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Neural circuitry for maternal oxytocin release induced by infant cries
Open accessPublished version of a preprint
Abstract
Oxytocin is a neuropeptide that is important for maternal physiology and childcare, including parturition and milk ejection during nursing 1-6. Suckling triggers the release of oxytocin, but other sensory cues-specifically, infant cries-can increase the levels of oxytocin in new human mothers 7, which indicates that cries can activate hypothalamic oxytocin neurons. Here we describe a neural circuit that routes auditory information about infant vocalizations to mouse oxytocin neurons. We performed in vivo electrophysiological recordings and photometry from identified oxytocin neurons in awake maternal mice that were presented with pup calls. We found that oxytocin neurons responded to pup vocalizations, but not to pure tones, through input from the posterior intralaminar thalamus, and that repetitive thalamic stimulation induced lasting disinhibition of oxytocin neurons. This circuit gates central oxytocin release and maternal behaviour in response to calls, providing a mechanism for the integration of sensory cues from the offspring in maternal endocrine networks to ensure modulation of brain state for efficient parenting.
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TL;DR
This study identifies a noncanonical auditory circuit from the posterior intralaminar thalamus (PIL) to hypothalamic oxytocin neurons that relays infant pup calls and gates central oxytocin release and maternal behavior. In maternal mice, pup calls—but not pure tones—produce delayed, persistent activation of PVN oxytocin neurons via NMDAR- and dynamin-dependent long-term depression of inhibition.
Key findings
- Pup-call presentation increased firing of identified PVN oxytocin neurons (ChR2+, OT+) from Pre 2.9 ± 0.7 Hz to Post 5.0 ± 1.6 Hz (P = 0.001, n = 11 cells from N = 6 dams), but not ChR2− (OT−) neurons (Pre 3.1 ± 0.9 Hz, Post 3.6 ± 1.0 Hz; P = 0.07, n = 11, N = 5). Fibre photometry in dams showed significant responses after calls (Pre versus Calls P = 0.0048; Pre versus Post P = 0.0179, N = 7 dams), significant as early as 25 s from call onset (P = 0.013); responses were specific to pup calls and absent for pure tones, adult calls, or FM down-sweeps, and were not observed in virgins.
- Rabies tracing showed the PIL contributed 100% of auditory inputs to PVN oxytocin cells versus 0% from the medial geniculate body, auditory cortex, and inferior colliculus. The PIL received synaptic inputs from both the inferior colliculus and auditory cortex, with a greater proportion from the inferior colliculus (P = 0.015, two-tailed Fisher’s test), and PIL-to-PVN oxytocin neuron connections occurred with high probability and preferentially targeted parvocellular oxytocin neurons.
- Repetitive optogenetic stimulation of PIL terminals in the PVN (30 Hz for 1 s, repeated every 2 s for 3 min) induced lasting disinhibition: IPSC amplitudes decreased and the IPSC/EPSC ratio decreased (P = 0.0018). This iLTD was blocked by AP5, intracellular MK801, and a dynamin inhibitory peptide, but not by MAP4 or the oxytocin receptor antagonist OTA; brief PIL stimulation did not trigger iLTD, and iLTD was occluded in slices from dams exposed to pup-call playback immediately before slice preparation.
- Saline-injected dams needed 41.6 ± 5.9 played calls to approach the speaker, whereas chemogenetic suppression of PIL-to-PVN input reduced speaker preference (P = 0.002) and decreased retrieval probability at later trials; blocking oxytocin signaling in the VTA also decreased retrieval probability (N = 4 dams, P at least <0.02). OXTR-iTango2 labelling in the VTA showed more tdTomato+EGFP+ cells after blue light + pup calls than after blue light + tones or blue light only, with fewer labelled cells when the PIL-to-PVN pathway was inhibited.
Methods
- Awake head-fixed maternal mice (dams 0–3 weeks postpartum, first or second birth, housed with pups P0–P21 or just weaned; virgins >6 weeks for some comparisons) underwent in vivo cell-attached/whole-cell recordings and fibre photometry from identified PVN oxytocin neurons during playback of pup distress calls, pure tones, adult calls, or FM sweeps.
- Circuit mapping used Cre-inducible retrograde rabies tracing, channelrhodopsin 2-assisted circuit mapping, in vitro whole-cell recordings in PVN/PIL slices, optogenetic stimulation of PIL terminals, and pharmacological blockers; behavior used chemogenetic inactivation of PIL-to-PVN neurons, VTA cannula infusion of an oxytocin receptor antagonist, and an OXTR-iTango2 oxytocin sensor in the VTA.
- Analyses used Wilcoxon matched-pairs signed-rank, Friedman, one-sample t-tests, Mann–Whitney, one-way ANOVA, Fisher’s exact, and binomial tests; sample sizes are reported in figure legends, with no statistical methods used to predetermine sample size and experiments not randomized.
Limitations
- Stated in the paper: no statistical methods were used to predetermine sample size; experiments were not randomized; blinding was not performed for in vivo cell-attached, whole-cell, and tungsten recordings, in vitro whole-cell recordings, and some real-time analyses, though investigators were blinded during behavioral testing and fibre photometry/oxytocin sensor data analysis.
- Evident from the text: all experiments are in mice, so the human relevance of infant cries increasing oxytocin is inferential; the paper cites human findings but does not test them directly.
- Evident from the text: several circuit and synaptic conclusions rely on viral tracing, optogenetic/chemogenetic manipulation, pharmacological blockade, and an engineered oxytocin sensor, and some experiments have small sample sizes (e.g., N = 2–7 dams in several photometry, tracing, and sensor experiments).
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In the paper
“This increase in the spiking of ChR2+ (OT+) neurons was not observed during call presentation itself”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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In the paper
“observed substantial responses after calls (Pre versus Calls: P = 0.0048; Pre versus Post: P = 0.0179, N = 7 dams”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
plaincorrelationaln = 7 ·- Asserted: passes — The authors put it forward as true.
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“We found that the PIL receives synaptic inputs from both the IC and the AuCx”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“and preferentially targeted parvocellular oxytocin neurons”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“This stimulation pattern also did not elicit suprathreshold spiking in oxytocin cells”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“We found that the PIL is activated by pup calls.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“this long-term depression of inhibition (iLTD) decreased the IPSC/EPSC ratio for oxytocin neurons”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“without affecting PIL transmission itself”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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In the paper
“We found that oxytocin neurons responded to pup vocalizations, but not to pure tones, through input from the posterior intralaminar thalamus”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“the amplitudes of IPSCs were significantly decreased after PIL opto”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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- It may state two separate claims as one. 30
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“We did not detect retrograde rabies infection and mCherry staining in the medial geniculate body of the thalamus (MGB; Fig. 2c), the auditory cortex (AuCx; Fig. 2d) or the inferior colliculus (IC; Fig. 2e).”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“these connections were too weak to trigger postsynaptic spiking responses”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“The sustained increase in oxytocin-neuron firing was specific to pup calls, as PVN neurons did not respond to pure tones, adult calls or frequency-modulated down-sweeps that retained key spectrotemporal characteristics of pup vocalizations”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“Optogenetic stimulation of PIL fibres activated NMDAR receptors on oxytocin neurons as it elicited outward oEPSCs, which were blocked by the NMDAR antagonist AP5 (P = 0.02; Fig. 3g).”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“iLTD and the change in the IPSC/EPSC ratio were blocked by infusing the postsynaptic oxytocin neuron with a membrane-impermeable dynamin inhibitory peptide (i-Dynamin inhibitor) through the recording pipette, but not by a scrambled dynamin inhibitor”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“these dams had a decreased probability of retrieving at later trials, without changes in the time to retrieval”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“both bath application of AP5 and intracellular delivery of the use-dependent NMDAR blocker MK801 (i-MK801) through a recording pipette abolished iLTD after PIL opto”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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“In dams, PVN oxytocin neurons showed delayed and long-lasting increases in firing after exposure to pup calls but not after exposure to pure tones”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
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“Multiple calls over several seconds were required to activate oxytocin cells through disinhibition and to induce dams to approach the speaker.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
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“Note increased firing rate for ChR2+ (OT+) neuron but not ChR2− (OT−) neuron.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Extended Data
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“Single pulse of optogenetic stimulation triggered postsynaptic potentials but did not induce spiking in oxytocin cells (n = 8 neurons).”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Extended Data
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“Prolonged but not brief optogenetic stimulation of PIL axons triggers iLTD.”
- Also stated in: § Extended Data · plain
“Repeated but brief optogenetic stimulation of PIL axons (‘PIL opto short’) did not induce iLTD: example cell (d; p = 0.74, Mann–Whitney two-tailed test) and summary (e; n = 6 neurons, p = 0.99, one-sample two-tailed Student’s t-test).”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Extended Data
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In the paper
“Suckling triggers the release of oxytocin, but other sensory cues—specifically, infant cries—can increase the levels of oxytocin in new human mothers7”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [1] Althammer, F. & Grinevich,. Diversity of oxytocin neurons: beyond magno- and parvocellular cell types?. J. Neuroendocrinol. 30, e12549 (2017). source
- Not checked yetcites [2] Jurek, B. & Neumann, I. D. The oxytocin receptor: from intracellular signaling to behavior. Physiol. Rev. 98, 1805–1908 (2018). source
- Not checked yetcites [3] Valtcheva, S. & Froemke, R. C. Neuromodulation of maternal circuits by oxytocin. Cell Tissue Res. 1, 57–68 (2019). source
- Not checked yetcites [4] Froemke, R. C. & Young, L. J. Oxytocin modulation and neural plasticity. Annu. Rev. Neurosci. 8, 359–381 (2021). source
- Not checked yetcites [5] Dulac, C., O’Connell, L. & Wu, Z. Neural control of maternal and paternal behaviors. Science 345, 1063–1069 (2014). source
- Not checked yetcites [6] Dölen, G. Oxytocin: parallel processing in the social brain? J. Neuroendocrinol. 27, 516–535 (2015). source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Oxytocin is a neuropeptide that is important for maternal physiology and childcare, including parturition and milk ejection during nursing1–6.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [1] Althammer, F. & Grinevich,. Diversity of oxytocin neurons: beyond magno- and parvocellular cell types?. J. Neuroendocrinol. 30, e12549 (2017). source
- Not checked yetcites [2] Jurek, B. & Neumann, I. D. The oxytocin receptor: from intracellular signaling to behavior. Physiol. Rev. 98, 1805–1908 (2018). source
- Not checked yetcites [3] Valtcheva, S. & Froemke, R. C. Neuromodulation of maternal circuits by oxytocin. Cell Tissue Res. 1, 57–68 (2019). source
- Not checked yetcites [4] Froemke, R. C. & Young, L. J. Oxytocin modulation and neural plasticity. Annu. Rev. Neurosci. 8, 359–381 (2021). source
- Not checked yetcites [5] Dulac, C., O’Connell, L. & Wu, Z. Neural control of maternal and paternal behaviors. Science 345, 1063–1069 (2014). source
- Not checked yetcites [6] Dölen, G. Oxytocin: parallel processing in the social brain? J. Neuroendocrinol. 27, 516–535 (2015). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This circuit gates central oxytocin release and maternal behaviour in response to calls, providing a mechanism for the integration of sensory cues from the offspring in maternal endocrine networks to ensure modulation of brain state for efficient parenting.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
plaindirect- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“oxytocin, a nine-amino-acid peptide that is produced mainly in the paraventricular nucleus (PVN) and supraoptic nucleus of the hypothalamus1–4”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [1] Althammer, F. & Grinevich,. Diversity of oxytocin neurons: beyond magno- and parvocellular cell types?. J. Neuroendocrinol. 30, e12549 (2017). source
- Not checked yetcites [2] Jurek, B. & Neumann, I. D. The oxytocin receptor: from intracellular signaling to behavior. Physiol. Rev. 98, 1805–1908 (2018). source
- Not checked yetcites [3] Valtcheva, S. & Froemke, R. C. Neuromodulation of maternal circuits by oxytocin. Cell Tissue Res. 1, 57–68 (2019). source
- Not checked yetcites [4] Froemke, R. C. & Young, L. J. Oxytocin modulation and neural plasticity. Annu. Rev. Neurosci. 8, 359–381 (2021). source
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“These findings are similar to those in other neurons in the paralaminar thalamus, which are more efficiently driven by inputs from the IC than those from the AuCx26.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [26] Smith, P. H. et al. Cortical and collicular inputs to cells in the rat paralaminar thalamic nuclei adjacent to the medial geniculate body. J. Neurophysiol. 98, 681–695 (2007). source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Peripheral oxytocin is important for milk ejection during nursing and uterine contractions during labour”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“Postpartum conditions might relate to lower levels of oxytocin and decreased sensitivity to infant cries9”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [9] Pawluski, J. L., Lonstein, J. S. & Fleming, A. S. The neurobiology of postpartum anxiety and depression. Trends Neurosci. 40, 106–120 (2017). source
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“In humans, baby cries are a powerful signal of infant distress, and most nursing mothers respond to cries with increased hypothalamic activity, rises in the levels of plasma oxytocin, comforting behaviours towards the infant and occasional milk ejection7,8.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [7] McNeilly, A. S., Robinson, I. C., Houston, M. J. & Howie, P. W. Release of oxytocin and prolactin in response to suckling. Br. Med. J. 286, 257–259 (1983). source
- Not checked yetcites [8] Bornstein, M. H. et al. Neurobiology of culturally common maternal responses to infant cry. Proc. Natl Acad. Sci. USA 114, E9465–E9473 (2017). source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“and has also been implicated in maternal and social behaviours22–24.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [22] Dobolyi, A., Cservenák, M. & Young, L. J. Thalamic integration of social stimuli regulating parental behavior and the oxytocin system. Front. Neuroendocrinol. 51, 102–115 (2018). source
- Not checked yetcites [23] Keller, D. et al. A thalamo-preoptic pathway promotes social grooming in rodents. Curr. Biol. 32, 4593–4606 (2022). source
- Not checked yetcites [24] Leithead, A. B., Godino, A., Barbier, M. & Harony-Nicolas, H. Social interaction elicits activity in glutamatergic neurons in the posterior intralaminar complex of the thalamus. Biol. Psychiatry https://doi.org/10.1016/j.biopsych.2023.05.016 (2023). source
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
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In the paper
“whereas oxytocin release in the central nervous system is involved in a wide range of behaviours including reproduction, parental care and pair bonding5,6.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“The PIL is part of the nonlemniscal auditory pathway that projects to the PVN13,21,22”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [13] Tang, Y. et al. Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons. Nat. Neurosci. 9, 1125–1137 (2020). source
- Not checked yetcites [21] Cai, D. et al. Distinct anatomical connectivity patterns differentiate subdivisions of the nonlemniscal auditory thalamus in mice. Cereb. Cortex 6, 2437–2454 (2018).
- Not checked yetcites [22] Dobolyi, A., Cservenák, M. & Young, L. J. Thalamic integration of social stimuli regulating parental behavior and the oxytocin system. Front. Neuroendocrinol. 51, 102–115 (2018). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“PVN oxytocin cells receive projections from many areas of the brain”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [3] Valtcheva, S. & Froemke, R. C. Neuromodulation of maternal circuits by oxytocin. Cell Tissue Res. 1, 57–68 (2019). source
- Not checked yetcites [10] Grinevich, V. & Stoop, R. Interplay between oxytocin and sensory systems in the orchestration of socio-emotional behaviors. Neuron 99, 887–904 (2018). source
- Not checked yetcites [11] Chini, B., Verhage, M. & Grinevich, V. The action radius of oxytocin release in the mammalian CNS: From single vesicles to behavior. Trends Pharmacol. Sci. 11, 982–991 (2017). source
- Not checked yetcites [12] Resendez, S. L. et al. Social stimuli induce activation of oxytocin neurons within the paraventricular nucleus of the hypothalamus to promote social behavior in male mice. J. Neurosci. 40, 2282–2295 (2020). source
- Not checked yetcites [13] Tang, Y. et al. Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons. Nat. Neurosci. 9, 1125–1137 (2020). source
- Not checked yetcites [14] Carcea, I. et al. Oxytocin neurons enable social transmission of maternal behaviour. Nature 596, 553–557 (2021). source
- Not checked yetcites [15] Yukinaga, H. et al. Recording and manipulation of the maternal oxytocin neural activities in mice. Curr. Biol. 32, 3821–3829 (2022). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“These results show that pup vocalizations can activate PVN oxytocin neurons, but not with stimulus-locked responses such as those typically observed in the central auditory system”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
plaindirectn = 7 ·- Asserted: passes — The authors put it forward as true.
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In the paper
“This effect is possibly because blocking oxytocin signalling in the VTA produces a more marked reduction of pup-retrieval behaviour than does selective chemogenetic inhibition of upstream PIL inputs to the PVN.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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In the paper
“Hypothalamic inhibition increases during lactation46 and might prevent the activation of oxytocin neurons by sparse synaptic inputs”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
What the sources say
- Not checked yetcites [46] Giesl, U. & Theodosis, T. Synaptic plasticity in the rat supraoptic nucleus during lactation involves GABA innervation and oxytocin neurons: a quantitative immunocytochemical analysis. J. Neurosci. 5, 2861–2869 (1994). source
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In the paper
“Sample sizes were chosen to reliably measure experimental effects while minimizing the number of animals used in accordance with ethical guidelines.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
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In the paper
“Parvocellular neurons can also directly activate magnocellular neurons and have been proposed to operate as ‘master cells’ that control the activity of magnocellular cells and gate oxytocin release1,13.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
What the sources say
- Not checked yetcites [1] Althammer, F. & Grinevich,. Diversity of oxytocin neurons: beyond magno- and parvocellular cell types?. J. Neuroendocrinol. 30, e12549 (2017). source
- Not checked yetcites [13] Tang, Y. et al. Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons. Nat. Neurosci. 9, 1125–1137 (2020). source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Experiments were repeated independently with similar results for: N = 6 mice, Fig. 1b; N = 7, Fig. 1i; N = 4, Fig. 2b–e; N = 27, Fig. 4b; N = 5, Fig. 5e,f; N = 4, Fig. 5g; N = 5, Fig. 5h; N = 4, Fig. 5j; N = 6, Extended Data Fig. 4a.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Statistics and reproducibility
plainn = 27- Asserted: passes — The authors put it forward as true.
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In the paper
“No statistical methods were used to predetermine sample size.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
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In the paper
“Blinding was not relevant and not performed for in vivo cell-attached, whole-cell and tungsten recordings, fiber photometry experiments, oxytocin sensor experiments and in vitro whole-cell recordings because auditory stimuli/optogenetic stimulation in vivo, and optogenetic/electrical stimulation and/or pharmacological application in vitro were performed in real time by the experimenter.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
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In the paper
“This shows that the enhanced firing of PVN oxytocin neurons after pup calls can lead to central oxytocin release in downstream brain areas controlling pup retrieval such as the VTA, and that this effect is mediated by the activation of PIL inputs to the PVN.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
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In the paper
“Animals were randomly assigned to different groups.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
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In the paper
“Postsynaptic NMDARs also regulate excitability48,49 and trigger somatodendritic oxytocin release47.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
What the sources say
- Not checked yetcites [47] de Kock, C. P. J., Burnashev, N., Lodder, J. C., Mansvelder, H. D. & Brussaard, A. B. NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats. J. Physiol. 561, 53–64 (2004). source
- Not checked yetcites [48] Fleming, T. M. et al. State-dependent changes in astrocyte regulation of extrasynaptic NMDA receptor signalling in neurosecretory neurons. J. Physiol. 16, 3929–3941 (2011). source
- Not checked yetcites [49] Naskar, K. & Stern, J. E. A functional coupling between extrasynaptic NMDA receptors and A-type K+ channels under astrocyte control regulates hypothalamic neurosecretory neuronal activity. J. Physiol. 592, 2813–2827 (2014). source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“PIL inputs onto parvocellular neurons controlled central oxytocin release and the efficiency of pup retrieval over time.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“These findings suggest that PIL opto rapidly triggers iLTD in oxytocin neurons through postsynaptic NMDARs and dynamin signalling, possibly triggering the internalization of postsynaptic GABAARs to decrease inhibitory transmission and increase spiking output.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Persistent activity seems to be a hallmark of hypothalamic neurons, which can be highly interconnected and have long integration periods42–45.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
What the sources say
- Not checked yetcites [42] Iremonger, K. J. & Bains, J. S. Integration of asynchronously released quanta prolongs the postsynaptic spike window. J. Neurosci. 27, 6684–6691 (2007). source
- Not checked yetcites [43] Branco, T. et al. Near-perfect synaptic integration by Nav1.7 in hypothalamic neurons regulates body weight. Cell 165, 1749–1761 (2016). source
- Not checked yetcites [44] Kennedy, A. et al. Stimulus-specific hypothalamic encoding of a persistent defensive state. Nature 586, 730–734 (2020). source
- Not checked yetcites [45] Daviu, N. et al. Paraventricular nucleus CRH neurons encode stress controllability and regulate defensive behavior selection. Nat. Neurosci. 23, 398–410 (2020). source
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“The investigators were blinded to allocation during behavioral testing, fiber photometry data analysis and oxytocin sensor data analysis.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
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In the paper
“This would allow parvocellular neurons to regulate or control oxytocin release into different brain areas such as the VTA according to animal state and sensory experience.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Detection of endogenously released oxytocin in the VTA of female and male mice during social interactions has been previously demonstrated using OXTR-iTango2 (ref. 40).”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [40] Mignocchi, N., Jung, K., Lee, D. & Kwon, H.-B. Development of a genetically-encoded oxytocin sensor. Preprint at bioRxiv https://doi.org/10.1101/2020.07.14.202598 (2020). source
boosted- Asserted: passes — The authors put it forward as true.
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In the paper
“Oxytocin-neuron NMDARs can be activated without the need for postsynaptic spiking47, suggesting that even if PIL inputs are too weak to trigger action potentials, prolonged subthreshold activation of oxytocin cells is sufficient to induce NMDAR-dependent inhibitory LTD.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
What the sources say
- Not checked yetcites [47] de Kock, C. P. J., Burnashev, N., Lodder, J. C., Mansvelder, H. D. & Brussaard, A. B. NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats. J. Physiol. 561, 53–64 (2004). source
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“The experiments were not randomized.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“PIL lesions can impair pup-retrieval behaviour34.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Abstract
What the sources say
- Not checked yetcites [34] Factor, E. M., Mayer, A. D. & Rosenblatt, J. S. Peripeduncular nucleus lesions in the rat: I. Effects on maternal aggression, lactation, and maternal behavior during pre- and postpartum periods. Behav. Neurosci. 107, 166–185 (1993). source
plainconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“Here we define a noncanonical auditory circuit from the PIL to hypothalamic oxytocin neurons, which relays infant distress sounds to induce the release of oxytocin and affect maternal behaviour.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Discussion
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In the paper
“Recordings were excluded from analysis if the access resistance (Ra) changed by more than 30% compared to baseline.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Long-term synaptic plasticity experiments
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
The paper relies on this without support.
Mouse pup distress vocalizations are a valid model for human infant cries in studying maternal oxytocin release.
“Here we describe a neural circuit that routes auditory information about infant vocalizations to mouse oxytocin neurons.”
“In humans, baby cries are a powerful signal of infant distress, and most nursing mothers respond to cries with increased hypothalamic activity, rises in the levels of plasma oxytocin, comforting behaviours towards the infant and occasional milk ejection7,8.”
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?
The cited source says what the claim attributes to it.
In the citing paper
“a study on C57BL/6 N maternal mice revealed that pup vocalizations activate OXT neurons in the PVN through the posterior intralaminar thalamus, part of the non-lemniscal auditory pathway implicated in maternal and social behaviour (Valtcheva et al., 2023).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Valtcheva et al., 2023
The cited source says what the claim attributes to it.
In the citing paper
“This activation results in increased firing of PVN-OXT neurons and central OXT release in areas controlling pup retrieval, especially triggering OXT release in the VTA.”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Valtcheva et al., 2023
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Each contradiction between two passages listed here was confirmed by an independent check.
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In the paper
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
“Animals were randomly assigned to different groups.”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
“The experiments were not randomized.”
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
“The light cycle was 12 h on–12 h off (06:30–18:30 light).”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Mice
“Mice were maintained on a normal 12-h light–dark cycle (dark cycle starts at 18:00) and given food and water ad libitum.”
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Neural circuitry for maternal oxytocin release induced by infant cries > Extended Data
“Pup calls trigger sustained increase in the activity of oxytocin neurons in dams (a; N = 7; Pre vs Post: p = 0.018; Wilcoxon matched-pairs signed-rank one-tailed test)”
§ Neural circuitry for maternal oxytocin release induced by infant cries > Methods > Statistics and reproducibility
“We used Wilcoxon matched-pairs signed-rank two-tailed test in Figs. 1m,n, 3c,d,g and 4d and Extended Data Figs. 1f, 2g,i, 3a–h, 4d, 5d,e and 7f–i.”
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Metadata
- Authors
- Valtcheva, S., Issa, H. A., Bair-Marshall, C. J., Martin, K. A., Jung, K., Zhang, Y., Kwon, H.-B., & Froemke, R. C.
- Affiliations
- NYU Langone Health (US)
- Johns Hopkins University (US)
- New York University (US)
- Corresponding author
- Valtcheva, Silvana
- Froemke, Robert C.
- ORCID
- Venue
- Nature
- Published
- 2023-09-20
- Volume
- 621
- Issue
- 7980
- Pages
- 788-795
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC10639004
- OpenAlex
- W4386886852
- Cited by
- 115
- References
- 74
- Citations by year
- 2026: 24 · 2025: 42 · 2024: 30 · 2023: 10
- FWCI
- 31.31
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Research Square (acceptedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation (HD088411)
- Leon Levy Foundation
- National Alliance for Research on Schizophrenia and Depression
- National Institute of Mental Health (DP1MH119428, T32MH019524)
- National Institute on Deafness and Other Communication Disorders (DC12557, HD088411, R01DC012557)
- National Institute of Neurological Disorders and Stroke (P01NS074972, U19NS107616)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD088411)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Infant Health and Development
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- oxytocin, maternal behavior, infant crying, pup vocalizations, auditory thalamus, neural circuits, disinhibition, sensory cue integration
- MeSH terms
- Animals, Cues, Female, Hypothalamus, Maternal Behavior, Neural Pathways, Neurons, Oxytocin, Photometry, Thalamic Nuclei, Vocalization, Animal, Wakefulness, Mice
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