Skip to main content
SpringerLink
Log in

Oxytocin and Social Isolation: Nonapeptide Regulation of Social Homeostasis

  • Chapter
  • First Online:
Neuroendocrinology of Behavior and Emotions

Part of the book series: Masterclass in Neuroendocrinology ((MANEURO,volume 16))

  • 179 Accesses

Abstract

Social isolation imposes physiological and behavioural effects that can have a severe impact on health, but the underlying mechanisms remain poorly understood. We reason that mechanisms responsible for the motivation to interact with others and the cognitive assessment of social interactions also mediate the effects of the lack of social interactions. This is because social isolation stress depends on the ability to maintain homeostasis against objective changes from sensory deprivation under physical isolation and subjective changes from perceived unmet social needs. Here, we review evidence for the conserved role played by the oxytocin neurosignalling system via its modulation of social decision-making and stress management. We discuss how oxytocin underlies the influence of both objective and subjective changes in social conditions, by featuring prominently in the control of motivational and cognitive functions in conserved brain regions, and eliciting ultimate health outcomes through interactions with other neuroendocrine systems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akinrinade I, Kareklas K, Teles MC, Reis TK, Gliksberg M, Petri G, Oliveira RF et al (2023) Evolutionarily conserved role of oxytocin in social fear contagion in zebrafish. Science 379(6638):1232–1237

    Article  CAS  PubMed  Google Scholar 

  • Anneser L, Alcantara IC, Gemmer A, Mirkes K, Ryu S, Schuman EM (2020) The neuropeptide Pth2 dynamically senses others via mechanosensation. Nature 588(7839):653–657

    Article  CAS  PubMed  Google Scholar 

  • Armitage KB (1987) Social dynamics of mammals: reproductive success, kinship and individual fitness. Trends Ecol Evol 2(9):279–284

    Article  CAS  PubMed  Google Scholar 

  • Baker M, Lindell SG, Driscoll CA, Zhou Z, Yuan Q, Schwandt ML, Barr CS et al (2017) Early rearing history influences oxytocin receptor epigenetic regulation in rhesus macaques. Proc Natl Acad Sci 114(44):11769–11774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balthazart J, Ball GF (2006) Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29(5):241–249

    Article  CAS  PubMed  Google Scholar 

  • Bartz JA, Zaki J, Bolger N, Ochsner KN (2011) Social effects of oxytocin in humans: context and person matter. Trends Cogn Sci 15(7):301–309

    CAS  PubMed  Google Scholar 

  • Beadle JN, Keady B, Brown V, Tranel D, Paradiso S (2012) Trait empathy as a predictor of individual differences in perceived loneliness. Psychol Rep 110(1):3–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Beets I, Janssen T, Meelkop E, Temmerman L, Suetens N, Rademakers S, Schoofs L et al (2012) Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. Elegans. Science 338(6106):543–545

    Article  CAS  PubMed  Google Scholar 

  • Beets I, Temmerman L, Janssen T, Schoofs L (2013) Ancient neuromodulation by vasopressin/oxytocin-related peptides. In: Worm, vol 2, No. 2. Taylor & Francis, p e24246

    Google Scholar 

  • Begni V, Sanson A, Pfeiffer N, Brandwein C, Inta D, Talbot SR, Mallien AS et al (2020) Social isolation in rats: effects on animal welfare and molecular markers for neuroplasticity. PLoS One 15(10):e0240439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatti AB, ul Haq A (2017) The pathophysiology of perceived social isolation: effects on health and mortality. Cureus 9(1)

    Google Scholar 

  • Bland AR, Roiser JP, Mehta MA, Sahakian BJ, Robbins TW, Elliott R (2022) The impact of COVID-19 social isolation on aspects of emotional and social cognition. Cognit Emot 36(1):49–58

    Article  Google Scholar 

  • Boinski S, Garber PA (eds) (2000) On the move: how and why animals travel in groups. University of Chicago Press

    Google Scholar 

  • Bosch OJ, Krömer SA, Brunton PJ, Neumann ID (2004) Release of oxytocin in the hypothalamic paraventricular nucleus, but not central amygdala or lateral septum in lactating residents and virgin intruders during maternal defence. Neuroscience 124(2):439–448

    Article  CAS  PubMed  Google Scholar 

  • Burkett JP, Young LJ (2012) The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction. Psychopharmacology 224(1):1–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkett JP, Andari E, Johnson ZV, Curry DC, de Waal FB, Young LJ (2016) Oxytocin-dependent consolation behavior in rodents. Science 351(6271):375–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cacioppo JT, Cacioppo S (2018) Loneliness in the modern age: an evolutionary theory of loneliness (ETL). In: Advances in experimental social psychology, vol 58. Academic Press, pp 127–197

    Google Scholar 

  • Cacioppo JT, Cacioppo S, Boomsma DI (2014) Evolutionary mechanisms for loneliness. Cognit Emot 28(1):3–21

    Article  Google Scholar 

  • Cacioppo JT, Cacioppo S, Capitanio JP, Cole SW (2015) The neuroendocrinology of social isolation. Annu Rev Psychol 66:733

    Article  PubMed  Google Scholar 

  • Cacioppo JT, Hawkley LC, Berntson GG (2003) The anatomy of loneliness. Curr Dir Psychol Sci 12(3):71–74

    Article  Google Scholar 

  • Caligioni CS, Oliver C, Jamur MC, Franci CR (2007) Presence of oxytocin receptors in the gonadotrophin-releasing hormone (GnRH) Neurones in female rats: A possible direct action of oxytocin on GnRH Neurones. J Neuroendocrinol 19(6):439–448

    Article  CAS  PubMed  Google Scholar 

  • Cantor M, Whitehead H (2013) The interplay between social networks and culture: theoretically and among whales and dolphins. Philos Trans R Soc Lond B Biol Sci 368(1618):20120340

    Article  PubMed  PubMed Central  Google Scholar 

  • Capitanio JP, Cacioppo S, Cole SW (2019) Loneliness in monkeys: neuroimmune mechanisms. Curr Opin Behav Sci 28:51–57

    Article  PubMed  PubMed Central  Google Scholar 

  • Carr L, Iacoboni M, Dubeau MC, Mazziotta JC, Lenzi GL (2003) Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci 100(9):5497–5502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrera-González MP, Ramírez-Expósito MJ, de Saavedra JMA, Sánchez-Agesta R, Mayas MD, Martínez-Martos JM (2011) Hypothalamus–pituitary–thyroid axis disruption in rats with breast cancer is related to an altered endogenous oxytocin/insulin-regulated aminopeptidase (IRAP) system. Tumor Biol 32(3):543–549

    Article  Google Scholar 

  • Carter DA, Lightman SL (1987) Oxytocin responses to stress in lactating and hyperprolactinaemic rats. Neuroendocrinology 46(6):532–537

    Article  CAS  PubMed  Google Scholar 

  • Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29(3):386–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Champagne FA, Meaney MJ (2007) Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121(6):1353

    Article  PubMed  Google Scholar 

  • Choe HK, Reed MD, Benavidez N, Montgomery D, Soares N, Yim YS, Choi GB (2015) Oxytocin mediates entrainment of sensory stimuli to social cues of opposing valence. Neuron 87(1):152–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dabrowska J, Hazra R, Ahern TH, Guo JD, McDonald AJ, Mascagni F, Rainnie DG et al (2011) Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin systems in the hypothalamus and the bed nucleus of the stria terminalis of the rat: implications for balancing stress and affect. Psychoneuroendocrinology 36(9):1312–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis JM, Mccourt WF, Courtney J, Solomon P (1961) Sensory deprivation: the role of social isolation. Arch Gen Psychiatry 5(1):84–90

    Article  CAS  PubMed  Google Scholar 

  • De Boer A, van Buel EM, Ter Horst GJ (2012) Love is more than just a kiss: a neurobiological perspective on love and affection. Neuroscience 201:114–124

    Article  PubMed  Google Scholar 

  • de Moura Oliveira VE, Neumann ID, de Jong TR (2019) Post-weaning social isolation exacerbates aggression in both sexes and affects the vasopressin and oxytocin system in a sex-specific manner. Neuropharmacology 156:107504

    Article  Google Scholar 

  • de Waal F, Preston SD (2017) Mammalian empathy: behavioural manifestations and neural basis. Nat Rev Neurosci 18(8):498–509

    Article  PubMed  Google Scholar 

  • Detillion CE, Craft TK, Glasper ER, Prendergast BJ, DeVries AC (2004) Social facilitation of wound healing. Psychoneuroendocrinology 29(8):1004–1011

    Article  CAS  PubMed  Google Scholar 

  • Dluzen DE, Muraoka S, Engelmann M, Ebner K, Landgraf R (2000) Oxytocin induces preservation of social recognition in male rats by activating α-adrenoceptors of the olfactory bulb. Eur J Neurosci 12(2):760–766

    Article  CAS  PubMed  Google Scholar 

  • Dölen G, Darvishzadeh A, Huang KW, Malenka RC (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501(7466):179–184

    Article  PubMed  PubMed Central  Google Scholar 

  • Duque-Wilckens N, Steinman MQ, Busnelli M, Chini B, Yokoyama S, Pham M, Trainor BC et al (2018) Oxytocin receptors in the anteromedial bed nucleus of the stria terminalis promote stress-induced social avoidance in female California mice. Biol Psychiatry 83(3):203–213

    Article  CAS  PubMed  Google Scholar 

  • Ferretti V, Maltese F, Contarini G, Nigro M, Bonavia A, Huang H, Papaleo F et al (2019) Oxytocin signaling in the central amygdala modulates emotion discrimination in mice. Curr Biol 29(12):1938–1953

    Article  CAS  PubMed  Google Scholar 

  • Frayne J, Townsend D, Nicholson HD (1996) Effects of oxytocin on sperm transport in the pubertal rat. Reproduction 107(2):299–306

    Article  CAS  Google Scholar 

  • Frith CD (2008) Social cognition. Philos Trans R Soc Lond B Biol Sci 363(1499):2033–2039

    Article  PubMed  PubMed Central  Google Scholar 

  • Froemke RC, Young LJ (2021) Oxytocin, neural plasticity, and social behavior. Annu Rev Neurosci 44:359–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garrison JL, Macosko EZ, Bernstein S, Pokala N, Albrecht DR, Bargmann CI (2012) Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. Science 338(6106):540–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gartland LA, Firth JA, Laskowski KL, Jeanson R, Ioannou CC (2022) Sociability as a personality trait in animals: methods, causes and consequences. Biol Rev 97(2):802–816

    Article  PubMed  Google Scholar 

  • Gilles YD, Polston EK (2017) Effects of social deprivation on social and depressive-like behaviors and the numbers of oxytocin expressing neurons in rats. Behav Brain Res 328:28–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81(2):629–683

    Article  CAS  PubMed  Google Scholar 

  • Gołyszny M, Obuchowicz E, Zieliński M (2021) Neuropeptides as regulators of the hypothalamus-pituitary-gonadal (HPG) axis activity and their putative roles in stress-induced fertility disorders. Neuropeptides 102216

    Google Scholar 

  • Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48(1):11–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Gordon I, Martin C, Feldman R, Leckman JF (2011) Oxytocin and social motivation. Dev Cogn Neurosci 1(4):471–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Grinevich V, Stoop R (2018) Interplay between oxytocin and sensory systems in the orchestration of socio-emotional behaviors. Neuron 99(5):887–904

    Article  CAS  PubMed  Google Scholar 

  • Grippo AJ, Gerena D, Huang J, Kumar N, Shah M, Ughreja R, Carter CS (2007) Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 32(8–10):966–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han RT, Kim YB, Park EH, Kim JY, Ryu C, Kim HY, Na HS et al (2018) Long-term isolation elicits depression and anxiety-related behaviors by reducing oxytocin-induced GABAergic transmission in central amygdala. Front Mol Neurosci 11:246

    Article  PubMed  PubMed Central  Google Scholar 

  • Harvey BH, Regenass W, Dreyer W, Möller M (2019) Social isolation rearing-induced anxiety and response to agomelatine in male and female rats: role of corticosterone, oxytocin, and vasopressin. J Psychopharmacol 33(5):640–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkley LC, Capitanio JP (2015) Perceived social isolation, evolutionary fitness and health outcomes: a lifespan approach. Philos Trans R Soc Lond B Biol Sci 370(1669):20140114

    Article  PubMed  PubMed Central  Google Scholar 

  • Holekamp KE, Strauss ED (2016) Aggression and dominance: an interdisciplinary overview. Curr Opin Behav Sci 12:44–51

    Article  Google Scholar 

  • Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7(7):e1000316

    Article  PubMed  PubMed Central  Google Scholar 

  • Holt-Lunstad J, Smith TB, Baker M, Harris T, Stephenson D (2015) Loneliness and social isolation as risk factors for mortality: a meta-analytic review. Perspect Psychol Sci 10(2):227–237

    Article  PubMed  Google Scholar 

  • House JS, Landis KR, Umberson D (1988) Social relationships and health. Science 241(4865):540–545

    Article  CAS  PubMed  Google Scholar 

  • Insel TR (1986) Postpartum increases in brain oxytocin binding. Neuroendocrinology 44(4):515–518

    Article  CAS  PubMed  Google Scholar 

  • Johnson ZV, Young LJ (2015) Neurobiological mechanisms of social attachment and pair bonding. Curr Opin Behav Sci 3:38–44

    Article  PubMed  PubMed Central  Google Scholar 

  • Jong TRD, Neumann ID (2017) Oxytocin and aggression. Curr Top Behav Neurosci:175–192

    Google Scholar 

  • Jurek B, Neumann ID (2018) The oxytocin receptor: from intracellular signaling to behavior. Physiol Rev 98(3):1805–1908

    Article  CAS  PubMed  Google Scholar 

  • Jurek B, Slattery DA, Hiraoka Y, Liu Y, Nishimori K, Aguilera G, Van Den Burg EH et al (2015) Oxytocin regulates stress-induced Crf gene transcription through CREB-regulated transcription coactivator 3. J Neurosci 35(35):12248–12260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karns CM, Moore WE III, Mayr U (2017) The cultivation of pure altruism via gratitude: a functional MRI study of change with gratitude practice. Front Hum Neurosci 599

    Google Scholar 

  • Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci 361(1476):2215–2228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Grinevich V (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73(3):553–566

    Article  CAS  PubMed  Google Scholar 

  • Krause J, Ruxton GD, Ruxton G, Ruxton IG et al (2002) Living in groups. Oxford University Press

    Book  Google Scholar 

  • Krause J, Ruxton GD, Krause S (2010) Swarm intelligence in animals and humans. Trends Ecol Evol 25(1):28–34

    Article  PubMed  Google Scholar 

  • Krimberg JS, Lumertz FS, Orso R, Viola TW, de Almeida RMM (2022) Impact of social isolation on the oxytocinergic system: A systematic review and meta-analysis of rodent data. Neurosci Biobehav Rev 104549:104549

    Article  Google Scholar 

  • Layden EA, Cacioppo JT, Cacioppo S (2018) Loneliness predicts a preference for larger interpersonal distance within intimate space. PLoS One 13(9):e0203491

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee HJ, Macbeth AH, Pagani JH, Young WS 3rd (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88(2):127–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lehtonen J, Jaatinen K (2016) Safety in numbers: the dilution effect and other drivers of group life in the face of danger. Behav Ecol Sociobiol 70(4):449–458

    Article  Google Scholar 

  • Lee CR, Chen A, Tye KM (2021) The neural circuitry of social homeostasis: Consequences of acute versus chronic social isolation. Cell 184(6):1500–1516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lui C, Cui XG, Wang YX, You ZD, Xu DF (2010) Association between neuropeptide oxytocin and male infertility. J Assist Reprod Genet 27(9):525–531

    Article  PubMed  PubMed Central  Google Scholar 

  • Maier A, Scheele D, Spengler FB, Menba T, Mohr F, Güntürkün O, Hurlemann R et al (2019) Oxytocin reduces a chemosensory-induced stress bias in social perception. Neuropsychopharmacology 44(2):281–288

    Article  CAS  PubMed  Google Scholar 

  • Marlin BJ, Mitre M, D’amour JA, Chao MV, Froemke RC (2015) Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520(7548):499–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McQuaid RJ, McInnis OA, Matheson K, Anisman H (2016) Oxytocin and social sensitivity: gene polymorphisms in relation to depressive symptoms and suicidal ideation. Front Hum Neurosci 10:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Mehta PH, Beer J (2010) Neural mechanisms of the testosterone–aggression relation: the role of orbitofrontal cortex. J Cogn Neurosci 22(10):2357–2368

    Article  PubMed  Google Scholar 

  • Mumtaz F, Khan MI, Zubair M, Dehpour AR (2018) Neurobiology and consequences of social isolation stress in animal model—A comprehensive review. Biomed Pharmacother 105:1205–1222

    Article  CAS  PubMed  Google Scholar 

  • Nair HP, Gutman AR, Davis M, Young LJ (2005) Central oxytocin, vasopressin, and corticotropin-releasing factor receptor densities in the basal forebrain predict isolation potentiated startle in rats. J Neurosci 25(49):11479–11488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasanbuyan N, Yoshida M, Takayanagi Y, Inutsuka A, Nishimori K, Yamanaka A, Onaka T (2018) Oxytocin–oxytocin receptor systems facilitate social defeat posture in male mice. Endocrinology 159(2):763–775

    Article  CAS  PubMed  Google Scholar 

  • Neumann ID (2007) Stimuli and consequences of dendritic release of oxytocin within the brain. Biochem Soc Trans 35(5):1252–1257

    Article  CAS  PubMed  Google Scholar 

  • Neumann ID, Slattery DA (2016) Oxytocin in general anxiety and social fear: a translational approach. Biol Psychiatry 79(3):213–221

    Article  CAS  PubMed  Google Scholar 

  • Nillni EA (2010) Regulation of the hypothalamic thyrotropin releasing hormone (TRH) neuron by neuronal and peripheral inputs. Front Neuroendocrinol 31(2):134–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunes AR, Carreira L, Anbalagan S, Blechman J, Levkowitz G, Oliveira RF (2020) Perceptual mechanisms of social affiliation in zebrafish. Sci Rep 10(1):1–14

    Article  Google Scholar 

  • Nunes AR, Gliksberg M, Varela SAM, Teles M, Wircer E, Blechman J, Petri G, Levkowitz G, Oliveira RF (2021) Developmental effects of oxytocin neurons on social affiliation and processing of social information. J Neurosci 41(42):8742–8760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O'Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519(18):3599–3639

    Article  PubMed  Google Scholar 

  • Okruszek Ł, Piejka A, Krawczyk M, Schudy A, Wiśniewska M, Żurek K, Pinkham A (2021) Owner of a lonely mind? Social cognitive capacity is associated with objective, but not perceived social isolation in healthy individuals. J Res Pers 93:104103

    Article  Google Scholar 

  • Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW (2013) Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 500(7463):458–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker KJ, Buckmaster CL, Schatzberg AF, Lyons DM (2005) Intranasal oxytocin administration attenuates the ACTH stress response in monkeys. Psychoneuroendocrinology 30(9):924–929

    Article  CAS  PubMed  Google Scholar 

  • Parra-Montes de Oca MA, Gutiérrez-Mariscal M, Salmerón-Jiménez MF, Jaimes-Hoy L, Charli JL, Joseph-Bravo P (2019) Voluntary exercise-induced activation of thyroid axis and reduction of white fat depots is attenuated by chronic stress in a sex dimorphic pattern in adult rats. Front Endocrinol 10:418

    Article  Google Scholar 

  • Pekarek BT, Hunt PJ, Arenkiel BR (2020) Oxytocin and sensory network plasticity. Front Neurosci 14:30

    Article  PubMed  PubMed Central  Google Scholar 

  • Peris J, MacFadyen K, Smith JA, de Kloet AD, Wang L, Krause EG (2017) Oxytocin receptors are expressed on dopamine and glutamate neurons in the mouse ventral tegmental area that project to nucleus accumbens and other mesolimbic targets. J Comp Neurol 525(5):1094–1108

    Article  CAS  PubMed  Google Scholar 

  • Perkeybile AM, Carter CS, Wroblewski KL, Puglia MH, Kenkel WM, Lillard TS, Connelly JJ et al (2019) Early nurture epigenetically tunes the oxytocin receptor. Psychoneuroendocrinology 99:128–136

    Article  CAS  PubMed  Google Scholar 

  • Pitcher TJ (1986) Functions of shoaling behaviour in teleosts. In: The behaviour of teleost fishes. Springer, Boston, MA, pp 294–337

    Chapter  Google Scholar 

  • Pittman TS, Heller JF (1987) Social motivation. Annu Rev Psychol 38(1):461–490

    Article  Google Scholar 

  • Rault JL, Carter CS, Garner JP, Marchant-Forde JN, Richert BT, Lay DC Jr (2013) Repeated intranasal oxytocin administration in early life dysregulates the HPA axis and alters social behavior. Physiol Behav 112:40–48

    Article  PubMed  Google Scholar 

  • Recoquillay J, Leterrier C, Calandreau L, Bertin A, Pitel F, Gourichon D, Arnould C et al (2013) Evidence of phenotypic and genetic relationships between sociality, emotional reactivity and production traits in Japanese quail. PLoS One 8(12):e82157

    Article  PubMed  PubMed Central  Google Scholar 

  • Ribeiro D, Nunes AR, Teles M, Anbalagan S, Blechman J, Levkowitz G, Oliveira RF (2020) Genetic variation in the social environment affects behavioral phenotypes of oxytocin receptor mutants in zebrafish. elife 9:e56973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers-Carter MM, Christianson JP (2019) An insular view of the social decision-making network. Neurosci Biobehav Rev 103:119–132

    Article  PubMed  PubMed Central  Google Scholar 

  • Salehi MS, Khazali H, Mahmoudi F, Janahmadi M (2017) Oxytocin intranasal administration affects neural networks upstream of GNRH neurons. J Mol Neurosci 62(3):356–362

    Article  CAS  PubMed  Google Scholar 

  • Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16(5):290–304

    Article  CAS  PubMed  Google Scholar 

  • Segerson TP, Kauer J, Wolfe HC, Mobtaker H, Wu P, Jackson IM, Lechan RM (1987) Thyroid hormone regulates TRH biosynthesis in the paraventricular nucleus of the rat hypothalamus. Science 238(4823):78–80

    Article  CAS  PubMed  Google Scholar 

  • Segura B, Melo AI, Fleming AS, Mendoza-Garrido ME, González del Pliego M, Aguirre-Benitez EL et al (2014) Early social isolation provokes electrophysiological and structural changes in cutaneous sensory nerves of adult male rats. Dev Neurobiol 74(12):1184–1193

    Article  PubMed  Google Scholar 

  • Seyfarth RM, Cheney DL (2015) Social cognition. Anim Behav 103:191–202

    Article  Google Scholar 

  • Shepherdson DJ, Mellen JD, Hutchins M (eds) (1999) Second nature: environmental enrichment for captive animals. Smithsonian Institution

    Google Scholar 

  • Shor E, Roelfs DJ (2015) Social contact frequency and all-cause mortality: a meta-analysis and meta-regression. Soc Sci Med 128:76–86

    Article  PubMed  Google Scholar 

  • Silk JB (2007) Social components of fitness in primate groups. Science 317(5843):1347–1351

    Article  CAS  PubMed  Google Scholar 

  • Soler-Gonzalez J, San-Martín M, Delgado-Bolton R, Vivanco L (2017) Human connections and their roles in the occupational Well-being of healthcare professionals: a study on loneliness and empathy. Front Psychol 8:1475

    Article  PubMed  PubMed Central  Google Scholar 

  • Song Z, Albers HE (2018) Cross-talk among oxytocin and arginine-vasopressin receptors: relevance for basic and clinical studies of the brain and periphery. Front Neuroendocrinol 51:14–24

    Article  CAS  PubMed  Google Scholar 

  • Stevenson JR, McMahon EK, Boner W, Haussmann MF (2019) Oxytocin administration prevents cellular aging caused by social isolation. Psychoneuroendocrinology 103:52–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sumpter DJ (2006) The principles of collective animal behaviour. Philos Trans R Soc Lond B Biol Sci 361(1465):5–22

    Article  CAS  PubMed  Google Scholar 

  • Székely T, Moore AJ, Komdeur J (eds) (2010) Social behaviour: genes, ecology and evolution. Cambridge University Press

    Google Scholar 

  • Tanaka K, Osako Y, Yuri K (2010) Juvenile social experience regulates central neuropeptides relevant to emotional and social behaviors. Neuroscience 166(4):1036–1042

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Osako Y, Takahashi K, Hidaka C, Tomita K, Yuri K (2019) Effects of post-weaning social isolation on social behaviors and oxytocinergic activity in male and female rats. Heliyon 5(5):e01646

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor DA, Altman I, Wheeler L, Kushner EN (1969) Personality factors related to response to social isolation and confinement. J Consult Clin Psychol 33(4):411

    Article  CAS  PubMed  Google Scholar 

  • Theofanopoulou C, Gedman G, Cahill JA, Boeckx C, Jarvis ED (2021) Universal nomenclature for oxytocin–vasotocin ligand and receptor families. Nature 592(7856):747–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tirko NN, Eyring KW, Carcea I, Mitre M, Chao MV, Froemke RC, Tsien RW (2018) Oxytocin transforms firing mode of CA2 hippocampal neurons. Neuron 100(3):593–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tops S, Habel U, Radke S (2019) Genetic and epigenetic regulatory mechanisms of the oxytocin receptor gene (OXTR) and the (clinical) implications for social behavior. Horm Behav 108:84–93

    Article  CAS  PubMed  Google Scholar 

  • Tribollet E, Charpak S, Schmidt A, Dubois-Dauphin M, Dreifuss JJ (1989) Appearance and transient expression of oxytocin receptors in fetal, infant, and peripubertal rat brain studied by autoradiography and electrophysiology. J Neurosci 9(5):1764–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uvnäs Moberg K, Julius H, Handlin L, Petersson M (2022) Sensory stimulation and oxytocin: their roles in social interaction and health promotion. Front Psychol 13:929741

    Article  PubMed  PubMed Central  Google Scholar 

  • Valtcheva S, Froemke RC (2019) Neuromodulation of maternal circuits by oxytocin. Cell Tissue Res 375(1):57–68

    Article  CAS  PubMed  Google Scholar 

  • Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD (2004) Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo–pituitary–adrenal activity. J Neurosci 24(12):2974–2982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Windle RJ, Shanks N, Lightman SL, Ingram CD (1997) Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 138(7):2829–2834

    Article  CAS  PubMed  Google Scholar 

  • Winter J, Jurek B (2019) The interplay between oxytocin and the CRF system: regulation of the stress response. Cell Tissue Res 375(1):85–91

    Article  CAS  PubMed  Google Scholar 

  • Winter J, Meyer M, Berger I, Royer M, Bianchi M, Kuffner K, Neumann ID et al (2021) Chronic oxytocin-driven alternative splicing of Crfr2α induces anxiety. Mol Psychiatry:1–14

    Google Scholar 

  • Witten L, Oranje B, Mørk A, Steiniger-Brach B, Glenthøj BY, Bastlund JF (2014) Auditory sensory processing deficits in sensory gating and mismatch negativity-like responses in the social isolation rat model of schizophrenia. Behav Brain Res 266:85–93

    Article  PubMed  Google Scholar 

  • Wright S, Silard A (2021) Unravelling the antecedents of loneliness in the workplace. Hum Relat 74(7):1060–1081

    Article  Google Scholar 

  • Yoshida M, Takayanagi Y, Inoue K, Kimura T, Young LJ, Onaka T, Nishimori K (2009) Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29(7):2259–2271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young LJ, Zhang Q (2021) On the origins of diversity in social behavior. Jpn J Animal Psychol 71:71–71

    Article  Google Scholar 

  • Zhang JB, Chen L, Lv ZM, Niu XY, Shao CC, Zhang C, Ding YQ et al (2016) Oxytocin is implicated in social memory deficits induced by early sensory deprivation in mice. Mol Brain 9:1–13

    Article  Google Scholar 

  • Zheng JJ, Li SJ, Zhang XD, Miao WY, Zhang D, Yao H, Yu X (2014) Oxytocin mediates early experience–dependent cross-modal plasticity in the sensory cortices. Nat Neurosci 17(3):391–399

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Babygirija R, Bülbül M, Cerjak D, Ludwig K, Takahashi T (2010) Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am J Physiol Gastrointest Liver Physiol 299(4):G946–G953

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuckerman M, Persky H, Link KE, Basu GK (1968a) Responses to confinement: an investigation of sensory deprivation, social isolation, restriction of movement and set factors. Percept Mot Skills 27(1):319–334

    Article  CAS  PubMed  Google Scholar 

  • Zuckerman M, Persky H, Link KE, Basu GK (1968b) Experimental and subject factors determining responses to sensory deprivation, social isolation, and confinement. J Abnorm Psychol 73(3p1):183

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

This review was conducted as part of KK’s Research Fellowship by the Portuguese Foundation for Science and Technology (Fundação para a Ciência e a Tecnologia - FCT; 2021.01659.CEECIND)and was funded by the FCT grant PTDC/BIA-COM/3068/2020 awarded to RFO.

Key References

  • House, J. S., Landis, K. R., & Umberson, D. (1988). Social relationships and health. Science, 241(4865), 540–545. This was one of the first studies to provide a synthesis of evidence on how social conditions can affect mortality rates through psychobehavioural implications and ultimate health outcomes.

  • Holt-Lunstad, J., Smith, T. B., & Layton, J. B. (2010). Social relationships and mortality risk: a meta-analytic review. PLoS medicine, 7(7), e1000316. This meta-analytic study provided one of the most comprehensive quantifications of mortality effects from social conditions, including isolation-loneliness and poor social relationships, as compared to other leading lifestyle factors, such as obesity, exercise, alcohol consumption and smoking.

  • O’Connell, L. A., & Hofmann, H. A. (2012) Evolution of a vertebrate social decision-making network. Science, 336(6085), 1154–1157. This hallmark study put forward compelling support for the evolutionary conservation of a vertebrate network of social behaviour, reward and relay brain areas, and quantified the level of conservation of signalling neuropeptide and endocrine systems across this network, enforcing the fundamental role of oxytocin signalling by the maintenance of oxytocin receptors.

  • Capitanio, J. P., Cacioppo, S., & Cole, S. W. (2019). Loneliness in monkeys: neuroimmune mechanisms. Current opinion in behavioural sciences, 28, 51–57. This was the first study to provide both a behavioural paradigm for inducing perceived loneliness in non-human animals, based on individual sociality levels and reciprocity from others, and how this influences immune function and associated stress-physiology, as well as susceptibility to a real-life immune challenge.

  • Lee, C. R., Chen, A., & Tye, K. M. (2021). The neural circuitry of social homeostasis: Consequences of acute versus chronic social isolation. Cell, 184(6), 1500–1516. This is a recent and compelling review offering a new social homeostasis framework for approaching the study of neuroendocrine mechanisms of social isolation stress, enabling the assessment of duration-based shifts and the identification of implicated components across a three-tier structure from detectors, to a command centre and ultimately an effector system.

Author information

Authors and Affiliations

  1. Instituto Gulbenkian de Ciência, Oeiras, Portugal

    Kyriacos Kareklas & Rui F. Oliveira

  2. Champalimaud Centre for the Unknown, Lisbon, Portugal

    Rui F. Oliveira

  3. ISPA–Instituto Universitário, Lisbon, Portugal

    Rui F. Oliveira

Authors
  1. Kyriacos Kareklas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rui F. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rui F. Oliveira .

Editor information

Editors and Affiliations

  1. Department of Biological Sciences, Kent State University, Kent, OH, USA

    Heather K. Caldwell

  2. Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA, USA

    H. Elliott Albers

Rights and permissions

Reprints and permissions

Copyright information

© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kareklas, K., Oliveira, R.F. (2024). Oxytocin and Social Isolation: Nonapeptide Regulation of Social Homeostasis. In: Caldwell, H.K., Albers, H.E. (eds) Neuroendocrinology of Behavior and Emotions. Masterclass in Neuroendocrinology, vol 16. Springer, Cham. https://doi.org/10.1007/978-3-031-51112-7_8

Download citation

Publish with us

Policies and ethics

Search

Navigation