Limbic brain activation for maternal acoustic perception and responding is different in mothers and virgin female mice

Mothers are primed to become maternal through hormonal changes during pregnancy and delivery of young, virgin females need experience with young for performing maternally. The activation of brain areas controlling maternal behavior can be studied by stimulus-induced expression of the immediate-early gene Fos and immunocytochemical labeling of the FOS protein in activated cells. With this technique we identified areas of the mouse limbic system stimulated by acoustically adequate or inadequate models of pup ultrasounds that, if perceived as adequate, direct the search for lost pups (phonotaxis). Behavioral observations and neural activation data suggest that adequate (50 kHz long tones) and inadequate ultrasound models (50 kHz short or 20 kHz long tones) are differently processed in limbic areas of mothers and virgin females with 1 or 5 days of pup-caring experience depending on the news value and the recognition of the stimuli: High numbers of FOS-positive cells in the medial preoptic area, lateral septum, and bed nucleus of the stria terminalis (mothers and virgins) relate to the salience (news value) of the perceived sounds; contextual stress may be reflected by high activation in parts of the amygdala and the ventromedial hypothalamus (virgins); high activation in the piriform cortex suggests associative learning of adequate sounds and in the entorhinal cortex remembering associations of adequate sounds with pups (virgins). Thus brain areas were differently activated in animals with maternal emotions, however different responses to pup cues depending on how they got primed to behave maternally and on how they evaluated the stimulation context.

► c-FOS immunocytochemistry detects activation differences in the limbic brain.
► Mothers’ limbic brain activation is low, virgin females’ high, when acting maternally.
► Mothers rest in confidence, virgin females are stressed by calls of young.
► Mothers know the meaning of sounds instinctively, virgin females have to learn.