Cited by 54Neuroendocrine regulation and behaviorNeurogenesis and neuroplasticity mechanismsTactile and Sensory Interactions

Neuromodulation of maternal circuits by oxytocin

Open access
Valtcheva, Silvana, Froemke, Robert C.·2019·Cell and Tissue Research

Abstract

Motherhood in mammals involves tremendous changes throughout the body and central nervous system, which support attention and nurturing of infants. Maternal care consists of complex behaviors, such as nursing and protection of the offspring, requiring new mothers to become highly sensitive to infant needs. Long-lasting neural plasticity in various regions of the cerebral cortex may enable the perception and recognition of infant cues, important for appropriate caregiving responses. Recent findings have demonstrated that the neuropeptide oxytocin is involved in a number of physiological processes, including parturition and lactation and dynamically shaping neuronal responses to infant stimuli as well. Here, we review experience-dependent changes within the cortex occurring throughout motherhood, focusing on plasticity of the somatosensory and auditory cortex. We outline the role of oxytocin in gating cortical plasticity and discuss potential mechanisms regulating oxytocin release in response to different sensory stimuli.

AI snapshot

Written from the paper’s full text.

TL;DR

This review synthesizes evidence that motherhood drives experience-dependent plasticity in somatosensory (S1) and auditory (A1) cortex, and argues that the neuropeptide oxytocin acts as a neuromodulator gating these cortical changes to heighten sensitivity to infant cues. It contrasts the transient, nursing-dependent plasticity of S1 with the longer-lasting changes in A1, and proposes that distinct firing patterns of hypothalamic oxytocin neurons may drive peripheral versus central oxytocin release.

Key findings

  • In primiparous lactating rats, the S1 representation of the ventrum expands roughly two-fold (nipple/areolae area), an effect absent in postpartum rats whose litters were removed at birth, implying active nursing rather than parturition alone drives the map change (Rosselet et al., 2006; Xerri et al., 1994).
  • S1 receptive fields for nipple-bearing skin shrink at one week after nursing onset, return to baseline by three weeks, while map extension appears later (two weeks) and persists until weaning; increased dendritic spine density in layer III/V pyramidal neurons remains up to six weeks after weaning (Chen et al., 2017).
  • In A1, pup distress calls are overrepresented in dams versus virgins, with more pup call-responding neurons, a shifted excitation/inhibition balance, and enhanced responses in ultrasound-responding regions; unlike S1, these auditory changes can persist up to several weeks after weaning, though one study reports single-cell responses disappearing at 10 days post-weaning (Tasaka et al., 2018).
  • Oxytocin neurons in PVN/SON fire in bursts of 50–100 Hz lasting 1–2 s every 5–10 min during parturition and suckling, but optogenetic studies show lower continuous frequencies (30 Hz; or 5 Hz for 3 min) suffice to trigger central oxytocin release and effects such as reduced inhibitory transmission and increased cortical spiking.

Methods

  • Narrative review of the literature on maternal cortical plasticity and oxytocin, focused on somatosensory and auditory cortex; the abstract states it reviews experience-dependent cortical changes across motherhood and discusses mechanisms regulating oxytocin release.
  • Synthesizes predominantly rodent (rat and mouse) studies using in vivo recording, imaging, tracing, and optogenetic manipulation, with some human studies on maternal cry reactivity and oxytocin receptor genetics.
  • No primary data are collected or analyzed; the paper integrates cited findings and proposes conceptual models (e.g., contrasting bursting versus tonic oxytocin neuron firing).

Limitations

  • Stated by the paper: it remains unknown whether oxytocin is important for the onset or maintenance of S1 plasticity; which inputs to PVN oxytocin neurons convey infant-cue information and what firing patterns are sufficient for central release remain unexplored; whether oxytocin is released centrally during the postpartum plasma spike is unknown; and the behavioral/evolutionary advantage of long-lasting auditory changes is unexplored.
  • Evident from the text: as a narrative review it presents no new data, and its conclusions rest on synthesis of others' work, much of it in rodents, with the human evidence largely correlational (e.g., oxytocin receptor gene associations, breastfeeding and cry-response studies).
  • The paper also notes unresolved debate about the exact nature of cortical oxytocin innervation, since one study found no direct PVN-to-sensory-cortex projections while others demonstrated PVN fibers in A1.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1007/s00441-018-2883-1

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 70 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    The emergence of different aspects of maternal behavior relies on experience-dependent changes within the maternal brain that enable the processing of sensory cues from the newborn.

    “the emergence of different aspects of maternal behavior relies on experience-dependent changes within the maternal brain that enable the processing of sensory cues from the newborn”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Bridges, 2015 source

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    • cites Kim et al., 2016 source

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    • cites Kohl and Dulac, 2018 source

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  • Premisenone given

    Oxytocin dynamically shapes neuronal responses to infant stimuli.

    “dynamically shaping neuronal responses to infant stimuli as well”
    Quote in the paperSubstantial claim
  • Premisenone given

    Oxytocin gates cortical plasticity.

    “We outline the role of oxytocin in gating cortical plasticity”
    Quote in the paperNot a substantial claim
  • Premisecitation

    Long-lasting plasticity in somatosensory and auditory cortex contributes to increased responsiveness to infant cues.

    “long-lasting plasticity in somatosensory (Rosselet et al., 2006; Xerri et al., 1994) and auditory (Cohen et al., 2011; Cohen and Mizrahi, 2015; Liu et al., 2006; Liu and Schreiner, 2007; Marlin et al., 2015; Shepard et al., 2016; Tasaka et al., 2018) cortex have recently been shown to contribute to increased responsiveness to infant cues”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Rosselet et al., 2006 source

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    • cites Xerri et al., 1994 source

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    • cites Cohen et al., 2011 source

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  • Premisecitation

    The overall tonotopic organization of A1 is not modified by motherhood compared to the S1 representational territory of the ventrum.

    “the overall tonotopic organization of A1 is not modified by motherhood compared to S1 representational territory of the ventrum”
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    • cites Rosselet et al., 2006 source

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    • cites Shepard et al., 2016

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  • May combine two claims. 8
  • Classified as probably not a substantial claim. 8
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    Premisecitation

    New mothers undergo dramatic endocrinological and physiological changes supporting the establishment and maintenance of maternal caregiving, including changes throughout the central nervous system.

    “New mothers themselves undergo dramatic endocrinological and physiological changes supporting the establishment and maintenance of maternal caregiving, including changes throughout the central nervous system”
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    • cites Bornstein et al., 2017 source

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    • cites Bridges, 2016 source

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    • cites Kim et al., 2016 source

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    Premisenone given

    Oxytocin is involved in physiological processes including parturition and lactation.

    “the neuropeptide oxytocin is involved in a number of physiological processes, including parturition and lactation”
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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Healthy maternal sensitivity is characterized by the ability to reliably recognize and respond to infant cues, thus initiating appropriate caregiving responses.

    “Healthy maternal sensitivity is characterized by the ability to reliably recognize and respond to infant cues, thus initiating appropriate caregiving responses”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Dulac et al., 2014

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    • cites Insel and Young, 2001 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    Early mother-infant relationships have long-term effects on the cognitive, behavioral, and emotional development of offspring.

    “Early mother-infant relationships have long-term effects on the cognitive, behavioral, and emotional development of offspring.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Maternal care is critical for child survival and health.

    “Maternal care is critical for child survival and health (Rilling and Young, 2014).”
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    • cites Rilling and Young, 2014 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Direct somatic contact with the offspring mainly initiates a nursing response, while other sensory stimuli like cries or odors contribute essentially to arousal and orientation.

    “direct somatic contact with the offspring mainly initiates a nursing response, while other sensory stimuli like cries or odors contribute essentially to arousal and orientation”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Bridges, 2016 source

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    • cites Swain et al., 2011 source

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    Premisecitation

    Oxytocin is responsible for various prosocial functions in mammals such as parental care, pair bonding and empathy.

    “Oxytocin is responsible for various prosocial functions in mammals such as parental care, pair bonding and empathy”
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    • cites Feldman, 2016 source

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    • cites Fineberg and Ross, 2017 source

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    • cites Insel and Young, 2001 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Oxytocin is synthesized in the paraventricular nucleus and supraoptic nucleus of the hypothalamus and exerts its central actions via the oxytocin receptor.

    “Oxytocin is synthesized in the paraventricular nucleus (PVN) and the supraoptic nucleus (SON) of the hypothalamus (Grinevich, 2017; Ludwig and Leng, 2006) and exerts its central actions via the oxytocin receptor (Ludwig and Leng, 2006).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
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    • cites Ludwig and Leng, 2006 source

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  • May combine two claims.

    Premisecitation

    Pup distress calls are overrepresented in dams compared to virgins, leading to a stronger activation of the deep layers and increased noise correlation in layer II/III of auditory cortex in lactating females.

    “Pup distress calls are overrepresented in dams compared to virgins, leading to a stronger activation of the deep layers and increased noise correlation in layer II/III of auditory cortex in lactating females”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Cohen et al., 2011 source

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    • cites Rothschild et al., 2013 source

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  • May combine two claims.

    Premisecitation

    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”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Cohen et al., 2011 source

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    • cites Marlin et al., 2015 source

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  • May combine two claims.

    Premisecitation

    Map extension appears much later, at two weeks after nursing onset, but is maintained until weaning.

    “map extension appears much later (at two weeks after nursing onset) but it is maintained until weaning”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Rosselet et al., 2006 source

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  • May combine two claims.

    Premisecitation

    Optogenetic oxytocin release from axons can be induced at much lower stimulation frequency (5 Hz for 3 min) in A1, piriform cortex, and PVN ex vivo, resulting in decreased inhibitory transmission and increased spiking output.

    “optogenetic oxytocin release from axons can be induced at much lower stimulation frequency at increased duration of 5 Hz during 3 min in different brain structures ex vivo as A1, piriform cortex, and PVN itself, resulting in a decrease of inhibitory transmission and increased spiking output (Mitre et al., 2016).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mitre et al., 2016 source

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    Interpretationnone given

    In the case of maternal behavior, oxytocin is a main candidate for hormonal regulation and neural circuit modulation relevant for parenting.

    “In the case of maternal behavior, oxytocin is a main candidate for hormonal regulation and neural circuit modulation relevant for parenting.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    The sound of a baby cry activates the hypothalamus and triggers oxytocin plasma elevations in human mothers.

    “the sound of a baby cry activates the hypothalamus (Lorberbaum et al., 2002) and triggers oxytocin plasma elevations in human mothers (McNeilly et al., 1983)”
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    • cites McNeilly et al., 1983 source

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  • The paper relies on this without support.

    Optogenetic stimulation patterns in ex vivo brain structures reflect the physiological firing patterns that trigger oxytocin release in central areas in vivo.

    “Although optogenetic stimulation might produce artificially-synchronous activity across oxytocin neurons or oxytocin axons, these data suggest that oxytocin release in central areas may be triggered by patterns of firing which differ from the well-known bursting activity important for parturition and lactation.”
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Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Oxytocin is well known for its influence on social bonding and maternal behavior, and its role in parental behavior highlights the putative function of oxytocin as an attentional modulator.

    “OXT is well known for its influence on social bonding and maternal behavior (9,18), and its role in parental behavior highlights the putative function of OXT as an attentional modulator (122).”
  • Oxytocin is important for maternal physiology and childcare, including parturition and milk ejection during nursing.

    “Oxytocin is a neuropeptide that is important for maternal physiology and childcare, including parturition and milk ejection during nursing1–6.”
  • Suckling triggers the release of oxytocin.

    “Suckling triggers the release of oxytocin, but other sensory cues—specifically, infant cries—can increase the levels of oxytocin in new human mothers7”
  • PVN oxytocin cells receive projections from many areas of the brain.

    “PVN oxytocin cells receive projections from many areas of the brain”
  • Oxytocin is produced mainly in the paraventricular nucleus and supraoptic nucleus of the hypothalamus.

    “oxytocin, a nine-amino-acid peptide that is produced mainly in the paraventricular nucleus (PVN) and supraoptic nucleus of the hypothalamus1–4”

The citation lists haven’t been fetched yet

References 146 · Cited by 54

Research works printed but not linked: 1

  1. Blass EM, Teicher MH (1980) Suckling. Science 210(4465):15–22. https://www.ncbi.nlm.nih.gov/pubmed/6997992 . Accessed 11 May 2018

Authors
Valtcheva, S., & Froemke, R. C.
Affiliations
  • NYU Langone Health (US)
  • Howard Hughes Medical Institute (US)
Corresponding author
Froemke, Robert C.
Venue
Cell and Tissue Research
Published
2018-07-30
Volume
375
Issue
1
Pages
57-68
ISSN
  • 0302-766X (ISSN-L)
  • 1432-0878
OpenAlex
W2887650927
Cited by
54
References
146
Citations by year
2026: 2 · 2025: 3 · 2024: 12 · 2023: 6 · 2022: 6 · 2021: 12 · 2020: 8 · 2019: 4 · 2018: 1
FWCI
0.94
Type
journal article
Language
en
Open access
Locations
  • Cell and Tissue Research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Leon Levy Foundation
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD088411)
  • Howard Hughes Medical Institute
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords
oxytocin, maternal behavior, neuroplasticity, somatosensory cortex, auditory cortex, infant cues, experience-dependent plasticity, oxytocin release, childbirth, lactation, maternal care
MeSH terms
Animals, Nerve Net, Neuronal Plasticity, Oxytocin, Somatosensory Cortex, Signal Transduction, Neurotransmitter Agents

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