Neuroimaging of human and non-human animal emotion and affect in the context of social relationships.

Pauline B Zablocki-Thomas, Forrest D Rogers, Karen L Bales
Author Information
  1. Pauline B Zablocki-Thomas: California National Primate Research Center, Davis, CA, United States.
  2. Forrest D Rogers: Princeton Neuroscience Institute, Princeton University, Princeton, NJ, United States.
  3. Karen L Bales: California National Primate Research Center, Davis, CA, United States.

Abstract

Long-term relationships are essential for the psychological wellbeing of humans and many animals. Positive emotions and affective experiences (e.g., romantic or platonic love) seem to be closely related to the creation and maintenance of social bonds. When relationships are threatened or terminated, other emotions generally considered to be negative can arise (e.g., jealousy or loneliness). Because humans and animals share (to varying degrees) common evolutionary histories, researchers have attempted to explain the evolution of affect and emotion through the comparative approach. Now brain imaging techniques allow the comparison of the neurobiological substrates of affective states and emotion in human and animal brains using a common methodology. Here, we review brain imaging studies that feature emotions characterized by the context of social bonding. We compare imaging findings associated with affective and emotional states elicited by similar social situations between humans and animal models. We also highlight the role of key neurohormones (i.e., oxytocin, vasopressin, and dopamine) that jointly support the occurrence of socially contextualized emotions and affect across species. In doing so, we seek to explore and clarify if and how humans and animals might similarly experience social emotion and affect in the context of social relationships.

Keywords

References

  1. Proc Natl Acad Sci U S A. 2021 Sep 14;118(37): [PMID: 34493677]
  2. Curr Opin Neurobiol. 2016 Oct;40:8-13 [PMID: 27290660]
  3. Eur J Neurosci. 2003 Aug;18(3):667-74 [PMID: 12911762]
  4. Front Endocrinol (Lausanne). 2017 Dec 22;8:356 [PMID: 29312146]
  5. Brain Res. 2007 Dec 12;1184:245-53 [PMID: 17976540]
  6. Eur J Neurosci. 2019 Nov;50(10):3674-3687 [PMID: 31336003]
  7. Neurosci Biobehav Rev. 2011 Oct;35(9):1791-804 [PMID: 21872619]
  8. Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):2126-31 [PMID: 22308343]
  9. Nat Neurosci. 2002 Mar;5(3):277-83 [PMID: 11850635]
  10. Neuroimage. 2006 Sep;32(3):1299-307 [PMID: 16829139]
  11. Trends Cogn Sci. 1999 Jan;3(1):11-21 [PMID: 10234222]
  12. Soc Cogn Affect Neurosci. 2017 Jan 1;12(1):95-105 [PMID: 27803286]
  13. Behav Brain Sci. 2010 Jun;33(2-3):61-83; discussion 83-135 [PMID: 20550733]
  14. Anim Cogn. 2018 May;21(3):331-343 [PMID: 29488110]
  15. Science. 1988 Jul 29;241(4865):540-5 [PMID: 3399889]
  16. Annu Rev Psychol. 2008;59:279-300 [PMID: 17550343]
  17. Curr Opin Neurobiol. 2021 Jun;68:52-56 [PMID: 33498010]
  18. Soc Cogn Affect Neurosci. 2015 Jan;10(1):19-27 [PMID: 25140048]
  19. Annu Rev Psychol. 2015 Jan 3;66:601-29 [PMID: 25251482]
  20. PLoS One. 2019 Oct 24;14(10):e0223675 [PMID: 31648222]
  21. Trends Cogn Sci. 2017 Apr;21(4):265-276 [PMID: 28214131]
  22. Soc Cogn Affect Neurosci. 2015 Feb;10(2):278-84 [PMID: 24752071]
  23. Ann N Y Acad Sci. 2011 Apr;1224:191-206 [PMID: 21486301]
  24. Front Neuroanat. 2011 Mar 02;5:13 [PMID: 21427780]
  25. Biol Psychiatry. 2008 Feb 15;63(4):415-23 [PMID: 17686467]
  26. J Sex Med. 2010 Nov;7(11):3541-52 [PMID: 20807326]
  27. Cult Med Psychiatry. 1984 Sep;8(3):283-309 [PMID: 6488847]
  28. Horm Behav. 2012 Mar;61(3):239-50 [PMID: 22269661]
  29. Soc Cogn Affect Neurosci. 2012 Feb;7(2):145-59 [PMID: 21208991]
  30. Psychol Sci. 2010 Jul;21(7):931-7 [PMID: 20548058]
  31. Neuropsychopharmacology. 2021 Oct;46(11):1873-1887 [PMID: 34230607]
  32. Nat Rev Neurosci. 2001 Feb;2(2):129-36 [PMID: 11252992]
  33. Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20308-13 [PMID: 24277856]
  34. Trends Cogn Sci. 2005 Nov;9(11):506-7; author reply 508-10 [PMID: 16199197]
  35. Front Ecol Evol. 2017 Oct;5: [PMID: 29682503]
  36. Behav Brain Res. 2010 Feb 11;207(1):196-207 [PMID: 19819265]
  37. Am J Psychiatry. 2003 Nov;160(11):1946-53 [PMID: 14594740]
  38. Nat Commun. 2018 Jan 30;9(1):332 [PMID: 29382820]
  39. Pers Soc Psychol Rev. 2003;7(2):102-28 [PMID: 12676643]
  40. Neuroimage. 2021 Feb 15;227:117666 [PMID: 33359341]
  41. Proc Biol Sci. 2004 Dec 7;271 Suppl 6:S468-70 [PMID: 15801606]
  42. Sci Rep. 2020 Oct 5;10(1):16503 [PMID: 33020542]
  43. Psychosom Med. 2012 Feb-Mar;74(2):126-35 [PMID: 22286852]
  44. Elife. 2020 Jun 09;9: [PMID: 32513386]
  45. Curr Biol. 2012 Dec 4;22(23):2268-73 [PMID: 23122847]
  46. Soc Cogn Affect Neurosci. 2012 Nov;7(8):969-79 [PMID: 22021653]
  47. Neuroscience. 2014 Jul 25;273:12-23 [PMID: 24814726]
  48. PLoS One. 2011;6(6):e20720 [PMID: 21694758]
  49. Philos Trans R Soc Lond B Biol Sci. 2022 Aug 29;377(1858):20210118 [PMID: 35858098]
  50. Psychol Bull. 2001 Jan;127(1):45-86 [PMID: 11271756]
  51. Int J Primatol. 2014 Feb 1;35(1):188-209 [PMID: 24659840]
  52. J Neurosci. 2005 Jan 5;25(1):149-56 [PMID: 15634776]
  53. Soc Cogn Affect Neurosci. 2017 Jan 1;12(1):1-23 [PMID: 27798257]
  54. Annu Rev Psychol. 2014;65:17-39 [PMID: 24050183]
  55. Curr Opin Psychol. 2017 Oct;17:184-188 [PMID: 28950967]
  56. Science. 2016 Jan 22;351(6271):375-8 [PMID: 26798013]
  57. J Pers Soc Psychol. 1987 Mar;52(3):511-24 [PMID: 3572722]
  58. Science. 2017 Sep 29;357(6358):1353-1354 [PMID: 28963241]
  59. Neuroimage. 2017 Jan 15;145(Pt A):74-81 [PMID: 27664826]
  60. Brain Res. 1991 Aug 2;555(2):220-32 [PMID: 1657300]
  61. Sci Rep. 2021 Feb 12;11(1):3746 [PMID: 33580133]
  62. Trends Cogn Sci. 2004 Jul;8(7):294-300 [PMID: 15242688]
  63. Ann N Y Acad Sci. 2014 May;1316:1-17 [PMID: 24329760]
  64. Brain Res. 1988 May 31;450(1-2):111-23 [PMID: 3401705]
  65. Science. 2003 Oct 10;302(5643):290-2 [PMID: 14551436]
  66. Horm Behav. 2016 Jan;77:98-112 [PMID: 26062432]
  67. Nat Rev Neurosci. 2017 Feb;18(2):115-126 [PMID: 28053326]
  68. Nature. 2004 Jan 22;427(6972):312 [PMID: 14737158]
  69. Biol Psychiatry. 2004 Sep 1;56(5):364-75 [PMID: 15336519]
  70. J Pers Assess. 1978 Jun;42(3):290-4 [PMID: 660402]
  71. CNS Spectr. 2004 Apr;9(4):258-66 [PMID: 15048050]
  72. Front Psychol. 2020 Jan 28;11:25 [PMID: 32047459]
  73. Trends Cogn Sci. 2018 Jan;22(1):32-51 [PMID: 29273112]
  74. Psychoneuroendocrinology. 2016 Feb;64:66-78 [PMID: 26615473]
  75. Biol Psychiatry. 2016 Feb 1;79(3):194-202 [PMID: 26321019]
  76. Soc Cogn Affect Neurosci. 2014 Feb;9(2):209-17 [PMID: 23171617]
  77. Biol Psychiatry. 2001 Jan 15;49(2):146-57 [PMID: 11164761]
  78. Biol Lett. 2006 Mar 22;2(1):36-8 [PMID: 17148320]
  79. Emotion. 2020 Sep;20(6):993-1004 [PMID: 31192659]
  80. J Neuroendocrinol. 2016 Apr;28(4): [PMID: 26940141]
  81. Neuroimage. 2011 Mar 1;55(1):381-8 [PMID: 21122817]
  82. J Comp Neurol. 2017 Apr 1;525(5):1094-1108 [PMID: 27615433]
  83. Front Psychol. 2019 Dec 04;10:2709 [PMID: 31866904]
  84. Hum Nat. 1990 Sep;1(3):261-89 [PMID: 24222085]
  85. Trends Neurosci. 1999 Jul;22(7):310-6 [PMID: 10370255]
  86. Biol Psychiatry. 2009 Jul 1;66(1):33-40 [PMID: 19249748]
  87. Soc Cogn Affect Neurosci. 2020 May 19;15(3):261-271 [PMID: 32232362]
  88. Brain Behav Evol. 2006;67(4):177-87 [PMID: 16432299]
  89. Biol Psychiatry. 2002 Mar 15;51(6):431-45 [PMID: 11922877]
  90. Neurosci Lett. 2009 Sep 25;461(3):217-22 [PMID: 19539696]
  91. ILAR J. 2014;55(2):259-73 [PMID: 25225305]
  92. Neuroscience. 2017 Apr 21;348:302-312 [PMID: 28242440]
  93. Brain Res. 2006 Mar 24;1079(1):4-14 [PMID: 16460715]
  94. Neurosci Lett. 2012 Sep 20;526(1):33-8 [PMID: 22902992]
  95. Nat Neurosci. 2013 Feb;16(2):243-50 [PMID: 23263442]
  96. J Comp Neurol. 2005 Dec 5;493(1):58-62 [PMID: 16255001]
  97. Bioorg Med Chem Lett. 2016 Jul 15;26(14):3370-3375 [PMID: 27209233]
  98. Behav Neurosci. 1994 Dec;108(6):1163-71 [PMID: 7893408]
  99. Psychol Rev. 2003 Jan;110(1):145-72 [PMID: 12529060]
  100. Science. 2012 Jun 1;336(6085):1154-7 [PMID: 22654056]
  101. Horm Behav. 2016 Feb;78:20-31 [PMID: 26476409]
  102. Horm Behav. 2021 Nov;136:105062 [PMID: 34601430]
  103. Cell. 2014 Mar 27;157(1):187-200 [PMID: 24679535]
  104. Front Behav Neurosci. 2016 Nov 14;10:221 [PMID: 27895565]
  105. Horm Behav. 2005 Jun;48(1):11-22 [PMID: 15885690]
  106. Behav Pharmacol. 2021 Apr 1;32(2&3):96-111 [PMID: 33136617]
  107. Brain Res Cogn Brain Res. 2005 May;23(2-3):448-52 [PMID: 15820652]
  108. Depress Anxiety. 1999;10(3):99-104 [PMID: 10604082]
  109. Proc Biol Sci. 2010 Oct 7;277(1696):2895-904 [PMID: 20685706]
  110. Front Psychol. 2020 May 07;11:634 [PMID: 32457675]
  111. Brain Sci. 2022 Jun 26;12(7): [PMID: 35884637]
  112. Nature. 1993 Oct 7;365(6446):545-8 [PMID: 8413608]
  113. J Pers Soc Psychol. 1993 Jun;64(6):906-20 [PMID: 8326472]
  114. Neuron. 2020 Feb 19;105(4):600-603 [PMID: 32078795]
  115. Neuroreport. 2000 Nov 27;11(17):3829-34 [PMID: 11117499]
  116. Hum Brain Mapp. 2011 Feb;32(2):249-57 [PMID: 21229613]
  117. Dev Psychobiol. 2020 Jul;62(5):573-590 [PMID: 31823359]
  118. Neurosci Biobehav Rev. 2011 Jan;35(3):565-72 [PMID: 20620164]
  119. Neuroimage. 2008 Aug 15;42(2):969-72 [PMID: 18559294]
  120. Q Rev Biol. 1977 Mar;52(1):39-69 [PMID: 857268]
  121. Soc Neurosci. 2020 Oct;15(5):571-583 [PMID: 32715953]
  122. J Psychopharmacol. 2021 Jun;35(6):668-680 [PMID: 33601928]
  123. J Clin Psychol Med Settings. 2021 Sep;28(3):637-648 [PMID: 33392890]
  124. J Comp Physiol Psychol. 1974 May;86(5):957-72 [PMID: 4833599]
  125. Appl Anim Behav Sci. 2018 Aug;205:202-209 [PMID: 30078924]
  126. Neurosci Biobehav Rev. 2020 Jun;113:273-286 [PMID: 31982603]
  127. Front Hum Neurosci. 2015 Apr 09;9:191 [PMID: 25914637]
  128. Am J Primatol. 2017 Mar;79(3):1-9 [PMID: 27757971]
  129. Neuroimage. 2008 Jan 15;39(2):903-10 [PMID: 17964185]
  130. Affect Sci. 2020 Nov 3;1(4):199-207 [PMID: 36042816]
  131. Brain Struct Funct. 2022 Jun;227(5):1907-1919 [PMID: 34482474]
  132. Psychoneuroendocrinology. 2014 Jul;45:128-41 [PMID: 24845184]
  133. Neuroimage. 2004 Mar;21(3):1155-66 [PMID: 15006682]

Grants

  1. R01 HD092055/NICHD NIH HHS

Word Cloud

Created with Highcharts 10.0.0socialrelationshipsemotionsaffecthumansemotionimaginganimalsaffectiveeanimalcontextgcommonbrainstateshumanneurohormonesLong-termessentialpsychologicalwellbeingmanyPositiveexperiencesromanticplatonicloveseemcloselyrelatedcreationmaintenancebondsthreatenedterminatedgenerallyconsiderednegativecanarisejealousylonelinesssharevaryingdegreesevolutionaryhistoriesresearchersattemptedexplainevolutioncomparativeapproachNowtechniquesallowcomparisonneurobiologicalsubstratesbrainsusingmethodologyreviewstudiesfeaturecharacterizedbondingcomparefindingsassociatedemotionalelicitedsimilarsituationsmodelsalsohighlightrolekeyioxytocinvasopressindopaminejointlysupportoccurrencesociallycontextualizedacrossspeciesseekexploreclarifymightsimilarlyexperienceNeuroimagingnon-human

Similar Articles

Cited By