The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent
Open accessAbstract
Social relationships significantly influence physiology and behavior, including the hypothalamo-pituitary-adrenal axis, anxiety, and mental health. Disruption of social bonds through separation or death often results in profound grieving, depression, and physical illness. As the monogamous prairie vole forms enduring, selective pair bonds with the mating partner, they provide an animal model to study the physiological consequences of pair bonding and, thus, the loss of the bonded partner. Male prairie voles were paired with a novel female or male sibling. After 5 days, half of the males of each group were separated from the partner. Elevated plus-maze, forced swim, and tail suspension tests were used to assess anxiety-like and passive stress-coping behaviors indicative of depressive-like behavior. Following 4 days of separation from the female but not the male partner, experimental males displayed increased passive stress-coping. This effect was abolished by long-term intracerebroventricular infusion of a nonselective corticotropin-releasing factor (CRF) receptor antagonist without disrupting the bond itself. Both CRF type 1 and 2 receptors were involved in the emergence of passive stress-coping behavior. Furthermore, pairing with a female was associated with elevated CRF mRNA in the bed nucleus of the stria terminalis, and partner loss elicited a pronounced increase in circulating corticosteroid and adrenal weight. We speculate that the CRF system may mediate an aversive affect following separation from the female partner, which may facilitate proximity seeking between the pair-bonded individuals. Hence, the prairie vole model may provide insights into brain mechanisms involved in the psychopathological consequences of partner loss.
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CRF mRNA is elevated in the BNST of pair-bonded male voles compared to non-paired males, and CRF2s colocalize to OT neurons in the PVN and OT fibers projecting to the NAc.
“Interestingly, CRF mRNA is elevated in the BNST of pair-bonded male voles, as compared to non-paired males, and CRF2s colocalize to OT neurons in the PVN and OT fibers projecting to the NAc [166,169].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [166]
The Results section, “Pairing with a Female Increased CRF mRNA in the mBNST” (page unavailable), reports higher CRF mRNA in males paired with a female than in males paired with a male sibling. The comparator was not an unpaired group, and our copy does not report CRF-R2 colocalization with oxytocin neurons in the PVN or oxytocin fibers projecting to the NAc. (LLM, conf=0.88)
Experimental — accuracy not yet measuredInfusions of OT to the NAc reduce passive stress-coping of separated male prairie voles.
“OT also plays a role in responses to partner loss, as infusions of OT to the NAc reduce passive stress-coping of separated males.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [166]
The Discussion reports increased passive stress-coping in male prairie voles after separation from a bonded female partner. But the Methods describe intracerebroventricular infusion of CRF-receptor antagonists, not oxytocin infusion into the nucleus accumbens; the copy does not support the claimed OT treatment or its effect. (LLM, conf=0.85)
Experimental — accuracy not yet measuredUpon separation from a pair-bonded partner, male and female prairie voles display depressive- and anxiety-like phenotypes, increased sensitivity to pain, and physiological changes, including elevated heart rate and increased circulating levels of corticosterone and adrenocorticotropic hormone.
“Upon separation from a pair-bonded partner, male and female prairie voles display depressive- and anxiety-like phenotypes, increased sensitivity to pain, and physiological changes, including elevated heart rate and increased circulating levels of corticosterone and adrenocorticotropic hormone [165,166,167] (Figure 2f).”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [166]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredHeightened HPA activity, shown by increased circulating corticosterone and ACTH, occurs after 1-5 days of isolation in juvenile or pair-bonded adult prairie voles.
“Heightened HPA axis activity (evidenced by a robust increase in circulating corticosterone and ACTH) is observed after 1–5 days of social isolation in juvenile (3–5 weeks old)68,69 or pair-bonded adult70–72 prairie voles.”
From Neural mechanisms of social homeostasis (2019) · cites this paper as [70]
CRF release during separation from a partner creates an aversive stressful state that motivates the prairie vole to return to the partner, maintaining the pair bond.
“Furthermore, it may be that CRF release during separation from the partner creates an aversive, stressful state that motivates the prairie vole to return to the partner, which in turn maintains the pair bond (Bosch et al 2009).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Bosch et al 2009
Four days of separation from a pair-bonded mate leads to increases in passive coping strategies in male prairie voles, and this does not occur after separation from a male sibling.
“Of more direct relevance is the finding that 4 days of separation from a pair-bonded mate leads to increases in passive coping strategies, a type of depressive-like behavior, in male prairie voles, and that this increase does not occur in response to separation from a male sibling (Bosch et al 2009).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Bosch et al 2009
Disruption of an established pair bond leads to high levels of passive behavior (immobility) in the tail suspension test in prairie voles.
“Disruption of an established pair bond leads to high levels of passive behavior (immobility) in the forced swim test and the tail suspension tests, a behavioral response reminiscent of grieving and bereavement in humans.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [44]
Disruption of an established pair bond leads to high levels of passive behavior (immobility) in the forced swim test in prairie voles.
“Disruption of an established pair bond leads to high levels of passive behavior (immobility) in the forced swim test and the tail suspension tests, a behavioral response reminiscent of grieving and bereavement in humans.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [44]
When prairie voles are chronically isolated or separated from their pair bonded partner, they display behaviors similar to those found in depression.
“When prairie voles are chronically isolated, or separated from their pair bonded partner, they display behaviors similar to those found in depression.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [44]
In separated males, chronic central infusion of CRF-R1 antagonist or CRF-R2 antagonist over 4 days normalizes passive stress-coping behavior.
“In separated males, chronic central infusion of the antagonist for CRF-R1 (CP-154526) or for CRF-R2 (astressin-2B) over 4 days normalizes passive stress-coping behavior”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
The depressive-like state after breaking the pair bond is accompanied by decreased parasympathetic and increased sympathetic drive to the heart, increased heart rate, adrenal hypertrophy, and higher basal plasma corticosterone concentration.
“The depressive-like state after breaking the pair bond is accompanied by decreased parasympathetic and increased sympathetic drive to the heart in conjunction with increased heart rate (McNeal et al. 2014), adrenal hypertrophy (Bosch et al. 2009), and higher basal plasma corticosterone concentration”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
Anxiety-related behavior is increased in separated male prairie voles for up to 4 weeks even in males separated from their siblings.
“Anxiety-related behavior is increased in separated males for up to 4 weeks (Bosch et al. 2009; McNeal et al. 2014; Sun et al. 2014) even in males separated from their siblings (Bosch et al. 2009)”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
Losing the female partner is chronic stress in male prairie voles.
“indicating that losing the female partner is chronic stress”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
Increased CRF signaling is not necessary to maintain a pair bond.
“increased CRF signaling is not necessary to maintain a pair bond”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
Only male prairie voles separated from female, but not from male, siblings show heightened levels of passive stress-coping behavior after short- and long-term separation.
“Interestingly, only males separated from female, but not from male, siblings show heightened levels of passive stress-coping behavior after short- (3–5 days; Fig. 2a, b) and long-term (4 weeks) separation”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
The negative emotional state during short separation encourages reunion with the partner and may have evolved to maintain long-term partnerships.
“Hence, this negative emotional state during short separation, i.e., 5 days, encourages reunion with the partner and may have evolved to maintain long-term partnerships”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Bosch et al. 2009
In highly social species, decreases in oxytocin signaling due to partner loss rapidly translate into stress-related disorders such as anxiety and depression.
“Furthermore, even short-term separation from their female partners induced profound grief reactions and heightened hypothalamic-pituitary-adrenal axis activity in male voles (27), suggesting that in highly social species, decreases in OXT signaling due to partner loss rapidly translate into stressrelated disorders such as anxiety and depression.”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [27]
Short-term separation from their female partners induced profound grief reactions and heightened hypothalamic-pituitary-adrenal axis activity in male voles.
“Furthermore, even short-term separation from their female partners induced profound grief reactions and heightened hypothalamic-pituitary-adrenal axis activity in male voles (27), suggesting that in highly social species, decreases in OXT signaling due to partner loss rapidly translate into stressrelated disorders such as anxiety and depression.”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [27]
In animal models, loss of a female partner (and not a sibling) is a stressful event that leads to increased cortisol and increased passive stress coping reminiscent of depression or bereavement.
“In animal models, the loss of a female partner (and not a sibling) is a stressful event that leads to increased levels of cortisol and increased passive stress coping reminiscent of depression or bereavement (Bosch et al. 2009).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Bosch et al. 2009
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“…of those bonds increases susceptibility to diseases (House et al, 1990; Kirschbaum et al, 1995; Uchino et al, 1996; Capitanio et al, 1998; for review see Biondi and Picardi, 1996; DeVries et al, 2003), including depression (Zisook et al, 1997; Watanabe et al, 2004; Grippo et al, 2007a, b).”
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The oxytocin receptor: from intracellular signaling to behavior
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Self-citationNeural mechanisms of social homeostasis
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κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance
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“Finally, since our data indicate that -opioid receptors within the NAc shell mediate selective aggression through modulation of aversive social motivation, and aversive stimuli are known to increase corticosterone signaling, we determined whether blockade of -opioid receptors alters selective aggression indirectly tho…”
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The neurobiological reward system in Prolonged Grief Disorder (PGD): A systematic review
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The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
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Self-citationSeparation from a bonded partner alters neural response to inflammatory pain in monogamous rodents
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Self-citation
- Authors
- Bosch, O. J., Nair, H. P., Ahern, T. H., Neumann, I. D., & Young, L. J.
- Affiliations
- University of Regensburg (DE)
- Emory University (US)
- Corresponding author
- Bosch, Oliver J
- Venue
- Neuropsychopharmacology
- Published
- 2008-10-15
- Volume
- 34
- Issue
- 6
- Pages
- 1406-1415
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC2669698
- OpenAlex
- W2035202887
- Cited by
- 216
- References
- 88
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 7 · 2023: 8 · 2022: 11 · 2021: 21 · 2020: 11 · 2019: 9 · 2018: 18 · 2017: 17 · 2016: 12 · 2015: 12 · 2014: 14 · 2013: 12 · 2012: 14
- FWCI
- 15.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- University of Regensburg Publication Server (University of Regensburg) (acceptedVersion)
- Funders
- National Science Foundation
- Deutscher Akademischer Austauschdienst
- Volkswagen Foundation
- Universität Regensburg
- U.S. Public Health Service (NCRR RR-00165)
- National Institute of Mental Health (K02MH064692, MH077776, MH064692, R01MH077776)
- National Center for Research Resources (RR-00 165, P51RR000165)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- corticotropin-releasing factor, CRF1 receptor, CRF receptor 2, loss of a partner, pair bonding, Microtus ochrogaster, depression-like behavior, anxiety-like behavior, bed nucleus of the stria terminalis, corticosteroids, adrenal weight, social separation, proximity seeking
- MeSH terms
- Adaptation, Psychological, Adrenal Cortex Hormones, Adrenal Glands, Adrenocorticotropic Hormone, Animals, Anxiety, Corticotropin-Releasing Hormone, Arvicolinae, Depression, Female, Male, Organ Size, Pair Bond, RNA, Messenger, Septal Nuclei, Stress, Psychological, Receptors, Corticotropin-Releasing Hormone
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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