Oxytocin enables maternal behaviour by balancing cortical inhibition
Open accessAbstract
Oxytocin is important for social interactions and maternal behaviour. However, little is known about when, where and how oxytocin modulates neural circuits to improve social cognition. Here we show how oxytocin enables pup retrieval behaviour in female mice by enhancing auditory cortical pup call responses. Retrieval behaviour required the left but not right auditory cortex, was accelerated by oxytocin in the left auditory cortex, and oxytocin receptors were preferentially expressed in the left auditory cortex. Neural responses to pup calls were lateralized, with co-tuned and temporally precise excitatory and inhibitory responses in the left cortex of maternal but not pup-naive adults. Finally, pairing calls with oxytocin enhanced responses by balancing the magnitude and timing of inhibition with excitation. Our results describe fundamental synaptic mechanisms by which oxytocin increases the salience of acoustic social stimuli. Furthermore, oxytocin-induced plasticity provides a biological basis for lateralization of auditory cortical processing.
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Cortical oxytocin receptors are found primarily on parvalbumin-positive or somatostatin-positive inhibitory interneurons, including at inhibitory synaptic terminals.
“Cortical oxytocin receptors are found primarily on parvalbumin-positive or somatostatin-positive inhibitory interneurons”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Marlin et al. 2015
The “Oxytocin Receptor Expression Is Lateralized” section reports that about 30–40% of PV-positive and SST-positive inhibitory interneurons in mouse auditory cortex expressed oxytocin receptors. That supports receptor expression in these cell types, but does not establish that cortical receptors are found primarily on them. The passages also do not establish receptor localization at inhibitory synaptic terminals. (LLM, conf=0.88)
Experimental — accuracy not yet measuredOxytocin modulation acts as a social salience signal to almost immediately boost neural responses, which are then consolidated via mechanisms of long-term plasticity so that auditory cortex remains responsive to pup calls perhaps for the lifetime of the animal.
“In this way, oxytocin modulation acts as a social salience signal to almost immediately boost neural responses, which are then consolidated via mechanisms of long-term plasticity (Marlin et al. 2015) so that auditory cortex remains responsive to pup calls perhaps for the lifetime of the animal.”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Marlin et al. 2015
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredOnce plasticity has occurred, blocking cortical oxytocin receptors did not substantially affect pup retrieval abilities.
“Once plasticity has occurred, blocking cortical oxytocin receptors did not substantially affect pup retrieval abilities”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Marlin et al. 2015
Pup retrieval in mice is enabled by increased attention to pup vocalizations as a consequence of oxytocin-dependent alterations in the excitatory-inhibitory balance within the auditory cortex.
“For instance, pup retrieval in mice is enabled by increased attention to pup vocalizations as a consequence of OT-dependent alterations in the excitatory-inhibitory balance within the auditory cortex.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [27]
Oxytocin further enables the process by which cohousing accelerates the onset of maternal behavior.
“and oxytocin further enables this process”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Marlin et al. 2015
Oxytocin receptor signalling tunes the auditory cortex to respond maximally to pup vocalisations, facilitating maternal responsiveness.
“Furthermore, an elegant study using a multidisciplinary approach demonstrated that OXTR signalling tunes the auditory cortex to maximally respond to pup vocalisations, which facilitates maternal responsiveness (26).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [26]
Oxytocin from the paraventricular nucleus increases the salience of mouse pup vocalizations, while a dam's experience with pups adjusts the balance of excitatory and inhibitory tuning in the auditory cortex.
“For example, OXT from PVN increases the salience of mouse pup vocalizations, while a dam's experience with pups adjusts the balance of excitatory and inhibitory tuning in the auditory cortex (54,123,124).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [123]
Oxytocin enables pup retrieval behavior in female mice by amplifying pup call responses in maternal auditory cortex.
“Recently, it was shown that OXT enables pup retrieval behavior in female mice by amplifying pup call responses in maternal auditory cortex (21).”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [21]
Neural representations of pup vocalizations in the auditory cortex undergo experience-dependent plasticity with the transition to motherhood, thus enhancing auditory responses to pup calls.
“Neural representations of pup vocalizations in the auditory cortex also undergo experience-dependent plasticity with the transition to motherhood (Fig. 1B-D), thus enhancing auditory responses to pup calls”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
Pup distress calls reliably drive individual neurons in mouse primary auditory cortex in a temporally precise manner.
“pup distress calls reliably drive individual neurons in mouse primary auditory cortex (A1) in a temporally precise manner”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
Oxytocin can selectively gate cortical responses to infant stimuli to subsequently enable maternal care.
“The neuropeptide oxytocin can selectively gate cortical responses to infant stimuli to subsequently enable maternal care”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
Oxytocin is involved in homeostatic regulation of reflexes such as parturition and lactation.
“Oxytocin is involved not only in homeostatic regulation of reflexes such as parturition and lactation, but it is crucial part of other aspects of motherhood such as care and protection of the offspring (Marlin et al., 2015; Nakajima et al., 2014; Sabihi et al., 2014).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
Oxytocin gates the representation of infant vocalizations in A1.
“Oxytocin gates the representation of infant vocalizations in A1 (Marlin et al., 2015) but it remains unknown whether it is also important for the onset and/or maintenance of plasticity in S1 (Rosselet et al., 2006; Xerri et al., 1994).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
Oxytocin is crucial for other aspects of motherhood such as care and protection of the offspring.
“Oxytocin is involved not only in homeostatic regulation of reflexes such as parturition and lactation, but it is crucial part of other aspects of motherhood such as care and protection of the offspring (Marlin et al., 2015; Nakajima et al., 2014; Sabihi et al., 2014).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
Oxytocin decreases the pup retrieval onset in cohoused virgins.
“decreases the pup retrieval onset in cohoused virgins (Marlin et al., 2015).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Marlin et al., 2015
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 [15]
In mice, oxytocin enables neuroplasticity in the auditory cortex for maternal recognition of pup distress.
“In mice, oxytocin enables neuroplasticity in the auditory cortex for maternal recognition of pup distress15.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [15]
Pup-naive virgin female mice initially ignore neonates and ultrasonic distress calls emitted by isolated pups.
“Pup-naive virgin female mice initially ignore neonates and ultrasonic distress calls emitted by isolated pups15.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [15]
One important neural adaptation with motherhood occurs in the left auditory cortex, which is modulated by oxytocin to amplify responses to pup distress calls to promote retrieval.
“One important neural adaptation with motherhood occurs in the left auditory cortex, which is modulated by oxytocin to amplify responses to pup distress calls to promote retrieval15,21.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [15]
Oxytocin enhances the auditory cortex response to pup calls to promote maternal nurturing.
“Likewise, oxytocin enhances the auditory cortex response to pup calls to promote maternal nurturing [17].”
From Translational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry (2021) · cites this paper as [17]
OXT is released within the brain as relationships form and facilitates experience-dependent social adaptations including formation of social memories, establishment of mating-induced pair bonds, and maternal responsiveness.
“OXT is released within the brain as relationships form and it facilitates experience-dependent social adaptations including the formation of social memories 14,15, the establishment of mating-induced pair bonds 2 and maternal responsiveness 16.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [16]
OT enhances responses to pup calls by balancing magnitude and timing of inhibition with excitation within the left auditory cortex.
“OT enhances responses to pup calls by balancing the magnitude and the timing of inhibition with excitation within the left auditory cortex (Marlin et al. 2015).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Marlin et al. 2015
OT regulates neuronal activities in multiple neural circuits, such as sensory cortices, nucleus accumbens, and prefrontal cortex.
“OT regulates neuronal activities in multiple neural circuits, such as sensory cortices (Marlin et al., 2015), nucleus accumbens (Dölen et al., 2013), and prefrontal cortex (Nakajima et al., 2014).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Marlin et al., 2015
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“…unusual hemispheric overrepresentation on the left side of auditory cortex paralleled by a left hemisphere advantage for behavioral responses to pup vocalizations as well as left-lateralized oxytocin receptor expression in female auditory cortex (Ehret 1987,Marlin et al. 2015, Schiavo et al. 2020).”
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A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors
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Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice
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“Furthermore, an elegant study using a multidisciplinary approach demonstrated that OXTR signalling tunes the auditory cortex to maximally respond to pup vocalisations, which facilitates maternal responsiveness (26).”
BackgroundOxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
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Oxytocin transforms firing mode of CA2 hippocampal neurons
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Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues
Yao, S., Bergan, J., Lanjuin, A., & Dulac, C. (2017) · eLife · doi:10.7554/elife.31373 · Cited by 151 · see citing works
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Interplay between Oxytocin and Sensory Systems in the Orchestration of Socio-Emotional Behaviors
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Extrahypothalamic oxytocin neurons drive stress-induced social vigilance and avoidance
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Diversity of oxytocin neurones: Beyond magno‐ and parvocellular cell types?
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Neural control of parental behaviors
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Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
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<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
Self-citationWhole-brain wiring diagram of oxytocin system in adult mice
Son, S., Manjila, S. B., Newmaster, K. T., Wu, Y.-T., Vanselow, D. J., Ciarletta, M., Anthony, T. E., Cheng, K. C., & Kim, Y. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.0307-22.2022 · Cited by 125 · see citing works
Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation
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Oxytocin mediates entrainment of sensory stimuli to social cues of opposing valence
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Innate and plastic mechanisms for maternal behaviour in auditory cortex
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Self-citationNeural circuitry for maternal oxytocin release induced by infant cries
Valtcheva, S., Issa, H. A., Bair-Marshall, C. J., Martin, K. A., Jung, K., Zhang, Y., Kwon, H.-B., & Froemke, R. C. (2023) · Nature · doi:10.1038/s41586-023-06540-4 · Cited by 115 · see citing works
Self-citationSteinman, M. Q., Duque-Wilckens, N., & Trainor, B. C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.10.008 · Cited by 105 · see citing works
Intranasal oxytocin, but not vasopressin, augments neural responses to toddlers in human fathers
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Less can be more: Fine tuning the maternal brain
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Oxytocin functions as a spatiotemporal filter for excitatory synaptic inputs to VTA dopamine neurons
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“Oxytocin is one of the two major neurohypophyseal peptides that function centrally as a neuromodulator and has been linked to the processing of socially rewarding stimuli via actions in the stria- tum and in the neocortex (Choe et al., 2015; Dölen et al., 2013; Marlin et al., 2015).”
BackgroundMethodPup exposure facilitates retrieving behavior via the oxytocin neural system in female mice
Okabe, S., Tsuneoka, Y., Takahashi, A., Ooyama, R., Watarai, A., Maeda, S., Honda, Y., Nagasawa, M., Mogi, K., Nishimori, K., et al. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.01.036 · Cited by 82 · see citing works
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Oxytocin and the Pharmacological Dissection of Affiliation
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Thalamic integration of social stimuli regulating parental behavior and the oxytocin system
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A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats
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The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
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“OT thereby influences the signal-to-noise ratio of stimuli to increase the saliency of pup calls [27].”
BackgroundNeural functions of hypothalamic oxytocin and its regulation
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Neuromodulation of maternal circuits by oxytocin
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Self-citationCircuits for social learning: a unified model and application to autism spectrum disorder
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Selective localization of oxytocin receptors and vasopressin 1a receptors in the human brainstem
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“OXT/OXTR signaling acts as a neuromodulator affecting social and sexual behavior, stress coping, and the processing of social stimuli, in many species (Knobloch et al., 2012; Dolen et al., 2013; Choe et al., 2015; Marlin et al., 2015; Wei et al., 2015; Oettl et al., 2016; Yokoi et al., 2020).”
BackgroundTranslational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry
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Paraventricular nucleus oxytocin subsystems promote active paternal behaviors in mandarin voles
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An integrated framework for the role of oxytocin in multistage social decision‐making
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“balance in the auditory cortex of rodents during pup calls (Marlin et al., 2015).”
BackgroundMethodInfluentialSocial experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles
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A precision medicine approach to oxytocin trials
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Recording and manipulation of the maternal oxytocin neural activities in mice
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Oxytocin, vasopressin and social behavior in the age of genome editing: a comparative perspective
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Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research
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Oxytocin increases eye gaze in schizophrenia
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Neuroendocrine mechanisms of social bonds and separation stress in rodents, dogs, and other species
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Context-dependent activation of a social behavior brain network during learned vocal production
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- Authors
- Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C.
- Affiliations
- NYU Langone Health (US)
- New York University (US)
- Corresponding author
- Froemke, Robert C.
- Venue
- Nature
- Published
- 2015-04-15
- Volume
- 520
- Issue
- 7548
- Pages
- 499-504
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4409554
- OpenAlex
- W2152504800
- Cited by
- 744
- References
- 56
- Citations by year
- 2026: 53 · 2025: 69 · 2024: 58 · 2023: 72 · 2022: 75 · 2021: 81 · 2020: 80 · 2019: 51 · 2018: 62 · 2017: 68 · 2016: 46 · 2015: 29
- FWCI
- 112.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Mental Health (T32MH019524)
- National Cancer Institute (P30CA016087)
- National Institute on Deafness and Other Communication Disorders (K99DC009635, DC12557, DC009635, R00DC009635, R01DC012557)
- National Institute of Neurological Disorders and Stroke (R56NS021072, T32NS086750)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- oxytocin, maternal behavior, pup retrieval, auditory cortex, cortical inhibition, hemispheric lateralization, pup calls, social cognition, synaptic plasticity, excitation-inhibition balance, oxytocin receptor, mice
- MeSH terms
- Acoustic Stimulation, Animals, Animals, Newborn, Auditory Cortex, Auditory Perception, Evoked Potentials, Auditory, Female, Male, Maternal Behavior, Mice, Inbred C57BL, Neural Inhibition, Neuronal Plasticity, Oxytocin, Sexual Abstinence, Vocalization, Animal, Receptors, Oxytocin, Mice
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