The neural circuits of monogamous behavior.

María Fernanda López-Gutiérrez, Sara Mejía-Chávez, Sarael Alcauter, Wendy Portillo
Author Information
  1. María Fernanda López-Gutiérrez: Instituto de Neurobiología, Universidad Nacional Autónoma de México (UNAM), Querétaro, Mexico.
  2. Sara Mejía-Chávez: Instituto de Neurobiología, Universidad Nacional Autónoma de México (UNAM), Querétaro, Mexico.
  3. Sarael Alcauter: Instituto de Neurobiología, Universidad Nacional Autónoma de México (UNAM), Querétaro, Mexico.
  4. Wendy Portillo: Instituto de Neurobiología, Universidad Nacional Autónoma de México (UNAM), Querétaro, Mexico.

Abstract

The interest in studying the neural circuits related to mating behavior and mate choice in monogamous species lies in the parallels found between human social structure and sexual behavior and that of other mammals that exhibit social monogamy, potentially expanding our understanding of human neurobiology and its underlying mechanisms. Extensive research has suggested that social monogamy, as opposed to non-monogamy in mammals, is a consequence of the neural encoding of sociosensory information from the sexual partner with an increased reward value. Thus, the reinforced value of the mate outweighs the reward value of mating with any other potential sexual partners. This mechanism reinforces the social relationship of a breeding pair, commonly defined as a pair bond. In addition to accentuated prosocial behaviors toward the partner, other characteristic behaviors may appear, such as territorial and partner guarding, selective aggression toward unfamiliar conspecifics, and biparental care. Concomitantly, social buffering and distress upon partner separation are also observed. The following work intends to overview and compare known neural and functional circuits that are related to mating and sexual behavior in monogamous mammals. We will particularly discuss reports on Cricetid rodents of the and genus, and New World primates (NWP), such as the subfamily of the titi monkey and the marmoset (). In addition, we will mention the main factors that modulate the neural circuits related to social monogamy and how that modulation may reflect phenotypic differences, ultimately creating the widely observed diversity in social behavior.

Keywords

References

  1. Front Neural Circuits. 2017 Jun 13;11:41 [PMID: 28659766]
  2. Psychoneuroendocrinology. 2007 Sep-Nov;32(8-10):966-80 [PMID: 17825994]
  3. BMC Genomics. 2021 May 31;22(1):399 [PMID: 34058981]
  4. Ann N Y Acad Sci. 1992 Jun 12;652:448-51 [PMID: 1320837]
  5. J Comp Neurol. 1997 Feb 24;378(4):535-46 [PMID: 9034909]
  6. J Neuroendocrinol. 2021 Aug;33(8):e13001 [PMID: 34189787]
  7. Brain Res. 2007 Dec 12;1184:245-53 [PMID: 17976540]
  8. Am J Primatol. 1995;36(3):185-200 [PMID: 31924092]
  9. Front Neurosci. 2017 Jul 11;11:397 [PMID: 28744194]
  10. Horm Behav. 2010 Feb;57(2):255-62 [PMID: 20025881]
  11. J Neurosci. 2020 Mar 11;40(11):2282-2295 [PMID: 32024781]
  12. Behav Brain Res. 2019 Oct 17;372:112006 [PMID: 31170433]
  13. Eur J Neurosci. 2018 Jan;47(1):95-108 [PMID: 29205599]
  14. Psychoneuroendocrinology. 2007 May;32(4):331-49 [PMID: 17363175]
  15. Front Behav Neurosci. 2015 Oct 14;9:251 [PMID: 26528149]
  16. Psychoneuroendocrinology. 2014 Nov;49:1-10 [PMID: 25038478]
  17. Physiol Behav. 2003 Oct;80(1):95-101 [PMID: 14568313]
  18. Psychoneuroendocrinology. 2013 Jun;38(6):916-26 [PMID: 23102690]
  19. Integr Zool. 2014 Jun;9(3):280-93 [PMID: 24952968]
  20. Behav Neurosci. 2010 Feb;124(1):159-163 [PMID: 20141291]
  21. Nat Neurosci. 2013 Jul;16(7):919-24 [PMID: 23727821]
  22. PLoS One. 2016 Mar 09;11(3):e0150373 [PMID: 26959827]
  23. Mol Biol Evol. 2004 Jun;21(6):1057-63 [PMID: 15014156]
  24. Neuroscience. 2004;125(1):35-45 [PMID: 15051143]
  25. Psychoneuroendocrinology. 2020 Mar;113:104494 [PMID: 31862614]
  26. Science. 2013 Aug 2;341(6145):526-30 [PMID: 23896459]
  27. Behav Brain Res. 2021 Jun 25;408:113264 [PMID: 33775781]
  28. Adv Exp Med Biol. 2020;1253:3-55 [PMID: 32445090]
  29. J Cereb Blood Flow Metab. 1993 Jan;13(1):5-14 [PMID: 8417010]
  30. Horm Behav. 2019 Apr;110:46-55 [PMID: 30836063]
  31. Curr Biol. 2022 Mar 14;32(5):1026-1037.e4 [PMID: 35108521]
  32. Ann N Y Acad Sci. 2007 May;1104:192-212 [PMID: 17416920]
  33. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2011 Mar;197(3):267-77 [PMID: 21104088]
  34. Mol Ecol. 2009 Nov;18(22):4680-95 [PMID: 19821904]
  35. Horm Behav. 2012 Mar;61(3):445-53 [PMID: 22285648]
  36. Front Behav Neurosci. 2019 Sep 13;13:206 [PMID: 31572140]
  37. Eur J Neurosci. 2017 Oct;46(7):2276-2284 [PMID: 28858415]
  38. Nature. 2017 Jun 8;546(7657):297-301 [PMID: 28562592]
  39. Proc Natl Acad Sci U S A. 2015 Nov 10;112(45):14084-9 [PMID: 26504214]
  40. Nat Neurosci. 2004 Oct;7(10):1048-54 [PMID: 15452576]
  41. Neuron. 2017 Jul 19;95(2):368-384.e5 [PMID: 28669546]
  42. Horm Behav. 2017 Jan;87:16-24 [PMID: 27793769]
  43. Ann N Y Acad Sci. 1999 Jun 29;877:242-57 [PMID: 10415653]
  44. Science. 2013 Nov 1;342(6158):1238411 [PMID: 24179229]
  45. Neuroimage. 2016 Sep;138:221-232 [PMID: 27238726]
  46. J Comp Neurol. 2007 Jun 20;502(6):1109-22 [PMID: 17444499]
  47. J Neurosci. 2018 Feb 21;38(8):1942-1958 [PMID: 29348191]
  48. Physiol Behav. 1995 Apr;57(4):615-27 [PMID: 7777594]
  49. Biol Psychiatry. 2022 Jan 1;91(1):141-151 [PMID: 33549315]
  50. Biomed Pharmacother. 2020 May;125:109832 [PMID: 32018219]
  51. Nat Rev Neurosci. 2018 Nov;19(11):643-654 [PMID: 30301953]
  52. Nat Neurosci. 2006 Jan;9(1):133-9 [PMID: 16327783]
  53. Proc Biol Sci. 2015 Nov 22;282(1819): [PMID: 26609086]
  54. Front Ecol Evol. 2017 Oct;5: [PMID: 29682503]
  55. Nat Commun. 2017 Sep 14;8(1):537 [PMID: 28912554]
  56. Horm Behav. 2008 Nov;54(5):694-702 [PMID: 18722379]
  57. Biol Psychiatry Cogn Neurosci Neuroimaging. 2022 Jun;7(6):576-587 [PMID: 34839018]
  58. Trends Neurosci. 1998 Feb;21(2):71-5 [PMID: 9498302]
  59. Int J Neuropsychopharmacol. 2009 Jul;12(6):761-72 [PMID: 19102816]
  60. Mol Biol Evol. 2010 Jun;27(6):1269-78 [PMID: 20097658]
  61. Elife. 2018 Apr 20;7: [PMID: 29676731]
  62. Behav Neurosci. 2000 Feb;114(1):173-83 [PMID: 10718272]
  63. Biol Psychiatry. 2004 Jul 15;56(2):72-9 [PMID: 15231438]
  64. J Neurosci. 2017 Apr 12;37(15):4103-4116 [PMID: 28292834]
  65. Behav Brain Res. 2014 May 15;265:22-31 [PMID: 24561258]
  66. Behav Neurosci. 1999 Oct;113(5):1071-9 [PMID: 10571489]
  67. Psychoneuroendocrinology. 2021 Jun;128:105209 [PMID: 33839431]
  68. Front Neuroendocrinol. 2019 Apr;53:100737 [PMID: 30753840]
  69. Nature. 2004 Jun 17;429(6993):754-7 [PMID: 15201909]
  70. Front Neurosci. 2017 Oct 04;11:537 [PMID: 29085274]
  71. Sci Rep. 2018 Jan 19;8(1):1231 [PMID: 29352154]
  72. Neurosci Biobehav Rev. 1995 Summer;19(2):303-14 [PMID: 7630584]
  73. Am J Primatol. 2018 Oct;80(10):e22907 [PMID: 30106168]
  74. Genes Brain Behav. 2005 Jul;4(5):289-301 [PMID: 16011575]
  75. Neuropsychopharmacology. 2009 May;34(6):1381-94 [PMID: 18615010]
  76. J Neurosci. 1994 Sep;14(9):5381-92 [PMID: 8083743]
  77. Physiol Behav. 2019 May 15;204:290-296 [PMID: 30853621]
  78. Neuroendocrinology. 2014;100(2-3):119-28 [PMID: 25116057]
  79. Psychoneuroendocrinology. 2017 Oct;84:124-134 [PMID: 28710956]
  80. Nat Commun. 2018 Feb 27;9(1):849 [PMID: 29487284]
  81. Neuroscience. 2014 Jul 25;273:12-23 [PMID: 24814726]
  82. Psychosom Med. 2018 Jan;80(1):62-68 [PMID: 28872575]
  83. Proc Natl Acad Sci U S A. 2019 Jan 22;116(4):1331-1336 [PMID: 30617061]
  84. Horm Behav. 2018 Jan;97:47-55 [PMID: 29111331]
  85. Brain Res. 1997 Sep 5;767(2):321-32 [PMID: 9367264]
  86. J Neurosci. 2003 Apr 15;23(8):3483-90 [PMID: 12716957]
  87. Neuroscience. 2009 Sep 15;162(4):892-903 [PMID: 19482070]
  88. J Neurosci. 2013 May 22;33(21):9140-9 [PMID: 23699524]
  89. J Neurosci. 2006 Nov 29;26(48):12387-96 [PMID: 17135400]
  90. Horm Behav. 1999 Aug;36(1):25-38 [PMID: 10433884]
  91. Elife. 2021 Jan 14;10: [PMID: 33443015]
  92. Horm Behav. 2015 May;71:83-90 [PMID: 25934057]
  93. Nature. 2013 Sep 12;501(7466):179-84 [PMID: 24025838]
  94. Sci Rep. 2021 Feb 12;11(1):3746 [PMID: 33580133]
  95. Psychoneuroendocrinology. 2019 Jan;99:128-136 [PMID: 30227351]
  96. Front Neurosci. 2021 Oct 15;15:748431 [PMID: 34720866]
  97. Elife. 2019 May 14;8: [PMID: 31084703]
  98. Horm Behav. 2013 Mar;63(3):518-26 [PMID: 23370363]
  99. PLoS One. 2014 Apr 14;9(4):e94771 [PMID: 24733061]
  100. Behav Brain Res. 2018 Apr 2;341:114-121 [PMID: 29288748]
  101. Horm Behav. 2006 Dec;50(5):699-707 [PMID: 16934808]
  102. PLoS One. 2010 Jan 27;5(1):e8931 [PMID: 20111713]
  103. Am J Primatol. 2017 Sep;79(9): [PMID: 28605039]
  104. Front Neurosci. 2021 Oct 01;15:720294 [PMID: 34658766]
  105. Psychoneuroendocrinology. 2019 Aug;106:259-267 [PMID: 31022585]
  106. FEBS Lett. 2007 Jun 12;581(14):2580-6 [PMID: 17507012]
  107. Horm Behav. 2016 Jan;77:98-112 [PMID: 26062432]
  108. Horm Behav. 2022 Apr;140:105126 [PMID: 35123106]
  109. Front Neuroendocrinol. 2016 Jul;42:18-39 [PMID: 27020799]
  110. Am J Physiol. 1997 Nov;273(5):R1683-9 [PMID: 9374810]
  111. Behaviour. 2012;149(3-4):407-440 [PMID: 30504964]
  112. Front Psychol. 2020 Jan 28;11:25 [PMID: 32047459]
  113. Psychoneuroendocrinology. 2016 Feb;64:66-78 [PMID: 26615473]
  114. Pharmacol Biochem Behav. 2017 Oct;161:38-46 [PMID: 28918226]
  115. Neuroscience. 2015 Feb 26;287:32-42 [PMID: 25485481]
  116. Behav Neurosci. 2001 Aug;115(4):910-9 [PMID: 11508730]
  117. Behav Neurosci. 1995 Aug;109(4):782-9 [PMID: 7576222]
  118. Horm Behav. 2012 Aug;62(3):314-23 [PMID: 22663934]
  119. Curr Opin Neurobiol. 2016 Oct;40:8-13 [PMID: 27290660]
  120. Nat Neurosci. 2017 Feb;20(2):260-270 [PMID: 28067904]
  121. J Comp Neurol. 2007 May 20;502(3):414-26 [PMID: 17366609]
  122. Elife. 2016 Jul 02;5: [PMID: 27371827]
  123. Psychoneuroendocrinology. 1998 Nov;23(8):765-78 [PMID: 9924737]
  124. Primates. 2016 Jan;57(1):103-12 [PMID: 26386712]
  125. Neuroscience. 2003;121(3):537-44 [PMID: 14568015]
  126. Eur J Neurosci. 2014 May;39(10):1632-41 [PMID: 24641515]
  127. Front Endocrinol (Lausanne). 2017 Jun 28;8:145 [PMID: 28701997]
  128. Horm Behav. 2004 Jun;46(1):30-8 [PMID: 15215039]
  129. Behav Brain Res. 2013 Aug 1;250:257-63 [PMID: 23707935]
  130. Trends Neurosci. 2017 Jul;40(7):385-396 [PMID: 28554687]
  131. J Neurosci. 2001 Oct 15;21(20):8278-85 [PMID: 11588199]
  132. Psychoneuroendocrinology. 2013 Dec;38(12):3128-38 [PMID: 24103891]
  133. Annu Rev Neurosci. 1992;15:353-75 [PMID: 1575447]
  134. J Neuroendocrinol. 2016 Apr;28(4): [PMID: 26940141]
  135. J Comp Neurol. 2011 Dec 15;519(18):3599-639 [PMID: 21800319]
  136. Horm Behav. 2018 Feb;98:88-95 [PMID: 29289657]
  137. Trends Neurosci. 2015 May;38(5):295-306 [PMID: 25847686]
  138. Proc Natl Acad Sci U S A. 2008 Jan 29;105(4):1249-54 [PMID: 18212120]
  139. Neuropsychopharmacology. 2011 Oct;36(11):2200-10 [PMID: 21734650]
  140. Neuron. 2008 Aug 28;59(4):648-61 [PMID: 18760700]
  141. Horm Behav. 2016 Nov;86:71-77 [PMID: 27712925]
  142. Auton Neurosci. 2014 Feb;180:9-16 [PMID: 24161576]
  143. J Neuroendocrinol. 1994 Jun;6(3):247-50 [PMID: 7920590]
  144. Neuropeptides. 2008 Oct-Dec;42(5-6):525-33 [PMID: 18675458]
  145. Proc Natl Acad Sci U S A. 2006 Jul 18;103(29):10956-60 [PMID: 16832060]
  146. J Neurosci. 2001 Sep 15;21(18):7392-6 [PMID: 11549749]
  147. Curr Top Behav Neurosci. 2017;30:411-429 [PMID: 26728172]
  148. Neurosci Lett. 2009 Sep 25;461(3):217-22 [PMID: 19539696]
  149. Behav Brain Res. 2011 Oct 31;224(2):279-89 [PMID: 21684307]
  150. J Neurosci. 2005 Dec 14;25(50):11777-86 [PMID: 16354936]
  151. Behav Neurosci. 2007 Dec;121(6):1353-63 [PMID: 18085888]
  152. Horm Behav. 2015 Jul;73:8-14 [PMID: 26012712]
  153. Horm Behav. 2001 Sep;40(2):133-8 [PMID: 11534973]
  154. Neuroscience. 2017 Apr 21;348:302-312 [PMID: 28242440]
  155. Nat Commun. 2018 Oct 19;9(1):4350 [PMID: 30341305]
  156. Horm Behav. 2018 Nov;106:150-161 [PMID: 30342885]
  157. Horm Behav. 2016 May;81:68-73 [PMID: 27074037]
  158. Neuroscience. 2017 Feb 20;343:284-297 [PMID: 27998780]
  159. Psychol Rep. 1993 Feb;72(1):316-8 [PMID: 8451367]
  160. Pharmacol Biochem Behav. 2002 Aug;73(1):259-69 [PMID: 12076744]
  161. Horm Behav. 2016 Mar;79:8-17 [PMID: 26643557]
  162. Horm Behav. 2020 Jul;123:104645 [PMID: 31778720]
  163. Yale J Biol Med. 2017 Sep 25;90(3):373-387 [PMID: 28955178]
  164. Neurobiol Stress. 2020 Nov 24;13:100278 [PMID: 33344730]
  165. Horm Behav. 2004 May;45(5):354-61 [PMID: 15109910]
  166. Adv Exp Med Biol. 1998;449:215-24 [PMID: 10026808]
  167. Front Behav Neurosci. 2016 Nov 14;10:221 [PMID: 27895565]
  168. Am J Psychiatry. 1997 Jun;154(6):726-35 [PMID: 9167498]
  169. Addict Biol. 2021 Jan;26(1):e12851 [PMID: 31691406]
  170. Neuroscience. 2015 Apr 2;290:421-34 [PMID: 25637809]
  171. Cell. 2017 Nov 16;171(5):1176-1190.e17 [PMID: 29107332]
  172. Brain Struct Funct. 2020 Jan;225(1):285-304 [PMID: 31820102]
  173. Neuropsychopharmacology. 2009 May;34(6):1406-15 [PMID: 18923404]
  174. Brain Res. 2003 Mar 7;965(1-2):203-11 [PMID: 12591139]
  175. Learn Mem. 2020 Jul 15;27(8):310-318 [PMID: 32669386]
  176. Biol Psychiatry. 2016 Jul 15;80(2):160-169 [PMID: 26893121]
  177. Horm Behav. 2012 May;61(5):669-77 [PMID: 22421629]
  178. Neuroscience. 1997 Mar;77(1):175-86 [PMID: 9044385]
  179. Nature. 1993 Oct 7;365(6446):545-8 [PMID: 8413608]
  180. Am J Primatol. 2018 Oct;80(10):e22756 [PMID: 29923206]
  181. Behav Brain Res. 2009 Jan 23;196(2):155-67 [PMID: 18955088]
  182. Front Behav Neurosci. 2009 Aug 11;3:15 [PMID: 19707518]
  183. J Neurosci. 2009 Feb 4;29(5):1312-8 [PMID: 19193878]
  184. Behav Brain Res. 2019 Jun 3;365:36-47 [PMID: 30802533]
  185. Sci Rep. 2020 Oct 14;10(1):17301 [PMID: 33057124]
  186. Brain Behav Evol. 2022;97(3-4):225-240 [PMID: 35051922]
  187. Neurosci Lett. 2006 Feb 13;394(2):146-51 [PMID: 16289323]
  188. Neurosci Biobehav Rev. 2009 Mar;33(3):383-93 [PMID: 19046987]
  189. Behav Brain Res. 1996 Feb;75(1-2):179-93 [PMID: 8800655]
  190. Adv Exp Med Biol. 1995;395:227-34 [PMID: 8713971]
  191. Cereb Cortex. 2010 Dec;20(12):2884-99 [PMID: 20308201]
  192. Psychoneuroendocrinology. 2016 Jun;68:156-62 [PMID: 26974500]
  193. Behav Processes. 2021 Nov;192:104497 [PMID: 34499983]
  194. Nature. 2017 Oct 18;550(7676):388-392 [PMID: 29052632]
  195. Dev Psychobiol. 2020 Jul;62(5):573-590 [PMID: 31823359]
  196. Proc Biol Sci. 2021 Aug 11;288(1956):20210318 [PMID: 34344176]
  197. Horm Behav. 2019 Nov;116:104578 [PMID: 31449813]
  198. Biol Psychiatry Cogn Neurosci Neuroimaging. 2022 Jun;7(6):588-597 [PMID: 33239258]
  199. Am J Primatol. 2012 Aug;74(8):758-69 [PMID: 22549396]
  200. Horm Behav. 2014 Jan;65(1):57-65 [PMID: 24291055]
  201. Proc Natl Acad Sci U S A. 2016 Nov 15;113(46):13233-13238 [PMID: 27807133]
  202. Behav Brain Res. 2010 Jan 5;206(1):120-6 [PMID: 19737580]
  203. J Neuroendocrinol. 2015 Apr;27(4):245-52 [PMID: 25659593]
  204. Neuroscience. 2006 Aug 25;141(2):559-568 [PMID: 16725274]
  205. Elife. 2020 May 26;9: [PMID: 32452763]
  206. Neuroscience. 2009 Sep 29;163(1):9-22 [PMID: 19524021]
  207. Am J Primatol. 2018 Oct;80(10):e22750 [PMID: 29527695]
  208. Neurosci Lett. 2009 Apr 17;454(1):67-71 [PMID: 19429056]
  209. J Comp Neurol. 2022 Nov;530(16):2881-2900 [PMID: 35763609]
  210. Genes Brain Behav. 2011 Apr;10(3):375-83 [PMID: 21255269]
  211. Neuron. 2005 Aug 18;47(4):503-13 [PMID: 16102534]
  212. Horm Behav. 2011 Nov;60(5):498-504 [PMID: 21851821]
  213. Am J Primatol. 2017 Mar;79(3):1-9 [PMID: 27757971]
  214. Horm Behav. 2010 Aug;58(3):385-9 [PMID: 20362577]
  215. Front Behav Neurosci. 2009 Aug 27;3:17 [PMID: 19753327]
  216. Horm Behav. 1992 Sep;26(3):339-49 [PMID: 1398553]
  217. Proc Biol Sci. 2000 Jan 22;267(1439):147-50 [PMID: 10687819]
  218. Horm Behav. 2016 Apr;80:10-18 [PMID: 26836769]

MeSH Term

Animals
Humans
Mammals
Pair Bond
Primates
Sexual Behavior, Animal
Social Behavior

Word Cloud

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