Advanced paternal age diversifies individual trajectories of vocalization patterns in neonatal mice

Lingling Mai; Hitoshi Inada; Ryuichi Kimura; Kouta Kanno; Takeru Matsuda; Ryosuke O Tachibana; Valter Tucci; Fumiyasu Komaki; Noboru Hiroi; Noriko Osumi

doi:10.1016/j.isci.2022.104834

Advanced paternal age diversifies individual trajectories of vocalization patterns in neonatal mice

iScience. 2022 Aug 11;25(8):104834. doi: 10.1016/j.isci.2022.104834. eCollection 2022 Aug 19.

Authors

Lingling Mai¹, Hitoshi Inada^{1

2}, Ryuichi Kimura^{1

3}, Kouta Kanno⁴, Takeru Matsuda⁵, Ryosuke O Tachibana⁶, Valter Tucci⁷, Fumiyasu Komaki^{8

9}, Noboru Hiroi^{10

11

12}, Noriko Osumi¹

Affiliations

¹ Department of Developmental Neuroscience, Tohoku University Graduate School of Medicine, Sendai 980-8575, Japan.
² Laboratory of Health and Sports Sciences, Division of Biomedical Engineering for Health and Welfare, Tohoku University Graduate School of Biomedical Engineering, Sendai 980-8575, Japan.
³ Department of Drug Discovery Medicine, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan.
⁴ Faculty of Law, Economics and Humanities, Kagoshima University, Kagoshima 890-0065, Japan.
⁵ Statistical Mathematics Unit, RIKEN Center for Brain Science, Wako 351-0198, Japan.
⁶ Department of Life Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo 153-8902, Japan.
⁷ Genetics and Epigenetics of Behavior (GEB) Laboratory, Istituto Italiano di Tecnologia, Genova 16163, Italy.
⁸ Department of Mathematical Informatics, Graduate School of Information Science and Technology, The University of Tokyo, Tokyo 113-8656, Japan.
⁹ Mathematical Informatics Collaboration Unit, RIKEN Center for Brain Science, Wako 351-0198, Japan.
¹⁰ Department of Pharmacology, University of Texas Health Science Center at San Antonio, San Antonio 78229, USA.
¹¹ Department of Cellular and Integrative Physiology, University of Texas Health Science Center at San Antonio, San Antonio 78229, USA.
¹² Department of Cell Systems and Anatomy, University of Texas Health Science Center at San Antonio, San Antonio 78229, USA.

Abstract

Infant crying is a communicative behavior impaired in neurodevelopmental disorders (NDDs). Because advanced paternal age is a risk factor for NDDs, we performed computational approaches to evaluate how paternal age affected vocal communication and body weight development in C57BL/6 mouse offspring from young and aged fathers. Analyses of ultrasonic vocalization (USV) consisting of syllables showed that advanced paternal age reduced the number and duration of syllables, altered the syllable composition, and caused lower body weight gain in pups. Pups born to young fathers had convergent vocal characteristics with a rich repertoire, whereas those born to aged fathers exhibited more divergent vocal patterns with limited repertoire. Additional analyses revealed that some pups from aged fathers displayed atypical USV trajectories. Thus, our study indicates that advanced paternal age has a significant effect on offspring's vocal development. Our computational analyses are effective in characterizing altered individual diversity.

Keywords: Behavioral neuroscience; Developmental neuroscience; Neuroscience.