Oxytocin and Vasopressin in Emotional Memory and “Face Reading”: a Neurobiological Approach and Clinical Aspects

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Abstract

The ability to adequately perceive and recognize emotions is a key and universal tool in interpersonal communication, which allows people to understand feelings, intentions, and emotional reactions of themselves and others. Throughout their life, people have to make inferences about mental state of others by interpreting subtle social signals, such as facial expressions, to understand or predict others’ behavior, which is crucial in constructive social interactions. Therefore, emotional memory associated with the ability to identify emotions based on one’s life experience is the cornerstone of social cognition and interpersonal relationships. Oxytocin and vasopressin are neurohypophysial peptides that have attracted scientific attention due to their role in the emotional and social aspects of behavior. Variable and contrasting effects of oxytocin and vasopressin may be related to the sites of the brain where they exert their activity.

Aim. This review aimed to evaluate neural mechanisms underlying oxytocin-mediated and vasopressin-mediated modulation of emotional memory; to assess how cerebral oxytocin-signal and vasopressin-signal transduction mediates emotional and social behavior; to discuss the role of the two neuropeptides in non-verbal interpersonal communication; and to present their cerebral effects in relation to an ability for “face reading” in patients with mental disorders.

About the authors

Yana V. Gorina

Professor V.F. Voino-Yasenetsky Krasnoyarsk State Medical University; Siberian Federal University

Author for correspondence.
Email: yana_20@bk.ru
ORCID iD: 0000-0002-3341-1557

Cand. Sci. (Pharm.), Associate Professor, senior researcher, Laboratory of social neurosciences, Associate Professor, Department of biological chemistry with courses medical, pharmaceutical and toxicological chemistry, Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University; Associate Professor, Department of biophysics, Siberian Federal University

Russian Federation, Krasnoyarsk; Krasnoyarsk

Olga L. Lopatina

Professor V.F. Voino-Yasenetsky Krasnoyarsk State Medical University; Siberian Federal University

Email: ol.lopatina@gmail.com
ORCID iD: 0000-0002-7884-2721

Dr. Sci. (Biol.), Associate Professor, Head, Laboratory of social neurosciences, Professor, Department of biological chemistry with courses medical, pharmaceutical and toxicological chemistry, Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University; Professor, Department of biophysics, Siberian Federal University

Russian Federation, Krasnoyarsk; Krasnoyarsk

Larisa V. Mararitsa

National Research University "Higher School of Economics"

Email: mararitsalarisa@gmail.com
ORCID iD: 0000-0003-3858-5369

Cand. Sci. PhD (Psychol.), senior researcher, Laboratory of social and cognitive informatics, St. Petersburg School of social sciences and area studies

Russian Federation, St. Petersburg

References

  1. Ghodousi M., Pousson J.E., Bernhofs V., Griškova-Bulanova I. Assessment of different feature extraction methods for discriminating expressed emotions during music performance towards BCMI application. Sensors. (Basel.). 2023;23(4):2252. doi: 10.3390/s23042252
  2. Dolcos F., Denkova E. Current emotion research in cognitive neuroscience: linking enhancing and impairing effects of emotion on cognition. Emot. Rev. 2014;6(4):362–375. doi: 10.1177/1754073914536449
  3. Harrison N.A., Gray M.A., Gianaros P.J., Critchley H.D. The embodiment of emotional feelings in the brain. J. Neurosci. 2010;30(38):12878–12884. doi: 10.1523/JNEUROSCI.1725-10.2010
  4. Ekman P. Are there basic emotions? Psychol. Rev. 1992;99(3):550–553. doi: 10.1037/0033-295X.99.3.550
  5. Le J., Kou J., Zhao W. et al. Oxytocin facilitation of emotional empathy is associated with increased eye gaze toward the faces of individuals in emotional contexts. Front. Neurosci. 2020;14:803. doi: 10.3389/fnins.2020.00803
  6. Motoki K., Sugiura M., Takeuchi H. et al. Are plasma oxytocin and vasopressin levels reflective of amygdala activation during the processing of negative emotions? A preliminary study. Front. Psychol. 2016;7:480. doi: 10.3389/fpsyg.2016.00480
  7. Carcea I., Caraballo N.L., Marlin B.J. et al. Oxytocin neurons enable social transmission of maternal behavior. Nature. 2021;596(7873):553–557. doi: 10.1038/s41586-021-03814-7
  8. Bosch O.J., Neumann I.D. Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm. Behav. 2012;61(3):293–303. doi: 10.1016/j.yhbeh.2011.11.002
  9. Wang Z., Aragona B.J. Neurochemical regulation of pair bonding in male prairie voles. Physiol. Behav. 2004;83(2):319–328. doi: 10.1016/j.physbeh.2004.08.024
  10. Behnia B., Heinrichs M., Bergmann W. et al. Differential effects of intranasal oxytocin on sexual experiences and partner interactions in couples. Horm. Behav. 2014;65(3):308–318. doi: 10.1016/j.yhbeh.2014.01.009
  11. Bertoni A., Schaller F., Tyzio R. et al. Oxytocin administration in neonates shapes hippocampal circuitry and restores social behavior in a mouse model of autism. Mol. Psychiatry. 2021;26(12):7582–7595. doi: 10.1038/s41380-021-01227-6
  12. Baumgartner T., Heinrichs M., Vonlanthen A. et al. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron. 2008;58(4):639–650. doi: 10.1016/j.neuron.2008.04.009
  13. Li X.H., Matsuura T., Xue M. et al. Oxytocin in the anterior cingulate cortex attenuates neuropathic pain and emotional anxiety by inhibiting presynaptic long-term potentiation. Cell Rep. 2021;36(3):109411. doi: 10.1016/j.celrep.2021.109411
  14. La Fratta I., Franceschelli S., Speranza L. et al. Salivary oxytocin, cognitive anxiety and self-confidence in pre-competition athletes. Sci. Rep. 2021;11(1):16877. doi: 10.1038/s41598-021-96392-7
  15. Taylor J.H., Walton J.C., McCann K.E. et al. CRISPR-Cas9 editing of the arginine-vasopressin V1a receptor produces paradoxical changes in social behavior in Syrian hamsters. Proc. Natl. Acad. Sci. U S A. 2022;119(19):e2121037119. doi: 10.1073/pnas.2121037119
  16. Freeman A.R., Hare J.F., Anderson W.G., Caldwell H.K. Effects of arginine vasopressin on Richardson's ground squirrel social and vocal behavior. Behav. Neurosci. 2018;132(1):34–50. doi: 10.1037/bne0000225
  17. Domes G., Normann C., Heinrichs M. The effect of oxytocin on attention to angry and happy faces in chronic depression. BMC Psychiatry. 2016;16:92. doi: 10.1186/s12888-016-0794-9
  18. Shamay-Tsoory S.G., Fischer M., Dvash J. et al. Intranasal administration of oxytocin increases envy and schadenfreude (gloating). Biol. Psychiatry. 2009;66(9):864–870. doi: 10.1016/j.biopsych.2009.06.009
  19. Hasan M.T., Althammer F., Silva da Gouveia M. A fear memory engram and its plasticity in the hypothalamic oxytocin system. Neuron. 2019;103(1):133–146.e8. doi: 10.1016/j.neuron.2019.04.029
  20. Campbell-Smith E.J., Holmes N.M., Lingawi N.W. et al. Oxytocin signaling in basolateral and central amygdala nuclei differentially regulates the acquisition, expression, and extinction of context-conditioned fear in rats. Learn Mem. 2015;22(5):247–257. doi: 10.1101/lm.036962.114
  21. Knobloch H.S., Charlet A., Hoffmann L.C. et al. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron. 2012;73(3):553–566. doi: 10.1016/j.neuron.2011.11.030
  22. Viviani D., Stoop R. Opposite effects of oxytocin and vasopressin on the emotional expression of the fear response. Prog. Brain Res. 2008;170:207–218. doi: 10.1016/S0079-6123(08)00418-4
  23. Steidl S., Razik F., Anderson A.K. Emotion enhanced retention of cognitive skill learning. Emotion. 2011;11(1):12–19. doi: 10.1037/a0020288
  24. Steidl S., Mohi-uddin S., Anderson A.K. Effects of emotional arousal on multiple memory systems: evidence from declarative and procedural learning. Learn Mem. 2006;13(5):650–658. doi: 10.1101/lm.324406
  25. Maliske L.Z., Schurz M., Kanske P. Interactions within the social brain: co-activation and connectivity among networks enabling empathy and theory of mind. Neurosci. Biobehav. Rev. 2023;147:105080. doi: 10.1016/j.neubiorev.2023.105080
  26. Matsunaga M., Kikusui T., Mogi K. et al. Breastfeeding dynamically changes endogenous oxytocin levels and emotion recognition in mothers. Biol. Lett. 2020;16(6):20200139. doi: 10.1098/rsbl.2020.0139
  27. Ferretti V., Maltese F., Contarini G. et al. Oxytocin signaling in the central amygdala modulates emotion discrimination in mice. Curr. Biol. 2019;29(12):1938–1953.e6. doi: 10.1016/j.cub.2019.04.070
  28. Lischke A., Berger C., Prehn K. et al. Intranasal oxytocin enhances emotion recognition from dynamic facial expressions and leaves eye-gaze unaffected. Psychoneuroendocrinology. 2012;37(4):475–481. doi: 10.1016/j.psyneuen.2011.07.015
  29. Uzefovsky F., Shalev I., Israel S. et al. Vasopressin selectively impairs emotion recognition in men. Psychoneuroendocrinology. 2012;37(4):576–580. doi: 10.1016/j.psyneuen.2011.07.018
  30. Knobloch H.S., Grinevich V. Evolution of oxytocin pathways in the brain of vertebrates. Front. Behav. Neurosci. 2014;8:31. doi: 10.3389/fnbeh.2014.00031
  31. Gimpl G., Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol Rev. 2001;81(2):629–683. doi: 10.1152/physrev.2001.81.2.629
  32. Guastella A.J., Mitchell P.B., Mathews F. Oxytocin enhances the encoding of positive social memories in humans. Biol. Psychiatry. 2008;64(3):256–258. doi: 10.1016/j.biopsych.2008.02.008
  33. Tse W.S., Siu A.F.Y., Zhang Q., Chan H.Y.E. Maternal oxytocin responsiveness improves specificity of positive social memory recall. Psychoneuroendocrinology. 2018;98:148–152. doi: 10.1016/j.psyneuen.2018.08.026
  34. Plasencia G., Luedicke J.M., Nazarloo H.P. et al. Plasma oxytocin and vasopressin levels in young and older men and women: functional relationships with attachment and cognition. Psychoneuroendocrinology. 2019;110:104419. doi: 10.1016/j.psyneuen.2019.104419
  35. Larrazolo-López A., Kendrick K.M., Aburto-Arciniega M. et al. Vaginocervical stimulation enhances social recognition memory in rats via oxytocin release in the olfactory bulb. Neuroscience. 2008;152(3):585–593. doi: 10.1016/j.neuroscience.2008.01.024
  36. Chini B., Leonzino M., Braida D., Sala M. Learning about oxytocin: pharmacologic and behavioral issues. Biol. Psychiatry. 2014;76(5):360–366. doi: 10.1016/j.biopsych.2013.08.029
  37. Heinrichs M., Meinlschmidt G., Wippich W. et al. Selective amnesic effects of oxytocin on human memory. Physiol. Behav. 2004;83(1):31–38. doi: 10.1016/j.physbeh.2004.07.020
  38. Brambilla M., Manenti R., de Girolamo G. et al. Effects of intranasal oxytocin on long-term memory in healthy humans: a systematic review. Drug Dev. Res. 2016;77(8):479–488. doi: 10.1002/ddr.21343
  39. Hu J., Qi S., Becker B. et al. Oxytocin selectively facilitates learning with social feedback and increases activity and functional connectivity in emotional memory and reward processing regions. Hum. Brain Mapp. 2015;36(6):2132–2146. doi: 10.1002/hbm.22760
  40. Takahashi J., Yamada D., Ueta Y. et al. Oxytocin reverses Aβ-induced impairment of hippocampal synaptic plasticity in mice. Biochem. Biophys. Res. Commun. 2020;528(1):174–178. doi: 10.1016/j.bbrc.2020.04.046
  41. Latt H.M., Matsushita H., Morino M. et al. Oxytocin inhibits corticosterone-induced apoptosis in primary hippocampal neurons. Neuroscience. 2018;379:383–389. doi: 10.1016/j.neuroscience.2018.03.025
  42. Leroy F., Park J., Asok A. et al. A circuit from hippocampal CA2 to lateral septum disinhibits social aggression. Nature. 2018;564(7735):213–218. doi: 10.1038/s41586-018-0772-0
  43. Finton C.J., Ophir A.G. Developmental exposure to intranasal vasopressin impacts adult prairie vole spatial memory. Psychoneuroendocrinology. 2022;141:105750. doi: 10.1016/j.psyneuen.2022.105750
  44. Lei S., Hu B., Rezagholizadeh N. Activation of V1a vasopressin receptors excite subicular pyramidal neurons by activating TRPV1 and depressing GIRK channels. Neuropharmacology. 2021;190:108565. doi: 10.1016/j.neuropharm.2021.108565
  45. Ramanathan G., Cilz N.I., Kurada L. et al. Vasopressin facilitates GABAergic transmission in rat hippocampus via activation of V(1A) receptors. Neuropharmacology. 2012;63(7):1218–1226. doi: 10.1016/j.neuropharm.2012.07.043
  46. Hsu D. The dentate gyrus as a filter or gate: a look back and a look ahead. Prog. Brain Res. 2007;163:601–613. doi: 10.1016/S0079-6123(07)63032-5
  47. Chen C., Díaz Brinton R.D., Shors T.J., Thompson R.F. Vasopressin induction of long-lasting potentiation of synaptic transmission in the dentate gyrus. Hippocampus. 1993;3(2):193–203. doi: 10.1002/hipo.450030211
  48. Dubrovsky B., Tatarinov A., Gijsbers K. et al. Effects of arginine-vasopressin (AVP) on long-term potentiation in intact anesthetized rats. Brain Res. Bull. 2003;59(6):467–472. doi: 10.1016/s0361-9230(02)00961-9
  49. Zhang X., Zhao F., Wang C. et al. AVP(4-8) improves cognitive behaviors and hippocampal synaptic plasticity in the APP/PS1 mouse model of Alzheimer's disease. Neurosci. Bull. 2020;36(3):254–262. doi: 10.1007/s12264-019-00434-0
  50. Török B., Varga J., Zelena D. Vasopressin as a possible link between sleep-disturbances and memory problems. Int. J. Mol. Sci. 2022;23(24):15467. doi: 10.3390/ijms232415467
  51. Guastella A.J., Kenyon A.R., Alvares G.A. et al. Intranasal arginine vasopressin enhances the encoding of happy and angry faces in humans. Biol. Psychiatry. 2010;67(12):1220–1222. doi: 10.1016/j.biopsych.2010.03.014
  52. Chatav Y., Whisman M.A. Partner schemas and relationship functioning: a states of mind analysis. Behav. Ther. 2009;40(1):50–56. doi: 10.1016/j.beth.2007.12.005
  53. Guastella A.J., Kenyon A.R., Unkelbach C. et al. Arginine vasopressin selectively enhances recognition of sexual cues in male humans. Psychoneuroendocrinology. 2011;36(2):294–297. doi: 10.1016/j.psyneuen.2010.07.023
  54. Duque-Wilckens N., Steinman M.Q., Laredo S.A. et al. Inhibition of vasopressin V1a receptors in the medioventral bed nucleus of the stria terminalis has sex- and context-specific anxiogenic effects. Neuropharmacology. 2016;110(Pt A):59–68. doi: 10.1016/j.neuropharm.2016.07.018
  55. Bielsky I.F., Hu S.B., Ren X. et al. The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron. 2005;47(4):503–513. doi: 10.1016/j.neuron.2005.06.031
  56. Bredewold R., Smith C.J.W., Dumais K.M., Veenema A.H. Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context. Front. Beha.v Neurosci. 2014;8:216. doi: 10.3389/fnbeh.2014.00216
  57. Gobrogge K.L., Liu Y., Young L.J., Wang Z. Anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent. Proc. Natl. Acad. Sci. USA. 2009;106(45):19144–19149. doi: 10.1073/pnas.0908620106
  58. Sun Y., Gooch H., Sah P. Fear conditioning and the basolateral amygdala. F1000Res. 2020;9:F1000 Faculty Rev-53. doi: 10.12688/f1000research.21201.1
  59. Song C., Ehlers V.L., Moyer J.R.Jr. Trace fear conditioning differentially modulates intrinsic excitability of medial prefrontal cortex-basolateral complex of amygdala projection neurons in infralimbic and prelimbic cortices. J. Neurosci. 2015;35(39):13511–13524. doi: 10.1523/JNEUROSCI.2329-15.2015
  60. Martinez R.C.R., de Oliveira A.R., Brandão M.L. Conditioned and unconditioned fear organized in the periaqueductal gray are differentially sensitive to injections of muscimol into amygdaloid nuclei. Neurobiol. Learn Mem. 2006;85(1):58–65. doi: 10.1016/j.nlm.2005.08.007
  61. Gu Y., Piper W.T., Branigan L.A. et al. A brainstem-central amygdala circuit underlies defensive responses to learned threats. Mol. Psychiatry. 2020;25(3):640–654. doi: 10.1038/s41380-019-0599-6
  62. Hubber D., Veinante P., Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science. 2005;308(5719):245–248. doi: 10.1126/science.1105636
  63. Rood B.D., Stott R.T., You S. et al. Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J. Comp. Neurol. 2013;521(10):2321–2358. doi: 10.1002/cne.23288
  64. Karakilic A., Kizildag S., Kandis S. et al. The effects of acute foot shock stress on empathy levels in rats. Behav. Brain Res. 2018;349:31–36. doi: 10.1016/j.bbr.2018.04.043
  65. Merali Z., Hayley S., Kent P. et al. Impact of repeated stressor exposure on the release of corticotropin-releasing hormone, arginine-vasopressin and bombesin-like peptides at the anterior pituitary. Behav. Brain Res. 2009;198(1):105–112. doi: 10.1016/j.bbr.2008.10.025
  66. Croiset G., Nijsen M.J., Kamphuis P.J. Role of corticotropin-releasing factor, vasopressin and the autonomic nervous system in learning and memory. Eur. J. Pharmacol. 2000;405(1-3):225–234. doi: 10.1016/s0014-2999(00)00556-2
  67. Tong W.H., Abdulai-Saiku S., Vyas A. Arginine vasopressin in the medial amygdala causes greater post-stress recruitment of hypothalamic vasopressin neurons. Mol. Brain. 2021;14(1):141. doi: 10.1186/s13041-021-00850-2
  68. Ehrlich I., Humeau Y., Grenier F. et al. Amygdala inhibitory circuits and the control of fear memory. Neuron. 2009;62(6):757–771. doi: 10.1016/j.neuron.2009.05.026
  69. Kida S. Interaction between reconsolidation and extinction of fear memory. Brain Res. Bull. 2023;195:141–144. doi: 10.1016/j.brainresbull.2023.02.009
  70. Zink C.F., Stein J.L., Kempf L. et al. Vasopressin modulates medial prefrontal cortex-amygdala circuitry during emotion processing in humans. J. Neurosci. 2010;30(20):7017–7022. doi: 10.1523/JNEUROSCI.4899-09.2010
  71. Zoicas I., Slattery D.A., Neumann I.D. Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum. Neuropsychopharmacology. 2014;39(13):3027–3035. doi: 10.1038/npp.2014.156
  72. Hodgson R.A., Mullins D., Lu S.X. et al. Characterization of a novel vasopressin V1b receptor antagonist, V1B-30N, in animal models of anxiety-like and depression-like behavior. Eur. J. Pharmacol. 2014;730:157–163. doi: 10.1016/j.ejphar.2014.02.027
  73. Brooks J.A., Freeman J.B. Neuroimaging of person perception: a social-visual interface. Neurosci. Lett. 2019;693:40–43. doi: 10.1016/j.neulet.2017.12.046
  74. Wang T., Tang Q., Wu X., Chen X. Attachment anxiety moderates the effect of oxytocin on negative emotion recognition: Evidence from eye-movement data. Pharmacol. Biochem. Behav. 2020;198:173015. doi: 10.1016/j.pbb.2020.173015
  75. Guastella A.J., Mitchell P.B., Dadds M.R. Oxytocin increases gaze to the eye region of human faces. Biol. Psychiatry. 2008;63(1):3–5. doi: 10.1016/j.biopsych.2007.06.026
  76. Leppanen J., Ng K.W., Tchanturia K., Treasure J. Meta-analysis of the effects of intranasal oxytocin on interpretation and expression of emotions. Neurosci. Biobehav. Rev. 2017;78:125–144. doi: 10.1016/j.neubiorev.2017.04.010
  77. Putnam P.T., Roman J.M., Zimmerman P.E., Gothard K.M. Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys. Psychoneuroendocrinology. 2016;72:47–53. doi: 10.1016/j.psyneuen.2016.05.016
  78. Parr L.A., Brooks J.M., Jonesteller T. et al. Effects of chronic oxytocin on attention to dynamic facial expressions in infant macaques. Psychoneuroendocrinology. 2016;74:149–157. doi: 10.1016/j.psyneuen.2016.08.028
  79. Grill-Spector K., Weiner K.S., Kay K., Gomez J. The functional neuroanatomy of human face perception. Annu. Rev. Vis. Sci. 2017;3:167–196. doi: 10.1146/annurev-vision-102016-061214
  80. Freiwald W., Duchaine B., Yovel G. Face processing systems: from neurons to real-world social perception. Annu. Rev. Neurosci. 2016;39:325–346. doi: 10.1146/annurev-neuro-070815-013934
  81. Savaskan E., Ehrhardt R., Schulz A. et al. Post-learning intranasal oxytocin modulates human memory for facial identity. Psychoneuroendocrinology. 2008;33(3):368–374. doi: 10.1016/j.psyneuen.2007.12.004
  82. Schulze L., Lischke A., Greif J. et al. Oxytocin increases recognition of masked emotional faces. Psychoneuroendocrinology. 2011;36(9):1378–1382. doi: 10.1016/j.psyneuen.2011.03.011
  83. Evans S., Shergill S.S., Averbeck B.B. Oxytocin decreases aversion to angry faces in an associative learning task. Neuropsychopharmacology. 2010;35(13):2502–2509. doi: 10.1038/npp.2010.110
  84. Andrews T.J., Ewbank M.P. Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. Neuroimage. 2004;23(3):905–913. doi: 10.1016/j.neuroimage.2004.07.060
  85. Pourtois G., Schwartz S., Spiridon M. et al. Object representations for multiple visual categories overlap in lateral occipital and medial fusiform cortex. Cereb. Cortex. 2009;19(8):1806–1819. doi: 10.1093/cercor/bhn210
  86. Vuilleumier P., Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia. 2007;45(1):174–194. doi: 10.1016/j.neuropsychologia.2006.06.003
  87. Parr L.A., Mitchell T., Hecht E. Intranasal oxytocin in rhesus monkeys alters brain networks that detect social salience and reward. Am. J. Primatol. 2018;80(10):e22915. doi: 10.1002/ajp.22915
  88. Liu P., Lin T., Feifel D., Ebner N.C. Intranasal oxytocin modulates the salience network in aging. Neuroimage. 2022;253:119045. doi: 10.1016/j.neuroimage.2022.119045
  89. Domes G., Steiner A., Porges S.W., Heinrichs M. Oxytocin differentially modulates eye gaze to naturalistic social signals of happiness and anger. Psychoneuroendocrinology. 2013;38(7):1198–1202. doi: 10.1016/j.psyneuen.2012.10.002
  90. Domes G., Heinrichs M., Michel A. et al. Oxytocin improves "mind-reading" in humans. Biol. Psychiatry. 2007;61(6):731–733. doi: 10.1016/j.biopsych.2006.07.015
  91. Adolphs R., Spezio M. Role of the amygdala in processing visual social stimuli. Prog. Brain Res. 2006;156:363–378. doi: 10.1016/S0079-6123(06)56020-0
  92. Todorov A. The role of the amygdala in face perception and evaluation. Motiv. Emot. 2012;36(1):16–26. doi: 10.1007/s11031-011-9238-5
  93. Said C.P., Dotsch R., Todorov A. The amygdala and FFA track both social and non-social face dimensions. Neuropsychologia. 2010;48(12):3596–3605. doi: 10.1016/j.neuropsychologia.2010.08.009
  94. Mende-Siedlecki P., Said C.P., Todorov A. The social evaluation of faces: a meta-analysis of functional neuroimaging studies. Soc. Cogn. Affect. Neurosci. 2013;8(3):285–299. doi: 10.1093/scan/nsr090
  95. Gamer M., Zurowski B., Büchel C. Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc. Natl. Acad. Sci. USA. 2010;107(20):9400–9405. doi: 10.1073/pnas.1000985107
  96. Taubert J., Flessert M., Liu N., Ungerleider L.G. Intranasal oxytocin selectively modulates the behavior of rhesus monkeys in an expression matching task. Sci. Rep. 2019;9(1):15187. doi: 10.1038/s41598-019-51422-3
  97. Herzmann G., Bird C.W., Freeman M., Curran T. Effects of oxytocin on behavioral and ERP measures of recognition memory for own-race and other-race faces in women and men. Psychoneuroendocrinology. 2013;38(10):2140–2151. doi: 10.1016/j.psyneuen.2013.04.002
  98. Hubble K., Daughters K., Manstead A.S.R. et al. Oxytocin reduces face processing time but leaves recognition accuracy and eye-gaze unaffected. J. Int. Neuropsychol. Soc. 2017;23(1):23–33. doi: 10.1017/S1355617716000886
  99. Sosnowski M.J., Kano F., Brosnan S.F. Oxytocin and social gaze during a dominance categorization task in tufted capuchin monkeys Front. Psychol. 2022;13: 977771. doi: 10.3389/fpsyg.2022.977771.
  100. Bartz J.A., Zaki J., Bolger N., Ochsner K.N. Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 2011;15(7):301–309. doi: 10.1016/j.tics.2011.05.002
  101. Egito J.H., Nevat M., Shamay-Tsoory S.G., Osório A.A.C. Oxytocin increases the social salience of the outgroup in potential threat contexts. Horm. Behav. 2020;122:104733. doi: 10.1016/j.yhbeh.2020.104733
  102. Chang Y.C., Hsing Y.C. Emotion-infused deep neural network for emotionally resonant conversation. Applied Soft Computing. 2021;113:107861. doi: 10.1016/j.asoc.2021.107861
  103. Fallon N., Roberts C., Stancak A. Shared and distinct functional networks for empathy and pain processing: a systematic review and meta-analysis of fMRI studies. Soc. Cogn. Affect Neurosci. 2020;15(7):709–723. doi: 10.1093/scan/nsaa090
  104. Thompson R.R., George K., Walton J.C. et al. Sex-specific influences of vasopressin on human social communication. Proc. Natl. Acad. Sci. USA. 2006;103(20):7889–7894. doi: 10.1073/pnas.0600406103
  105. Polk R., Horta M., Lin T. et al. Evaluating the neuropeptide-social cognition link in ageing: the mediating role of basic cognitive skills. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2022;377(1858):20210048. doi: 10.1098/rstb.2021.0048
  106. Brunnlieb C., Nave G., Camerer C.F. et al. Vasopressin increases human risky cooperative behavior. Proc. Natl. Acad. Sci. USA. 2016;113(8):2051–2056. doi: 10.1073/pnas.1518825113
  107. Feng C., Hackett P.D., DeMarco A.C. et al. Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans. Brain Imaging Behav. 2015;9(4):754–764. doi: 10.1007/s11682-014-9333-9
  108. Yamamoto D.J., Woo C.W., Wager T.D. et al. Influence of dorsolateral prefrontal cortex and ventral striatum on risk avoidance in addiction: a mediation analysis. Drug Alcohol Depend. 2015;149:10–17. doi: 10.1016/j.drugalcdep.2014.12.026
  109. Lim M.M., Young L.J. Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience. 2004;125(1):35–45. doi: 10.1016/j.neuroscience.2003.12.008
  110. Nair H.P., Young L.J. Vasopressin and pair-bond formation: genes to brain to behavior. Physiology (Bethesda). 2006;21:146–152. doi: 10.1152/physiol.00049.2005
  111. Wu X., Feng C., He Z. et al. Gender-specific effects of vasopressin on human social communication: аn ERP study. Horm. Behav. 2019;113:85–94. doi: 10.1016/j.yhbeh.2019.04.014
  112. Vehlen A., Kellner A., Normann C. et al. Reduced eye gaze during facial emotion recognition in chronic depression: effects of intranasal oxytocin. J. Psychiatr Res. 2023;159:50–56. doi: 10.1016/j.jpsychires.2023.01.016
  113. Spilka M.J., Keller W.R., Buchanan R.W. et al. Endogenous oxytocin levels are associated with facial emotion recognition accuracy but not gaze behavior in individuals with schizophrenia. Acta Psychiatr. Scand. 2022;145(5):494–506. doi: 10.1111/acps.13421
  114. Averbeck B.B., Bobin T., Evans S., Shergill S.S. Emotion recognition and oxytocin in patients with schizophrenia. Psychol. Med. 2012;42(2):259–266. doi: 10.1017/S0033291711001413
  115. Andari E., Massa N.M., Fargotstein M.D. et al. Effects of oxytocin on emotion recognition in schizophrenia: a randomized double-blind pilot study. J. Clin. Psychopharmacol. 2021;41(2):103–113. doi: 10.1097/JCP.0000000000001367
  116. Wynn J.K., Green M.F., Hellemann G. et al. A dose-finding study of oxytocin using neurophysiological measures of social processing. Neuropsychopharmacology. 2019;44(2):289–294. doi: 10.1038/s41386-018-0165-y
  117. Brambilla M., Cotelli M., Manenti R. et al. Oxytocin to modulate emotional processing in schizophrenia: a randomized, double-blind, cross-over clinical trial. Eur. Neuropsychopharmacol. 2016;26(10):1619–1628. doi: 10.1016/j.euroneuro.2016.08.001
  118. Wigton R., Tracy D.K., Verneuil T.M. et al. The importance of pro-social processing, and ameliorating dysfunction in schizophrenia. An FMRI study of oxytocin. Schizophr. Res. Cogn. 2021;27:100221. doi: 10.1016/j.scog.2021.100221
  119. Horta de Macedo L.R., Zuardi A.W., Machado-de-Sousa J.P. et al. Oxytocin does not improve performance of patients with schizophrenia and healthy volunteers in a facial emotion matching task. Psychiatry Res. 2014;220(1-2):125–128. doi: 10.1016/j.psychres.2014.07.082
  120. Schmidt A., Davies C., Paloyelis Y. et al. Acute oxytocin effects in inferring others' beliefs and social emotions in people at clinical high risk for psychosis. Transl. Psychiatry. 2020;10(1):203. doi: 10.1038/s41398-020-00885-4
  121. Bekkali S., Youssef G.J., Donaldson P.H. et al. Is the putative mirror neuron system associated with empathy? A systematic review and meta-analysis. Neuropsychol. Rev. 2021;31(1):14–57. doi: 10.1007/s11065-020-09452-6
  122. van der Burght C.L., Numssen O., Schlaak B. et al. Differential contributions of inferior frontal gyrus subregions to sentence processing guided by intonation. Hum Brain Mapp. 2023;44(2):585–598. doi: 10.1002/hbm.26086. PMID: 36189774.
  123. Iarrobino I., Bongiardina A., Dal Monte O. et al. Right and left inferior frontal opercula are involved in discriminating angry and sad facial expressions. Brain Stimul. 2021;14(3):607–615. doi: 10.1016/j.brs.2021.03.014
  124. Bloch B., Levin R., Vadas L. et al. Sex-specific effect of intranasal vasopressin, but not oxytocin, on emotional recognition and perception in schizophrenia patients. Isr. J. Psychiatry. 2019;56(1):21–25.
  125. Rubin L.H., Carter C.S., Bishop J.R. et al. Reduced levels of vasopressin and reduced behavioral modulation of oxytocin in psychotic disorders. Schizophr. Bull. 2014; 40(6):1374–1384. doi: 10.1093/schbul/sbu027
  126. Rubin L.H., Li S., Yao L. et al. Peripheral oxytocin and vasopressin modulates regional brain activity differently in men and women with schizophrenia. Schizophr. Res. 2018; 202:173–179. doi: 10.1016/j.schres.2018.07.003
  127. Carson D.S., Garner J.P., Hyde S.A. et al. Arginine vasopressin is a blood-based biomarker of social functioning in children with autism. PLoS One. 2015;10(7):e0132224. doi: 10.1371/journal.pone.0132224
  128. Shou X.J., Xu X.J., Zeng X.Z. et al. A volumetric and functional connectivity MRI study of brain arginine-vasopressin pathways in autistic children. Neurosci. Bull. 2017;33(2):130–142. doi: 10.1007/s12264-017-0109-2

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2. Fig. 1. Oxytocin-mediated modulation of emotional memory.

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3. Fig. 2. Vasopressinergic memory modulation.

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4. Fig. 3. Oxytocinergic regulation of social interaction.

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