Innate and plastic mechanisms for maternal behaviour in auditory cortex

Schiavo, Jennifer K.; Valtcheva, Silvana; Bair-Marshall, Chloe J.; Song, Soomin C.; Martin, Kathleen A.; Froemke, Robert C.

doi:10.1038/s41586-020-2807-6

Cited by 83 publications

(83 citation statements)

References 30 publications

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“…Oxytocin release throughout the central nervous system might then promote plasticity relevant for childcare and other social behaviors, depending on the context and cues linked to oxytocin neuron firing. Specifically, in the mouse auditory cortex, some cells are intrinsically tuned to certain acoustic features of baby cries (Schiavo et al, 2020). These cells might provide an upstream signal driving midbrain and then PIL activity, leading to the sustained increase in oxytocin neuron firing reported here.…”

Section: Discussionmentioning

confidence: 99%

“…Pup distress vocalizations were recorded from isolated pups aged postnatal day (P) 2-8 using an ultrasonic microphone (CM16/CMPA, Avisoft Bioacoustics, Item# 41163, 200 kHz sampling rate; connected to UltraSoundGate 116H recording interface, Avisoft-Bioacoustics, Item# 41163) and de-noised/matched in peak amplitude (Adobe Audition) similar to previous work (Schiavo et al, 2020). To investigate responses to pup calls in individual oxytocin neurons, we monitored baseline firing rates for 1-2 min.…”

Section: Methodsmentioning

confidence: 99%

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Neural circuitry for maternal oxytocin release induced by infant cries

Valtcheva

Issa

Martin

et al. 2021

Preprint

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SummaryOxytocin is a neuropeptide important for maternal physiology and childcare, including parturition and milk ejection during nursing. Suckling triggers oxytocin release, but other sensory cues- specifically infant cries- can elevate oxytocin levels in new human mothers, indicating that cries can activate hypothalamic oxytocin neurons. Here we describe a neural circuit routing auditory information about infant vocalizations to the oxytocin system of the mouse brain. We performed in vivo electrophysiological recordings and photometry from identified oxytocin neurons in awake maternal mice presented with pup calls. We found that oxytocin neurons responded to pup vocalizations via input from the posterior intralaminar thalamus, and repetitive thalamic stimulation induced lasting disinhibition of oxytocin neurons. Suppression of this pathway impaired maternal behavior and playing pup calls led to central oxytocin release in vivo. This circuit provides a mechanism for transforming acoustic input into hormonal output to ensure modulation of brain state required for successful parenting.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Neural circuitry for maternal oxytocin release induced by infant cries

Valtcheva

Issa

Martin

et al. 2021

Preprint

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“…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 15 , 21 . Our results show that although virgin PVN did not respond directly to pup calls, virgin PVN and OT-PVN neurons were recruited by specific experiences during co-housing when abandoned pups would emit distress calls (Extended Data Fig.…”

Section: Pvn Activity and Cortical Plasticitymentioning

confidence: 99%

Oxytocin neurons enable social transmission of maternal behaviour

Carcea

Caraballo

Marlin

et al. 2021

Nature

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161

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Maternal care, including by non-biological parents, is important for offspring survival1–8. Oxytocin1,2,9–15, which is released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone. In mice, oxytocin enables neuroplasticity in the auditory cortex for maternal recognition of pup distress15. However, it is unclear how initial parental experience promotes hypothalamic signalling and cortical plasticity for reliable maternal care. Here we continuously monitored the behaviour of female virgin mice co-housed with an experienced mother and litter. This documentary approach was synchronized with neural recordings from the virgin PVN, including oxytocin neurons. These cells were activated as virgins were enlisted in maternal care by experienced mothers, who shepherded virgins into the nest and demonstrated pup retrieval. Virgins visually observed maternal retrieval, which activated PVN oxytocin neurons and promoted alloparenting. Thus rodents can acquire maternal behaviour by social transmission, providing a mechanism for adapting the brains of adult caregivers to infant needs via endogenous oxytocin.

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“…Interestingly, female mice that learned to retrieve pups show a higher neural response in the auditory cortex to pup distress calls than naive ones (Liu et al, 2006 ). Froemke’s group reported that OT is crucial to drive the cortical plasticity occurring in the auditory cortex of mice which initiated pup retrieval behavior (Marlin et al, 2015 ; Schiavo et al, 2020 ). The recruitment of OTR neurons in the left auditory cortex increases the signal-to-noise ratio of pup calls responses of principal neurons, enabling efficient pup retrieval by their mothers as well as experienced virgins trained by lactating dams.…”

Section: Long-range Oxytocin Modulation Of Sensory Cortical Circuitsmentioning

confidence: 99%

Oxytocinergic Feedback Circuitries: An Anatomical Basis for Neuromodulation of Social Behaviors

Lefèvre

Benusiglio

Tang

et al. 2021

Front. Neural Circuits

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Oxytocin (OT) is a neuropeptide produced by hypothalamic neurons and is known to modulate social behavior among other functions. Several experiments have shown that OT modulates neuronal activity in many brain areas, including sensory cortices. OT neurons thus project axons to various cortical and subcortical structures and activate neuronal subpopulations to increase the signal-to-noise ratio, and in turn, increases the saliency of social stimuli. Less is known about the origin of inputs to OT neurons, but recent studies show that cells projecting to OT neurons are often located in regions where the OT receptor (OTR) is expressed. Thus, we propose the existence of reciprocal connectivity between OT neurons and extrahypothalamic OTR neurons to tune OT neuron activity depending on the behavioral context. Furthermore, the latest studies have shown that OTR-expressing neurons located in social brain regions also project to other social brain regions containing OTR-expressing neurons. We hypothesize that OTR-expressing neurons across the brain constitute a common network coordinated by OT.

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Innate and plastic mechanisms for maternal behaviour in auditory cortex

Cited by 83 publications

References 30 publications

Neural circuitry for maternal oxytocin release induced by infant cries

Neural circuitry for maternal oxytocin release induced by infant cries

Oxytocin neurons enable social transmission of maternal behaviour

Oxytocinergic Feedback Circuitries: An Anatomical Basis for Neuromodulation of Social Behaviors

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