Serotonin and neuropeptides in affiliative behaviors

Insel, Thomas R.; Winslow, James T.

doi:10.1016/s0006-3223(98)00094-8

Cited by 105Neuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on BehaviorNeuropeptides and Animal Physiology

Serotonin and neuropeptides in affiliative behaviors

Insel, Thomas R., Winslow, James T.·1998·Biological Psychiatry

DOI 10.1016/s0006-3223(98)00094-8

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Abstract

The neuropharmacological study of serotonin and behavior has followed two fundamentally different strategies. One approach has used behavior as a dependent variable for assaying drug effects. To characterize serotonergic drugs, most studies have used relatively simple behaviors, such as locomotor activity, startle, exploration, operant responses, and sleep. A second approach has focused on behavior, with drugs used as tools to elucidate the physiological role of serotonin. These studies have increasingly focused on behaviors of ethological importance, including aggression, sexual behavior, and other forms of social interaction. Here we review studies using this approach to focus on one particular kind of social interaction: affiliation.

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Animal studies show that early stressors result in long-term changes in peptides such as oxytocin that regulate pair bonding and social attachment.
“Animal studies show that early stressors result in long-term changes in peptides such as oxytocin that regulate pair bonding and social attachment (Insel and Winslow 1998; Francis 2002).”
From The enduring effects of abuse and related adverse experiences in childhood: A convergence of evidence from neurobiology and epidemiology (2006) · cites this paper as Insel and Winslow 1998

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Association between serotonin transporter genotype and extraversion
Gillihan, S. J., Farah, M., Sankoorikal, G., Breland, J. Y., & Brodkin, E. (2007) · Psychiatric Genetics · doi:10.1097/ypg.0b013e3281ac236e · Cited by 21 · see citing works
“Moreover, serotonergic pathways affect affiliative behaviors and other social behaviors in humans, other primates, and rodents (Insel and Winslow, 1998; Tse and Bond, 2002; Suomi, 2003).”
Background
Serotonergic function, behavioral disinhibition, and negative affect in children of alcoholics: the moderating effects of puberty.
Twitchell, G. R., Hanna, G., Cook, E., Fitzgerald, H., & Zucker, R. (2000) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2000.tb04639.x · Cited by 20 · see citing works
Endophenotypes for Marital Status in the NAS-NRC Twin Registry
Trumbetta, S., & Gottesman, I. (2000) · Springer eBooks · doi:10.1007/978-1-4615-4467-8_15 · Cited by 20 · see citing works
An Association Between Serotonin 1A Receptor, Gray Matter Volume, and Sociability in Healthy Subjects and in Autism Spectrum Disorder
Lefèvre, A., Richard, N., Mottolese, R., Leboyer, M., & Angela Sirigu, B. (2020) · Autism Research · doi:10.1002/aur.2360 · Cited by 18 · see citing works
Perinatal Risk Factors in the Development of Aggression and Violence
LaPrairie, J. L., Schechter, J. C., Robinson, B. A., & Brennan, P. A. (2011) · Advances in genetics · doi:10.1016/b978-0-12-380858-5.00004-6 · Cited by 21 · see citing works
Behavioral, neurochemical, and neuroimmune changes associated with social buffering and stress contagion
Chun, E. K., Donovan, M., Liu, Y., & Wang, Z. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100427 · Cited by 18 · see citing works
“5-HT has oftentimes been characterized as “prosocial” due to its positive correlation with affiliative behaviors and negative association with aggression and isolation in males (Insel and Winslow, 1998; Siegel and Crockett, 2013; Young and Leyton, 2002).”
Background
Providing straw to allow exploratory behaviour in a pig experimental system does not modify putative indicators of positive welfare: peripheral oxytocin and serotonin
Marcet‐Rius, M., Cozzi, A., Bienboire‐Frosini, C., Teruel, E., Chabaud, C., Monneret, P., Leclercq, J., Lafont‐Lecuelle, C., & Pageat, P. (2018) · animal · doi:10.1017/s175173111800006x · Cited by 27 · see citing works
Affiliation in Four Echimyid Rodent Species based on Intrasexual Dyadic Encounters: Evolutionary Implications
de Freitas, J. N. S., El-Hani, C., & da Rocha, P. L. B. (2008) · doi:10.1111/j.1439-0310.2008.01481.x · Cited by 16
Assessing Sociability, Social Memory, and Pup Retrieval in Mice
Zimprich, A., Niessing, J., Cohen, L., Garrett, L., Einicke, J., Sperling, B., Schmidt, M. V., & Hölter, S. M. (2017) · Current Protocols in Mouse Biology · doi:10.1002/cpmo.36 · Cited by 12 · see citing works
“COMMENTARY Background Information As outlined by Insel and Winslow (1998), the study of complex social behaviors provides an important basic science for psychiatry because the detailed understanding of the role of neurotransmitters, neuropeptides, neural circuits, and genetic pathways involved in…”
Background
Influence of toys on behavioural patterns of pigs and their association with the concentration of serotonin in blood plasma
Lykhach, A., Lykhach, V., Шпетний, М. Б., Mykhalko, О., & Zhyzhka, S. V. (2020) · Regulatory Mechanisms in Biosystems · doi:10.15421/022022 · Cited by 11 · see citing works
“At low concentration of serotonin in blood plasma in animals, aggressive behaviour, disorders, frustration, boredom were observed, therefore reducing the productivity of quality of pigs (Insel & Winslow, 1998; Young & Moskowitz, 2005).”
Background
Conditional approach as cooperation in predator inspection: A role for serotonin?
Pimentel, A. F. N., Carvalho, T. D. S., Lima, F., Lima, M. G., Soares, M. C., & Maximino, C. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.005 · Cited by 10 · see citing works
“This monoamine participates in the modulation of stress and defensive behaviour in fish (Herculano & Maximino, 2014; Soares, Gerlai, & Maximino, 2018; Winberg & Thörnqvist, 2016)◻, and has been implicated in vertebrate social behaviour (Insel & Winslow, 1998; Soares, Gerlai, et al., 2018)◻.”
Background
Chronic postnatal monoamine oxidase inhibition affects affiliative behavior in rat pups
Blažević, S. A., Merkler, M., Peršić, D., & Hranilović, D. (2016) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2016.12.008 · Cited by 12 · see citing works
“Dopamine receptor agonists (Dastur et al., 1999) and reuptake inhibitors (Kehoe and Boylan, 1992) are shown to significantly reduce USV.”
Perspectives on Human Attachment (Pair Bonding): Eve's Unique Legacy of a Canine Analogue
Immerman, R. S., & Mackey, W. C. (2003) · Evolutionary Psychology · doi:10.1177/147470490300100110 · Cited by 9 · see citing works
Pre-weaning social behaviours and peripheral serotonin levels are associated with behavioural and physiological responses to weaning and social mixing in pigs
Clouard, C., Resmond, R., Vesque-Annear, H., Prunier, A., & Merlot, E. (2023) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2023.105833 · Cited by 9 · see citing works
Neuroendocrine Mechanisms Underlying the Intergenerational Transmission of Maternal Behavior and Infant Abuse in Rhesus Macaques
Dario Maestripieri, A. (2008) · Springer eBooks · doi:10.1007/978-3-540-79288-8_9 · Cited by 8 · see citing works
“Although serotonin might affect maternal motivation through its actions on oxytocin or prolactin release, serotonin and other monoamines are generally viewed as having aspecific effects on emotionality, motivation, or memory rather than specific effects on parentally motivated behaviors ( Insel and Winslow 1998; Numan…”
The Role of the Brain Serotonergic System in the Origin and Transmission of Adaptive and Maladaptive Variations in Maternal Behavior in Rhesus Macaques
Dario Maestripieri, A. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374285-8.00011-1 · Cited by 5 · see citing works
“Effects of mothering style on offspring behavior have been shown to extend into adulthood ( Fairbanks & McGuire, 1988 ; 1993; Schino et al. , 2001 ; Bardi et al. , 2005 ; Bardi & Huffman, 2006 ; Maestripieri et al. , 2006b ).”
Background
Antidepressant Psychopharmacology and the Social Brain
Novick, A. M. (2011) · Psychiatry · doi:10.1521/psyc.2011.74.1.72 · Cited by 7 · see citing works
“This neurotransmitter, which is enhanced by multiple classes of antidepressants, is involved in mitigating the response to separation, promoting grooming and affiliative behaviors, as well as decreasing aggression (Insel & Winslow, 1998).”
Background
The Neurochemical Basis of Motivation for Affiliative Touch
Løseth, G. E., Leknes, S., & Ellingsen, D. (2016) · Springer eBooks · doi:10.1007/978-1-4939-6418-5_15 · Cited by 5 · see citing works
Obsessional Jealousy: A Narrative Literature Review
Sheikhmoonesi, F. (2017) · Iranian Journal of Psychiatry and Behavioral Sciences · doi:10.5812/ijpbs.7273 · Cited by 5 · see citing works
“According to neurobiological aspects, jealousy involves the attachment system (oxytocin) (12, 13) and different neurotransmitters such as 5HT (12, 14, 15).”
Background
The father(to)child affiliative bond: Convergent evolution with the canid analogue
Mackey, W. C., & Immerman, R. S. (2003) · Biodemography and Social Biology · doi:10.1080/19485565.2003.9989064 · Cited by 3 · see citing works
About possible functional interaction between serotonin and neuropeptides in control processes of embryogenesis (Experiments on embryos ofTritonia diomedea)
Willows, A., Nikitina, L. A., Bezuglov, V., Gretskaya, N., & Buznikov, G. (2000) · Russian Journal of Developmental Biology · doi:10.1007/bf02758813 · Cited by 4
“Neuropeptides coexist in the neurons and functionally interact with classical neurotransmitters, specifically with serotonin (Buznikov, 1990; Insel and Winslow, 1998; Weiss et al., 1998).”
Background
Involvement of Serotonergic Projections from the Dorsal Raphe to the Medial Preoptic Area in the Regulation of the Pup-Directed Paternal Response of Male Mandarin Voles
Lv, Z., Li, L., Li, Y., Zhang, L., Guo, X., Huang, C., Hou, W., Qu, Y., Liu, L., Li, Y., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411605 · Cited by 3 · see citing works
“It has been found that 5-HT alters maternal behaviors and increases the affiliative behaviors of males [32,47].”
Background
Molecular Genetics Meets Sociology: Birth Cohort Effects on Alcohol Use and Relationship With Candidate Genes
Harro, J., & Vaht, M. (2019) · Neuroscience of Alcohol · doi:10.1016/b978-0-12-813125-1.00002-7 · Cited by 3 · see citing works
Serotonin blocker Ketanserin reduces coral reef fish Ctenochaetus striatus aggressive behaviour during between-species social interactionsPreprint
Staubli, V., Bshary, R., & Triki, Z. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.20.524902 · Cited by 1 · see citing works
“…cooperative cleaner fish, we conclude that serotonin does affect the client’s tolerance levels to proximity by cleaner fish, similar to what has been described in the literature about serotonin’s role in conspecifics’ tolerance and close contact (Insel and Winslow, 1998; Stettler et al., 2021).”
Background
Physiological and behavioural indicators of positive animal welfare in pigs
Marcet‐Rius, M. (2019) · doi:10.70675/9045e97cz3be7z4880z8de3zec989917b9d3
“Some authors suggested that serotonin may also promote calm, prosocial interactions, such as allogrooming in vervet monkeys and positive social interaction in young adult humans, both of which are positively associated with increased serotonin activity (Insel and Winslow, 1998).”
Influential
Role of vasopressin V1a receptor in ∆9-tetrahydrocannabinol-induced cataleptic immobilization in mice
Egashira, N., Koushi, E., Myose, T., Tanoue, A., Mishima, K., Tsuchihashi, R., Kinjo, J., Tanaka, H., Morimoto, S., & Iwasaki, K. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4735-1 · Cited by 3 · see citing works
Lessons from Neuroscience and Experimental Psychology for a Partnership Society
Levine, D. S. (2015) · Interdisciplinary Journal of Partnership Studies · doi:10.24926/ijps.v2i2.111 · Cited by 3 · see citing works
“But Thomas Insel, James Winslow, and their colleagues discovered that oxytocin has broader importance for bonding, in male as well as female animals (Insel, 1992; Insel & Winslow, 1998; Winslow, Shapiro, Carter, & Insel, 1993).”
Serotonin-manipulated juvenile green sea turtles Chelonia mydas exhibit reduced fear-like behaviour
Kudo, H., Okuyama, M., Sakamoto, K. Q., Uchida, K., & Sato, K. (2021) · Endangered Species Research · doi:10.3354/esr01153 · Cited by 1 · see citing works
Evolutionary Neuroscience and Motivation in Organizations
Wood, R. C., Levine, D. S., Cory, G. A., & Wilson, D. R. (2015) · Emerald Group Publishing Limited eBooks · doi:10.1108/s1479-357120150000007005 · Cited by 4 · see citing works
The serotonin blocker Ketanserin reduces coral reef fish Ctenochaetus striatus aggressive behaviour during between-species social interactions
Staubli, V., Bshary, R., & Triki, Z. (2024) · PeerJ · doi:10.7717/peerj.16858
A Bridge between Psychoanalysis and Neuroscience: An Overview of the Neurobiological Effects of Psychoanalytical Psychotherapy
Cohen, D. (2021) · Journal of Psychology and Neuroscience · doi:10.47485/2693-2490.1049
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Ευθυμίου, Κ., & Καπνογιάννη, Σ. (2020) · Psychology the Journal of the Hellenic Psychological Society · doi:10.12681/psy_hps.23538
Neural mechanisms of oxytocin and serotonin interaction in non-human primates and patients with autism
Lefevre, A. (2016) · doi:10.70675/137893f0z4808z4aa8z9008z05c2a19b5144
“Thus, serotonin has been shown to modulate aggressiveness (Olivier, 2004) and affiliation (Insel and Winslow, 1998) in many different species including humans.”
Background
Age, Sex, and Parenting
Johnson, M. E., & Rausch, J. L. (2008) · Medical psychiatry · doi:10.3109/9780849383649.012
Examining Dehumanization Through the "Political Brain Perspective": Towards a Minimal Neuropolitical Theory for Hyperdiverse Societies
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“…where this new field moved away from a hitherto health-and-animal focused research agenda that had primarily analyzed how the social world affected the peripheral nervous system and other bodily systems (Cacioppo, 1994; Berntson, Sarter, and Cacioppo, 1989; Insel and Winslow, 1998; Panksepp, 1998).”
Background

Authors: Insel, T. R., & Winslow, J. T.
Affiliations: Emory University (US)
Corresponding author: Insel, Thomas R.
ORCID: Insel, Thomas R.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 1998-08
Volume: 44
Issue: 3
Pages: 207-219
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/s0006-3223(98)00094-8
OpenAlex: W2049240042
Cited by: 105
References: 0
Citations by year: 2026: 1 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 2 · 2021: 1 · 2020: 3 · 2019: 4 · 2018: 2 · 2017: 6 · 2016: 3 · 2015: 7 · 2014: 4 · 2013: 3 · 2012: 4
FWCI: 0.83
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: serotonin, neuropeptides, affiliative behavior, social interaction, serotonergic drugs, aggression, sexual behavior, social behavior
MeSH terms: Animals, Brain, Brain Mapping, Humans, Neuropeptides, Oxytocin, Serotonin, Social Behavior, Vasopressins

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Serotonin and neuropeptides in affiliative behaviors

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