Becoming a better parent: Mice learn sounds that improve a stereotyped maternal behavior
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...
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Published in | Hormones and behavior Vol. 124; p. 104779 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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01.08.2020
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Abstract | 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. |
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AbstractList | 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. 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. |
ArticleNumber | 104779 |
Author | Dunlap, Alexander G. Chong, Kelly K. Kacsoh, Dorottya B. Walum, Hasse Liu, Robert C. Tankeu, Brenda B. Lu, Kai Pascual, Leila M. Besosa, Cristina |
AuthorAffiliation | h Silvio O. Conte Center for Oxytocin and Social Cognition and Center for Translational Social Neuroscience, Atlanta, GA, USA b Department of Biology, Emory University, Atlanta, GA, USA a Bioengineering Interdisciplinary Graduate Program, Georgia Institute of Technology, Atlanta, GA, USA e Emory College Summer Undergraduate Research Experience Program, Atlanta, GA, USA d Department of Natural Sciences, Bowie State University, Bowie, MD, USA g Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA f Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, USA c Neuroscience Graduate Program, Emory University, Atlanta, GA, USA |
AuthorAffiliation_xml | – name: b Department of Biology, Emory University, Atlanta, GA, USA – name: c Neuroscience Graduate Program, Emory University, Atlanta, GA, USA – name: a Bioengineering Interdisciplinary Graduate Program, Georgia Institute of Technology, Atlanta, GA, USA – name: h Silvio O. Conte Center for Oxytocin and Social Cognition and Center for Translational Social Neuroscience, Atlanta, GA, USA – name: d Department of Natural Sciences, Bowie State University, Bowie, MD, USA – name: g Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – name: e Emory College Summer Undergraduate Research Experience Program, Atlanta, GA, USA – name: f Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, USA |
Author_xml | – sequence: 1 givenname: Alexander G. surname: Dunlap fullname: Dunlap, Alexander G. organization: Bioengineering Interdisciplinary Graduate Program, Georgia Institute of Technology, Atlanta, GA, USA – sequence: 2 givenname: Cristina surname: Besosa fullname: Besosa, Cristina organization: Department of Biology, Emory University, Atlanta, GA, USA – sequence: 3 givenname: Leila M. surname: Pascual fullname: Pascual, Leila M. organization: Neuroscience Graduate Program, Emory University, Atlanta, GA, USA – sequence: 4 givenname: Kelly K. surname: Chong fullname: Chong, Kelly K. organization: Department of Biology, Emory University, Atlanta, GA, USA – sequence: 5 givenname: Hasse surname: Walum fullname: Walum, Hasse organization: Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – sequence: 6 givenname: Dorottya B. surname: Kacsoh fullname: Kacsoh, Dorottya B. organization: Department of Biology, Emory University, Atlanta, GA, USA – sequence: 7 givenname: Brenda B. surname: Tankeu fullname: Tankeu, Brenda B. organization: Department of Natural Sciences, Bowie State University, Bowie, MD, USA – sequence: 8 givenname: Kai surname: Lu fullname: Lu, Kai organization: Department of Biology, Emory University, Atlanta, GA, USA – sequence: 9 givenname: Robert C. surname: Liu fullname: Liu, Robert C. email: robert.liu@emory.edu organization: Department of Biology, Emory University, Atlanta, GA, USA |
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CitedBy_id | crossref_primary_10_1016_j_mex_2021_101536 crossref_primary_10_1016_j_neuron_2020_07_022 crossref_primary_10_12688_molpsychol_17558_1 crossref_primary_10_1016_j_mex_2020_101051 crossref_primary_10_1371_journal_pone_0244033 crossref_primary_10_3389_fnbeh_2023_1139254 crossref_primary_10_1016_j_heares_2023_108738 crossref_primary_10_1016_j_neuron_2022_11_019 crossref_primary_10_1111_1749_4877_12722 crossref_primary_10_1016_j_bbr_2022_113846 |
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Copyright | 2020 The Authors Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved. |
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Keywords | Parental behavior Ultrasonic vocalizations Operant conditioning Social behavior Sensory learning Predisposition Plasticity Auditory cortex |
Language | English |
License | This is an open access article under the CC BY-NC-ND license. Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AGD and RCL designed research; AGD, CB, LMP, KKC, DBK and BBT carried out experiments; HW and KL contributed to methods; AGD, CB, LMP and DBK analyzed data; AGD and RCL wrote the paper. We thank Vanessa Wong for experimental assistance. Contributions |
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Snippet | While mothering is often instinctive and stereotyped in species-specific ways, evolution can favor genetically “open” behavior programs that allow experience... While mothering is often instinctive and stereotyped in species-specific ways, evolution can favor genetically "open" behavior programs that allow experience... |
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SubjectTerms | 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 |
Title | Becoming a better parent: Mice learn sounds that improve a stereotyped maternal behavior |
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