Innate and plastic mechanisms for maternal behaviour in auditory cortex
- 6 October 2020
- journal article
- research article
- Published by Springer Science and Business Media LLC in Nature
- Vol. 587 (7834), 426-+
- https://doi.org/10.1038/s41586-020-2807-6
Abstract
The onset of maternal behaviour in mice involves an interaction between intrinsic tuning of auditory cortical neurons and experience-dependent plasticity. Infant cries evoke powerful responses in parents(1-4). Whether parental animals are intrinsically sensitive to neonatal vocalizations, or instead learn about vocal cues for parenting responses is unclear. In mice, pup-naive virgin females do not recognize the meaning of pup distress calls, but retrieve isolated pups to the nest after having been co-housed with a mother and litter(5-9). Distress calls are variable, and require co-caring virgin mice to generalize across calls for reliable retrieval(10,11). Here we show that the onset of maternal behaviour in mice results from interactions between intrinsic mechanisms and experience-dependent plasticity in the auditory cortex. In maternal females, calls with inter-syllable intervals (ISIs) from 75 to 375 milliseconds elicited pup retrieval, and cortical responses were generalized across these ISIs. By contrast, naive virgins were neuronally and behaviourally sensitized to the most common ('prototypical') ISIs. Inhibitory and excitatory neural responses were initially mismatched in the cortex of naive mice, with untuned inhibition and overly narrow excitation. During co-housing experiments, excitatory responses broadened to represent a wider range of ISIs, whereas inhibitory tuning sharpened to form a perceptual boundary. We presented synthetic calls during co-housing and observed that neurobehavioural responses adjusted to match these statistics, a process that required cortical activity and the hypothalamic oxytocin system. Neuroplastic mechanisms therefore build on an intrinsic sensitivity in the mouse auditory cortex, and enable rapid plasticity for reliable parenting behaviour.Keywords
This publication has 30 references indexed in Scilit:
- Becoming a mother—circuit plasticity underlying maternal behaviorCurrent Opinion in Neurobiology, 2015
- Decoding of Baby Calls: Can Adult Humans Identify the Eliciting Situation from Emotional Vocalizations of Preverbal Infants?PLOS ONE, 2015
- Oxytocin enables maternal behaviour by balancing cortical inhibitionNature, 2015
- Neural control of maternal and paternal behaviorsScience, 2014
- What makes a cry a cry? A review of infant distress vocalizationsCurrent Zoology, 2012
- Neuroendocrinology of Parental Response to Baby‐CryJournal of Neuroendocrinology, 2011
- Infant Rodent Ultrasounds ? A Gate to the Understanding of Sound CommunicationBehavior Genetics, 2005
- Acoustic variability and distinguishability among mouse ultrasound vocalizationsThe Journal of the Acoustical Society of America, 2003
- Estradiol and parental experience, but not prolactin are necessary for ultrasound recognition and pup-retrieving in the mousePhysiology & Behavior, 1989
- Sex and parental experience determine the onset of an instinctive behavior in miceThe Science of Nature, 1987