Innate and plastic mechanisms for maternal behaviour in auditory cortex

Infant cries evoke powerful responses in parents. 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 litte. Distress calls are variable, and require co-caring virgin mice to generalize across calls for reliable retrieval. 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.

幼崽啼哭（Infant cries）会在亲代个体身上引发强烈反应。目前学界尚未明确，亲代动物究竟是天生对新生子代的发声信号具有敏感性，还是后天习得了抚育行为所需的发声线索。在小鼠模型中，未接触过幼崽的处女雌性个体无法识别幼崽遇险叫声的含义，但在与母鼠及其幼崽同笼饲养后，它们会将分离的幼崽叼回巢穴。幼崽的遇险叫声存在显著个体差异，需经抚育经验的处女雌性个体对不同叫声进行泛化，才能可靠完成幼崽叼回行为。本研究证实，小鼠母性行为的产生源于听觉皮层（auditory cortex）内先天机制与经验依赖性可塑性（experience-dependent plasticity）的相互作用。在具备母性的雌性小鼠中，音节间间隔（inter-syllable intervals, ISIs）处于75至375毫秒区间的叫声可诱发幼崽叼回行为，且皮层反应可对该区间内的不同ISIs实现泛化。与之形成鲜明对比的是，未经历抚育的处女雌性个体仅对最常见的“典型”ISIs表现出神经与行为层面的敏化反应。未接触过幼崽的小鼠皮层内，抑制性与兴奋性神经反应最初并不匹配：抑制作用未经过调谐，而兴奋性反应范围过窄。在同笼饲养实验过程中，兴奋性反应的范围逐渐拓宽，以覆盖更广泛的ISIs区间，而抑制性调谐则逐渐收窄，形成感知边界。我们在同笼饲养期间人工合成叫声进行刺激，观察到神经行为反应会随这些叫声的统计特征进行调整，这一过程依赖于皮层活动与下丘脑催产素系统（hypothalamic oxytocin system）。综上，神经可塑性机制基于小鼠听觉皮层的先天敏感性，可快速实现可塑性变化，从而保障可靠的抚育行为。