Becoming a better parent: Mice learn sounds that improve a stereotyped maternal behavior

• Published in: Hormones and behavior Vol. 124; p. 104779
• Main Authors: Dunlap, Alexander G., Besosa, Cristina, Pascual, Leila M., Chong, Kelly K., Walum, Hasse, Kacsoh, Dorottya B., Tankeu, Brenda B., Lu, Kai, Liu, Robert C.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.08.2020
• Subjects: Acoustic Stimulation; Animals; Animals, Newborn; Auditory cortex; Auditory Cortex - physiology; Behavior, Animal - physiology; Conditioning, Operant - physiology; Female; Humans; Learning - physiology; Maternal Behavior - physiology; Maze Learning; Mice; Mice, Inbred CBA; Motivation; Neuronal Plasticity - physiology; Operant conditioning; Parental behavior; Plasticity; Predisposition; Sensory learning; Social Behavior; Sound Localization - physiology; Stereotyped Behavior - physiology; Ultrasonic vocalizations; Vocalization, Animal - physiology; Parental behavior; Ultrasonic vocalizations; Operant conditioning; Social behavior; Sensory learning; Predisposition; Plasticity; Auditory cortex
• ISSN: 0018-506X; 1095-6867
• DOI: 10.1016/j.yhbeh.2020.104779

While mothering is often instinctive and stereotyped in species-specific ways, evolution can favor genetically “open” behavior programs that allow experience to shape infant care. Among experience-dependent maternal behavioral mechanisms, sensory learning about infants has been hard to separate from motivational changes arising from sensitization with infants. We developed a paradigm in which sensory learning of an infant-associated cue improves a stereotypical maternal behavior in female mice. Mice instinctively employed a spatial memory-based strategy when engaged repetitively in a pup search and retrieval task. However, by playing a sound from a T-maze arm to signal where a pup will be delivered for retrieval, mice learned within 7 days and retained for at least 2 weeks the ability to use this specific cue to guide a more efficient search strategy. The motivation to retrieve pups also increased with learning on average, but their correlation did not explain performance at the trial level. Bilaterally silencing auditory cortical activity significantly impaired the utilization of new strategy without changing the motivation to retrieve pups. Finally, motherhood as compared to infant-care experience alone accelerated how quickly the new sensory-based strategy was acquired, suggesting a role for the maternal hormonal state. By rigorously establishing that newly formed sensory associations can improve the performance of a natural maternal behavior, this work facilitates future studies into the neurochemical and circuit mechanisms that mediate novel sensory learning in the maternal context, as well as more learning-based mechanisms of parental behavior in rodents. •Mice learn to switch from a spatial to a sound-based strategy to retrieve pups.•Sensory learning of pup-associated sounds is separable from maternal motivation.•Sound-specific learning lasts for more than 2 weeks.•Learned sound-based strategy requires auditory cortex.•Maternal state accelerates learning the sound-based strategy.