Innate and plastic mechanisms in auditory cortex for maternal behavior

Infant cries evoke powerful responses in parents(1–4). To what extent are parental animals intrinsically sensitive to neonatal vocalizations, or might instead learn about vocal cues for parenting responses? In mice, pup-naive virgins do not recognize the meaning of pup distress calls, but retrieve isolated pups to the nest following cohousing with a mother and litter(5–9). Distress calls are variable, requiring co-caring virgins to generalize across calls for reliable retrieval(10,11). Here we show that the onset of maternal behavior in mice results from interactions between intrinsic mechanisms and experience-dependent plasticity in auditory cortex. In maternal females, calls with inter-syllable intervals (ISIs) from 75:375 ms elicited pup retrieval, and cortical responses generalized across these ISIs. In contrast, naive virgins were behaviorally sensitive only to the most common (‘prototypical’) ISIs. Inhibitory and excitatory neural responses were initially mismatched in naive cortex, with untuned inhibition and overly-narrow excitation. During cohousing, excitatory responses broadened to represent a wider range of ISIs, while inhibitory tuning sharpened to form a perceptual boundary. We presented synthetic calls during cohousing and observed that neurobehavioral responses adjusted to match these statistics, a process requiring cortical activity and the hypothalamic oxytocin system. Neuroplastic mechanisms therefore build on an intrinsic sensitivity in mouse auditory cortex, enabling rapid plasticity for reliable parenting behavior.