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Open Access 01-12-2024 | Research

Socio-affective communication in Tph2-deficient rat pups: communal nesting aggravates growth retardation despite ameliorating maternal affiliation deficits

Authors: Tianhua Wang, Judith R. Homberg, Laura Boreggio, Marta C. F. Samina, Rogério C. R. Castro, Sharon M. Kolk, Natalia Alenina, Michael Bader, Jinye Dai, Markus Wöhr

Published in: Molecular Autism | Issue 1/2024

Abstract

Background

A lack of serotonin (also known as 5-hydroxytryptamine, 5-HT) in the brain due to deficiency of the rate-limiting enzyme in 5-HT synthesis, tryptophan hydroxylase 2 (TPH2), was recently reported to result in impaired maternal affiliation across species, including mice, rats, and monkeys. In rodents, this was reflected in a lack of preference for maternal odors and reduced levels of isolation-induced ultrasonic vocalizations (USV), possibly contributing to a severe growth retardation phenotype.

Methods

Here, we tested whether growth retardation, maternal affiliation deficits, and/or impairments in socio-affective communication caused by Tph2 deficiency can be rescued through early social enrichment in rats. To this aim, we compared male and female Tph2^−/− knockout and Tph2^+/− heterozygous rat pups to Tph2^+/+ wildtype littermate controls, with litters being randomly assigned to standard nesting (SN; one mother with her litter) or communal nesting (CN; two mothers with their two litters).

Results

Our results show that Tph2 deficiency causes severe growth retardation, together with moderate impairments in somatosensory reflexes and thermoregulatory capabilities, partially aggravated by CN. Tph2 deficiency further led to deficits in socio-affective communication, as evidenced by reduced emission of isolation-induced USV, associated with changes in acoustic features, clustering of subtypes, and temporal organization. Although CN did not rescue the impairments in socio-affective communication, CN ameliorated the maternal affiliation deficit caused by Tph2 deficiency in the homing test. To close the communicative loop between mother and pup, we assessed maternal preference and showed that mothers display a preference for Tph2^+/+ controls over Tph2^−/− pups, particularly under CN conditions. This is consistent with the aggravated growth phenotype in Tph2^−/− pups exposed to the more competitive CN environment.

Conclusion

Together, this indicates that CN aggravates growth retardation despite ameliorating maternal affiliation deficits in Tph2-deficient rat pups, possibly due to reduced and acoustically altered isolation-induced USV, hindering efficient socio-affective communication between mother and pup.

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Title: Socio-affective communication in Tph2-deficient rat pups: communal nesting aggravates growth retardation despite ameliorating maternal affiliation deficits
Authors: Tianhua Wang
Judith R. Homberg
Laura Boreggio
Marta C. F. Samina
Rogério C. R. Castro
Sharon M. Kolk
Natalia Alenina
Michael Bader
Jinye Dai
Markus Wöhr
Publication date: 01-12-2024
Publisher: BioMed Central
Published in: Molecular Autism / Issue 1/2024
Electronic ISSN: 2040-2392
DOI: https://doi.org/10.1186/s13229-024-00629-x

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Neuroligin-2 shapes individual slow waves during slow-wave sleep and the response to sleep deprivation in mice

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Autistic and non-autistic individuals show the same amygdala activity during emotional face processing

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Autism Spectrum Disorder
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Superior temporal sulcus folding, functional network connectivity, and autistic-like traits in a non-clinical population

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Publisher Correction: Measuring self and informant perspectives of restricted and repetitive behaviours (RRBs): psychometric evaluation of the repetitive Behaviours Questionnaire-3 (RBQ-3) in adult clinical practice and research settings

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Publisher Correction

Phenome-wide profiling identifies genotype-phenotype associations in Phelan-McDermid syndrome using family-sourced data from an international registry

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Socio-affective communication in Tph2-deficient rat pups: communal nesting aggravates growth retardation despite ameliorating maternal affiliation deficits

Abstract

Background

Methods

Results

Conclusion

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Abstract

Background

Methods

Results

Conclusion

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Fetal brain growth and infant autistic traits

Neuroligin-2 shapes individual slow waves during slow-wave sleep and the response to sleep deprivation in mice

Autistic and non-autistic individuals show the same amygdala activity during emotional face processing

Superior temporal sulcus folding, functional network connectivity, and autistic-like traits in a non-clinical population

Publisher Correction: Measuring self and informant perspectives of restricted and repetitive behaviours (RRBs): psychometric evaluation of the repetitive Behaviours Questionnaire-3 (RBQ-3) in adult clinical practice and research settings

Phenome-wide profiling identifies genotype-phenotype associations in Phelan-McDermid syndrome using family-sourced data from an international registry