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Nonapeptides and the evolutionary patterning of sociality
Open accessAbstract
Neuropeptides of the arginine vastocin (AVT) family, including the mammalian peptides arginine vasopressin (AVP) and oxytocin (OXT), comprise neuroendocrine circuits that range from being evolutionarily conserved to evolutionarily diverse. For instance, the functions and anatomy of the AVT/AVP projections to the pituitary (which arise in the preoptic area and hypothalamus) are strongly conserved, whereas the functions and anatomy of AVT/AVP circuits arising in the medial bed nucleus of the stria terminalis (BSTm) are species-specific and change rapidly over evolutionary time. Circuits arising in the BSTm mediate various affiliative behaviors and exhibit species-specific evolution in relation to mating system in mammals (monogamous vs. non-monogamous) and sociality in songbirds (gregarious vs. relatively asocial). In estrildid songbirds AVT neurons in the BSTm increase their Fos expression only in response to "positively-valenced" social stimuli (stimuli that normally elicit affiliation), whereas "negative" stimuli (which elicit aggression or aversion) produce no response or even suppress Fos expression. Relative to territorial species, gregarious species show: (1) greater social induction of Fos within AVT neurons, (2) a higher baseline of Fos expression in AVT neurons, (3) more AVT neurons in the BSTm and (4) a higher density of V(1a)-like binding sites in the lateral septum. Furthermore, septal AVT infusions inhibit resident-intruder aggression, but facilitate aggression that is motivated by mate competition (an affiliative context). This functional profile of the BSTm AVT neurons is quite distinct from that of hypothalamic AVT/AVP neurons, particularly those of the paraventricular nucleus (PVN), which are classically stress-responsive. This is paradoxical, given that AVT/AVP projections from the PVN and BSTm likely overlap. However, despite this overlap, each AVT/AVP cell group should produce a distinct pattern of modulation across brain regions. Relative weighting of hypothalamic and BSTm nonapeptide circuitries may therefore be an important determinant of approach-avoidance behaviour, and may be a prime target of natural selection related to sociality.
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In the citing paper
“AVP, OT, and their homologs regulate social behavior across vertebrate taxa (for review, see Goodson 2008; Kelly & Ophir 2015)”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as Goodson 2008
In the citing paper
“Central OTRs exhibit extraordinarily diverse expression patterns that are associated with individual and species differences in social behavior.”
From Oxytocin receptors modulate a social salience neural network in male prairie voles (2017) · cites this paper as Goodson, 2008
In the citing paper
“Central distribution patterns and region-specific densities of OT receptors (OTRs) have undergone rapid evolutionary divergence between closely related species of birds and mammals that exhibit divergent social behavior”
From Oxytocin receptors modulate a social salience neural network in male prairie voles (2017) · cites this paper as Goodson, 2008
In the citing paper
“comparative analyses have revealed that the effects of OT and AVP on social behavior are as complex and diverse as the differences in reproductive and social strategies found across the animal kingdom (Goodson, 2008; Kelly and Ophir, 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Goodson, 2008
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Cites
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · cited 10×
“AVT/AVP cells of the BSTm likely contribute to the regulation of multiple affiliative behaviours, including pair bonding in rodents (Young and Wang, 2004; De Vries and Panzica, 2006), but no research had previously determined how different classes of social stimuli elicit responses in these neurons.”
BackgroundInfluentialNeuroendocrine perspectives on social attachment and love
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Cerebral hemisphere regulation of motivated behavior
Swanson, L. W. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02905-x · Cited by 846
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
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The vertebrate social behavior network: Evolutionary themes and variations
Goodson, J. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.02.003 · Cited by 771
Self-citationGoodson, J. L., & Bass, A. H. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00043-1 · Cited by 646
Self-citationLim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J. (2004) · Nature · doi:10.1038/nature02539 · Cited by 628
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“…voles, mice and primates) point toward two brain areas as being relevant for monogamous pair bonding — the nucleus accumbens in the case of OXT receptors, and the ventral pallidum in the case of AVP V1a receptors (Wang et al., 1997; Young et al., 1999; Liu and Wang, 2003; Lim et al., 2004a).”
Background
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Cited by
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The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999
The Peptide That Binds: A Systematic Review of Oxytocin and its Prosocial Effects in Humans
MacDonald, K., & MacDonald, T. M. (2010) · Harvard Review of Psychiatry · doi:10.3109/10673220903523615 · Cited by 585
Bosch, O. J., & Neumann, I. D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.002 · Cited by 400
Graustella, A. J., & MacLeod, C. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.002 · Cited by 379
Genetics of Human Social Behavior
Ebstein, R. P., Israel, S., Chew, S. H., Zhong, S., & Knafo, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.020 · Cited by 323
Metadata
- Authors
- GOODSON, J.
- Affiliations
- Indiana University Bloomington (US)
- Corresponding author
- GOODSON, J
- Venue
- Progress in brain research
- Publisher
- Elsevier
- Published
- 2008
- Volume
- 170
- Pages
- 3-15
- ISSN
- 0079-6123 (ISSN-L)
- PMC
- PMC2570786
- OpenAlex
- W1538837544
- Cited by
- 228
- References
- 74
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 7 · 2023: 8 · 2022: 9 · 2021: 10 · 2020: 5 · 2019: 12 · 2018: 12 · 2017: 14 · 2016: 14 · 2015: 15 · 2014: 14 · 2013: 20 · 2012: 20
- FWCI
- 49.24
- Type
- book chapter
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Progress in brain research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH062656, MH62656)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- arginine vasotocin, vasopressin, oxytocin, nonapeptide, evolution of social behavior, Fos expression, songbirds, aggression, mate competition, approach-avoidance behavior, paraventricular nucleus, lateral septum, V1a receptor, affiliative behavior
- MeSH terms
- Animals, Annelida, Arginine Vasopressin, Brain, Fishes, Genetics, Behavioral, Humans, Neurons, Oligopeptides, Social Behavior, Vertebrates, Evolution, Molecular, MicroRNAs
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