Maternal motivation overcomes innate fear via prefrontal switching dynamics

Parental care is altruistic. In natural environments, parents are often faced with challenging environmental conditions, such as severe weather, complex terrain and predatory threats, and therefore need to overcome the fear of adverse conditions to protect and raise the offspring. Although a few studies have reported risk-taking maternal behaviors1-3, it is unknown how maternal motivation and environmental threats are represented and integrated in neural circuits to resolve the conflict and dynamically drive behaviors. Here we report a novel risk-taking maternal behavior paradigm in a semi-naturalistic context, in which a female mouse has to overcome fear and jump off an elevated platform to retrieve pups outside a nest on the ground. We show that while fear of heights reduces the motivation to jump, the presence of pups dramatically facilitates overcoming such fear. A medial prefrontal-periaqueductal gray (mPFC-PAG) pathway is specifically required for the effect of pups on overcoming fear of height, and this circuit integrates conflicting cues about pup and height and encodes motivation to drive risk-taking jumping behaviors. In contrast to cued, fast and predictable reaction timing in typical structured tasks4,5, behaviors in our paradigm are highly spontaneous, characterized by stochastic transitions between low-motivation and high-motivation states. Our data reveal that such spontaneity is shaped by the switching ramping dynamics of neural activity in the motivation-encoding dimension, rather than continuous ramping dynamics. Pup and height cues modulate the switching ramping dynamics to influence, but not immediately evoke behaviors. Together, we propose that the prefrontal-brainstem pathway plays vital roles in encoding altruistic motivation to overcome innate fear, and the switching ramping dynamics might represent a general mechanism that gives rise to spontaneous behaviors in naturalistic and conflicting conditions.