Oxytocin-dependent consolation behavior in rodents
Open accessAbstract
Consolation behavior toward distressed others is common in humans and great apes, yet our ability to explore the biological mechanisms underlying this behavior is limited by its apparent absence in laboratory animals. Here, we provide empirical evidence that a rodent species, the highly social and monogamous prairie vole (Microtus ochrogaster), greatly increases partner-directed grooming toward familiar conspecifics (but not strangers) that have experienced an unobserved stressor, providing social buffering. Prairie voles also match the fear response, anxiety-related behaviors, and corticosterone increase of the stressed cagemate, suggesting an empathy mechanism. Exposure to the stressed cagemate increases activity in the anterior cingulate cortex, and oxytocin receptor antagonist infused into this region abolishes the partner-directed response, showing conserved neural mechanisms between prairie vole and human.
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Oxytocin acting in anterior cingulate cortex also mediates empathy-based consoling behaviors in prairie voles.
“Oxytocin acting in anterior cingulate cortex also mediates empathy-based consoling behaviors in prairie voles”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Burkett et al. 2016
Neuroendocrine studies link social bonding practices to release of oxytocin.
“Neuroendocrine studies (Burkett et al., 2016; Carter, 2014; Ma et al., 2016b; Samuni et al., 2017) have linked these and related practices to the release of oxytocin, a nine-amino acid neuropeptide.”
From Oxytocin promotes coordinated out-group attack during intergroup conflict in humans (2019) · cites this paper as Burkett et al., 2016
OT has been implicated in the onset of parental nurturing and maternal bonds, the consequences of parenting on the developing brain, pair bonding, empathy-based consoling behavior, and the consequences of social loss in animal models.
“Specifically, the neuropeptide oxytocin (OT) has been implicated in the onset of parental nurturing and maternal bonds (Bosch and Neumann 2012; Numan and Young 2016; Rilling and Young 2014), the consequences of parenting on the developing brain (Champagne et al. 2001; Barrett et al. 2015), pair bonding (Johnson et al. 2016; Johnson and Young 2015), empathy-based consoling behavior (Burkett et al.”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Burkett et al. 2016
There is an increase in anterior cingulate cortex activity in voles exposed to a stressed partner.
“Specifically, there is an increase in ACC activity in voles exposed to a stressed partner [93] and inhibition of ACC projections to the BLA prevents the acquisition of fear, as assessed by freezing, in observer mice [98,102,103].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [93]
Projections from the anterior cingulate cortex and insula to the basolateral amygdala have been implicated in social transfer of fear.
“Projections from the ACC and insula to the BLA have been implicated in this form of emotional contagion.”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [93]
Inhibition of oxytocin receptors in the anterior cingulate cortex alters interaction with a stressed partner.
“Antagonism of insula OXT receptors recapitulates the effects of optogenetic inhibition of this circuit [107] and inhibition of OXT receptors in the ACC similarly alters interaction with a stressed partner [93].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [93]
Oxytocin modulation of anterior cingulate cortex- and insula-to-basolateral amygdala circuits regulates social transfer of fear.
“OXT modulation of ACC-and insula-to-BLA circuits also regulates social transfer of fear.”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [93]
Prairie voles display empathy-based consoling behavior toward their distress partner, sibling, or familiar cage mate, which is mediated by OXTR in the anterior cingulate cortex, a region involved in empathetic responses in humans.
“Prairie voles also display empathy-based consoling behavior toward their distress partner, sibling, or familiar cage mate, which is mediated by OXTR in the anterior cingulate cortex, a region involved in empathetic responses in humans (8).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [8]
There are examples of prosocial responses to stressed conspecifics in both voles and mice.
“and there are examples of prosocial responses to stressed conspecifics in both voles21 and mice41.”
From Insular cortex mediates approach and avoidance responses to social affective stimuli (2018) · cites this paper as [21]
Some paradigms require learning or direct exposure to a conspecific in pain, making it difficult to isolate social affective processes from other motivations.
“However, some paradigms require learning or direct exposure to a conspecific in pain, making it difficult to isolate social affective processes from other motivations21,25.”
From Insular cortex mediates approach and avoidance responses to social affective stimuli (2018) · cites this paper as [21]
OT modulates social behaviors across species, including empathic cognition in both humans and rodents.
“OT modulates social behaviors across species19, including empathic cognition in both humans20 and rodents21.”
From Insular cortex mediates approach and avoidance responses to social affective stimuli (2018) · cites this paper as [21]
Sample sizes were consistent with those of previous studies.
“although sample sizes were consistent with those of previous studies [19,23,80].”
From Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice (2019) · cites this paper as [19]
Oxytocin, released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone.
“Oxytocin1,2,9–15, which is released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [12]
Oxytocin acts in the brain to increase the salience of social information and enable alloparenting in mice.
“Oxytocin also acts in the brain to increase the salience of social information and enable alloparenting in mice1,9,12–14.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [12]
Oxytocin signaling in insular cortex, central amygdala, and anterior cingulate cortex modulates emotion detection and responses to social affect of conspecifics.
“Additionally, oxytocin signaling in insular cortex, central amygdala, and anterior cingulate cortex modulates emotion detection and responses to social affect of conspecifics [26–28].”
From Translational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry (2021) · cites this paper as [27]
Prior investigations have provided evidence for neurons that encode another animal's familiarity or dominance.
“They have also provided evidence for neurons that encode another animals’ familiarity or dominance 12,13”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [12]
The mPFC is an area suggested to be involved in social behavior and disorders such as ASD.
“Here, we used microelectrode arrays that were implanted in the animal’s mPFC (Extended Data Fig. 1b), an area suggested to be involved in social behavior 1,7,12,26,34 and disorders such as ASD 14,21,35,36.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [12]
No statistical methods were used to predetermine sample sizes.
“No statistical methods were used to predetermine sample sizes, although sample sizes were consistent with those from previous studies of this kind7,9,29.”
From Oxytocin enhances observational fear in mice (2017) · cites this paper as [29]
Previous studies suggest that prairie voles show empathy-like behavior, such as freezing caused by emotional contagion of conspecifics' fear, and consolation.
“Previous studies suggest that prairie voles show empathy-like behavior, such as freezing caused by emotional contagion of conspecifics' fear, and consolation (Burkett et al., 2016; Stetzik et al., 2018; Wardwell et al., 2020).”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Burkett et al., 2016
Prairie voles exhibit allogrooming that functions as social buffering to relieve the fear of their partner.
“Prairie voles exhibit allogrooming that functions as social buffering to relieve the fear of their partner.”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Burkett et al., 2016
Allogrooming to a cagemate and a sibling is observed more frequently than that to a stranger in prairie voles.
“Allogrooming to a cagemate and a sibling is observed more frequently than that to a stranger (Burkett et al., 2016).”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Burkett et al., 2016
Upon reunion, naive observer prairie voles increase partner-directed grooming toward the stressed cagemate.
“Upon reunion, the naïve observer increased partner-directed grooming toward the stressed cagemate.”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Burkett et al. 2016
More grooming is observed in response to familiar conspecifics compared to strangers, resulting in a familiarity bias.
“More grooming was observed in response to familiar conspecifics compared to strangers, resulting in a familiarity bias.”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Burkett et al. 2016
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Adolescents growing up amidst intractable conflict attenuate brain response to pain of outgroup
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Intranasal oxytocin, but not vasopressin, augments neural responses to toddlers in human fathers
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Oxytocin promotes coordinated out-group attack during intergroup conflict in humans
Zhang, H., Gross, J., De Dreu, C., & Ma, Y. (2019) · eLife · doi:10.7554/elife.40698 · Cited by 87 · see citing works
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Neural mechanisms necessary for empathy-related phenomena across species
Paradiso, E., Gazzola, V., & Keysers, C. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.005 · Cited by 78 · see citing works
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Self-citationPupil-mimicry conditions trust in partners: moderation by oxytocin and group membership
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Thalamic integration of social stimuli regulating parental behavior and the oxytocin system
Dobolyi, A., Cservenák, M., & Young, L. J. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.05.002 · Cited by 64 · see citing works
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Oti, T., Satoh, K., Uta, D., Nagafuchi, J., Tateishi, S., Ueda, R., Takanami, K., Young, L. J., Galione, A., Morris, J. F., et al. (2021) · Current Biology · doi:10.1016/j.cub.2020.09.089 · Cited by 63 · see citing works
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“The prairie vole (Microtus ochrogaster) is a monogamous rodent species showing enduring pair bonding between mates, biparental care, and the consoling behavior toward a distressed partner (Young and Wang, 2004; Aragona et al., 2006; Gobrogge et al., 2009; Young et al., 2011; Johnson and Young, 2015; Burkett et al., 20…”
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Oxytocin, vasopressin and social behavior in the age of genome editing: a comparative perspective
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“This mapping enabled subsequent rodent studies to perform site-specific pharmacological manipulations in regions where OXTRs were expressed to delineate circuits where OT affects behavior (Bosch et al., 2016; Burkett et al., 2016).”
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Self-citation
- Authors
- Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J.
- Affiliations
- Emory University (US)
- Center for Translational Social Neuroscience, Emory University, Atlanta, GA, USA.
- Corresponding author
- Burkett, J. P.
- Young, L. J.
- Venue
- Science
- Published
- 2016-01-22
- Volume
- 351
- Issue
- 6271
- Pages
- 375-378
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4737486
- OpenAlex
- W2252899440
- Cited by
- 692
- References
- 47
- Citations by year
- 2026: 41 · 2025: 59 · 2024: 61 · 2023: 82 · 2022: 56 · 2021: 73 · 2020: 50 · 2019: 65 · 2018: 118 · 2017: 52 · 2016: 34
- FWCI
- 141.32
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (1P50MH100023, R01MH096983)
- NIGMS (T32GM08605-10, F31 MH102911-01)
- Emory University
- NIH (OD P51OD011132)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- oxytocin, Microtus ochrogaster, social buffering, empathy, anxiety, corticosterone, anterior cingulate cortex, oxytocin receptor antagonist, social stress, monogamy, rodents
- MeSH terms
- Animals, Anxiety, Anxiety, Separation, Corticosterone, Arvicolinae, Emotions, Female, Helping Behavior, Injections, Intraventricular, Male, Oxytocin, Stress, Psychological
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