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Father’s care uniquely influences male neurodevelopment

Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early biparental care on development of alloparenting behavior, or caring for offspring that a...

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Detalles Bibliográficos
Autores principales: Danoff, Joshua S., Ramos, Erin N., Hinton, Taylor D., Perkeybile, Allison M., Graves, Andrew J., Quinn, Graham C., Lightbody-Cimer, Aaron R., Gordevičius, Juozas, Milčiūtė, Milda, Brooke, Robert T., Carter, C. Sue, Bales, Karen L., Erisir, Alev, Connelly, Jessica J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10400995/
https://www.ncbi.nlm.nih.gov/pubmed/37487074
http://dx.doi.org/10.1073/pnas.2308798120
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author Danoff, Joshua S.
Ramos, Erin N.
Hinton, Taylor D.
Perkeybile, Allison M.
Graves, Andrew J.
Quinn, Graham C.
Lightbody-Cimer, Aaron R.
Gordevičius, Juozas
Milčiūtė, Milda
Brooke, Robert T.
Carter, C. Sue
Bales, Karen L.
Erisir, Alev
Connelly, Jessica J.
author_facet Danoff, Joshua S.
Ramos, Erin N.
Hinton, Taylor D.
Perkeybile, Allison M.
Graves, Andrew J.
Quinn, Graham C.
Lightbody-Cimer, Aaron R.
Gordevičius, Juozas
Milčiūtė, Milda
Brooke, Robert T.
Carter, C. Sue
Bales, Karen L.
Erisir, Alev
Connelly, Jessica J.
author_sort Danoff, Joshua S.
collection PubMed
description Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early biparental care on development of alloparenting behavior, or caring for offspring that are not one’s own. We find that receiving high parental care early in life leads to slower epigenetic aging of both sexes and widespread male-specific differential expression of genes related to synaptic transmission and autism in the nucleus accumbens. Examination of parental care composition indicates that high-care fathers promote a male-specific increase in excitatory synapses and increases in pup retrieval behavior as juveniles. Interestingly, females raised by high-care fathers have the opposite behavioral response and display fewer pup retrievals. These results support the concept that neurodevelopmental trajectories are programmed by different features of early-life parental care and reveal that male neurodevelopmental processes are uniquely sensitive to care by fathers.
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spelling pubmed-104009952023-08-05 Father’s care uniquely influences male neurodevelopment Danoff, Joshua S. Ramos, Erin N. Hinton, Taylor D. Perkeybile, Allison M. Graves, Andrew J. Quinn, Graham C. Lightbody-Cimer, Aaron R. Gordevičius, Juozas Milčiūtė, Milda Brooke, Robert T. Carter, C. Sue Bales, Karen L. Erisir, Alev Connelly, Jessica J. Proc Natl Acad Sci U S A Biological Sciences Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early biparental care on development of alloparenting behavior, or caring for offspring that are not one’s own. We find that receiving high parental care early in life leads to slower epigenetic aging of both sexes and widespread male-specific differential expression of genes related to synaptic transmission and autism in the nucleus accumbens. Examination of parental care composition indicates that high-care fathers promote a male-specific increase in excitatory synapses and increases in pup retrieval behavior as juveniles. Interestingly, females raised by high-care fathers have the opposite behavioral response and display fewer pup retrievals. These results support the concept that neurodevelopmental trajectories are programmed by different features of early-life parental care and reveal that male neurodevelopmental processes are uniquely sensitive to care by fathers. National Academy of Sciences 2023-07-24 2023-08-01 /pmc/articles/PMC10400995/ /pubmed/37487074 http://dx.doi.org/10.1073/pnas.2308798120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Danoff, Joshua S.
Ramos, Erin N.
Hinton, Taylor D.
Perkeybile, Allison M.
Graves, Andrew J.
Quinn, Graham C.
Lightbody-Cimer, Aaron R.
Gordevičius, Juozas
Milčiūtė, Milda
Brooke, Robert T.
Carter, C. Sue
Bales, Karen L.
Erisir, Alev
Connelly, Jessica J.
Father’s care uniquely influences male neurodevelopment
title Father’s care uniquely influences male neurodevelopment
title_full Father’s care uniquely influences male neurodevelopment
title_fullStr Father’s care uniquely influences male neurodevelopment
title_full_unstemmed Father’s care uniquely influences male neurodevelopment
title_short Father’s care uniquely influences male neurodevelopment
title_sort father’s care uniquely influences male neurodevelopment
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10400995/
https://www.ncbi.nlm.nih.gov/pubmed/37487074
http://dx.doi.org/10.1073/pnas.2308798120
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