150. J Psychopharmacol. 1996 Jan;10(1):39-47 [PMID: 22302726]
  151. Ann N Y Acad Sci. 1990;604:323-43 [PMID: 2171398]
  152. Psychoneuroendocrinology. 2007 Jul;32(6):587-603 [PMID: 17590276]
  153. Synapse. 2005 Sep 1;57(3):167-74 [PMID: 15945060]
  154. Behav Brain Res. 2002 Dec 2;137(1-2):115-27 [PMID: 12445718]
  155. J Comp Neurol. 2010 Feb 15;518(4):493-512 [PMID: 20020540]
  156. Eur J Neurosci. 2001 Mar;13(6):1254-6 [PMID: 11285023]
  157. Biol Psychiatry. 2008 Oct 15;64(8):691-700 [PMID: 18639865]
  158. J Neurochem. 2008 Aug;106(4):1780-90 [PMID: 18554320]
  159. Endocrinology. 1980 Feb;106(2):526-9 [PMID: 7353525]
  160. J Neurosci. 2002 Jun 1;22(11):4709-19 [PMID: 12040078]
  161. Neuroscience. 2003;118(1):123-34 [PMID: 12676144]
  162. J Comp Psychol. 1989 Mar;103(1):70-82 [PMID: 2924531]
  163. Psychopharmacology (Berl). 2008 Apr;197(2):203-16 [PMID: 18097654]
  164. J Neurosci. 2010 Jun 2;30(22):7652-63 [PMID: 20519540]
  165. Psychoneuroendocrinology. 1999 Apr;24(3):285-300 [PMID: 10101734]
  166. West J Med. 1998 Feb;168(2):93-7 [PMID: 9499742]
  167. Curr Neuropharmacol. 2006 Oct;4(4):277-91 [PMID: 18654637]
  168. Nat Neurosci. 2006 Apr;9(4):519-25 [PMID: 16501568]
  169. Annu Rev Neurosci. 1999;22:295-318 [PMID: 10202541]
  170. Brain Res. 1996 May 20;721(1-2):140-9 [PMID: 8793094]
  171. Behav Neurosci. 1997 Feb;111(1):219-24 [PMID: 9109641]
  172. Physiol Behav. 2009 Feb 16;96(2):218-32 [PMID: 18957299]
  173. Brain Res Mol Brain Res. 2001 Nov 30;96(1-2):77-81 [PMID: 11731011]
  174. Psychoneuroendocrinology. 1995;20(2):117-34 [PMID: 7899533]
  175. Horm Behav. 2003 Sep;44(3):185-98 [PMID: 14609541]
  176. Neurosci Biobehav Rev. 2011 Jan;35(3):565-72 [PMID: 20620164]
  177. Neurosci Biobehav Rev. 2011 Jan;35(3):794-803 [PMID: 20888857]
  178. Depress Anxiety. 2008;25(6):E17-26 [PMID: 17935206]
  179. PLoS One. 2011 Feb 25;6(2):e17405 [PMID: 21364768]
  180. Brain Res. 1992 Apr 17;577(2):194-9 [PMID: 1606494]
  181. Science. 1997 Mar 14;275(5306):1593-9 [PMID: 9054347]
  182. Horm Behav. 2010 Aug;58(3):506-12 [PMID: 20430027]
  183. Philos Trans R Soc Lond B Biol Sci. 2006 Jul 29;361(1471):1149-58 [PMID: 16874930]
  184. PLoS One. 2009;4(1):e4190 [PMID: 19142237]
  185. Brain Res. 1986 Nov 12;397(2):395-400 [PMID: 3801880]
  186. Physiol Behav. 2010 Feb 9;99(2):194-203 [PMID: 19419678]
  187. Eur J Pharmacol. 1978 Feb 15;47(4):379-91 [PMID: 204499]
  188. J Stud Alcohol Drugs. 2008 Sep;69(5):629-38 [PMID: 18781237]
  189. Neuroscience. 2009 Jun 16;161(1):3-12 [PMID: 19298844]
  190. Brain Res Dev Brain Res. 1991 Sep 19;62(1):109-14 [PMID: 1836980]
  191. Brain Res. 1995 Mar 27;675(1-2):325-8 [PMID: 7796146]
  192. Mol Psychiatry. 2004 Apr;9(4):326-57 [PMID: 14743184]
  193. Psychopharmacology (Berl). 2007 Apr;191(3):439-59 [PMID: 17318502]
  194. J Neurosci. 2001 May 1;21(9):3236-41 [PMID: 11312308]
  195. Psychopharmacology (Berl). 1995 Jan;117(1):116-24 [PMID: 7724696]
  196. Am J Psychiatry. 2010 Nov;167(11):1305-20 [PMID: 20843874]
  197. J Comp Neurol. 2002 May 6;446(3):288-300 [PMID: 11932944]
  198. J Comp Neurol. 1990 Apr 1;294(1):76-95 [PMID: 2324335]
  199. Behav Neurosci. 2003 Feb;117(1):150-68 [PMID: 12619918]
  200. J Comp Neurol. 2010 Aug 15;518(16):3302-26 [PMID: 20575061]

Grants

  1. R01 MH085069/NIMH NIH HHS
  2. R01MH085069/NIMH NIH HHS
  3. R21 MH090392-02/NIMH NIH HHS
  4. R21 MH090392/NIMH NIH HHS
  5. R01 MH085069-02/NIMH NIH HHS

MeSH Term

Animals
Dominance-Subordination
Dopamine
Dopaminergic Neurons
Female
Humans
Hypothalamo-Hypophyseal System
Male
Mice
Neural Pathways
Pituitary-Adrenal System
Pleasure
Rats
Sex Factors
Social Isolation
Stress, Psychological

Chemicals

Dopamine

Word Cloud

Created with Highcharts 10.0.0mesolimbicdopamineresponsesstresssystemcontextseffectsspeciesbehaviorevidencesocialsexdifferencesbehavioralimportancefocuscontextdatanumberlimitedsetapproachimportantOrganismsreactthreatsvarietyhormonalneurobiologicalstudybiologicalhistoricallyfocusedhypothalamic-pituitary-adrenalaxissystemsinvolvedBehavioralneuroendocrinologistslongrecognizedmediatinghormonesspecificespeciallyaspectsreproductivelessroleperhapsdueextensiveoutliningrewardapproach-basedHoweversteadilygrowingneuronscriticalcollectedexperimentsusingsmallanimalmodelleddiscoveriesaccumulatingdependentThusfocusingnarrowcontrolledconditionsconstrainsunderstandingregulatesresponseaffiliativeantagonisticinteractionsfunctionpreliminarywellreviewwillhighlightbenefitsexpandingcanimpactStresssystem:

Similar Articles

Cited By