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Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks

Thyroid hormones play a critical role in the initiation of the sensitive period of filial imprinting. The amount of thyroid hormones in the brains of chicks increases intrinsically during the late embryonic stages and peaks immediately before hatching. After hatching, a rapid imprinting-dependent in...

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Autores principales: Serizawa, Shouta, Aoki, Naoya, Mori, Chihiro, Fujita, Toshiyuki, Yamaguchi, Shinji, Matsushima, Toshiya, Homma, Koichi J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9978523/
https://www.ncbi.nlm.nih.gov/pubmed/36875018
http://dx.doi.org/10.3389/fphys.2023.1084816
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author Serizawa, Shouta
Aoki, Naoya
Mori, Chihiro
Fujita, Toshiyuki
Yamaguchi, Shinji
Matsushima, Toshiya
Homma, Koichi J.
author_facet Serizawa, Shouta
Aoki, Naoya
Mori, Chihiro
Fujita, Toshiyuki
Yamaguchi, Shinji
Matsushima, Toshiya
Homma, Koichi J.
author_sort Serizawa, Shouta
collection PubMed
description Thyroid hormones play a critical role in the initiation of the sensitive period of filial imprinting. The amount of thyroid hormones in the brains of chicks increases intrinsically during the late embryonic stages and peaks immediately before hatching. After hatching, a rapid imprinting-dependent inflow of circulating thyroid hormones into the brain occurs via vascular endothelial cells during imprinting training. In our previous study, inhibition of hormonal inflow impeded imprinting, indicating that the learning-dependent inflow of thyroid hormones after hatching is critical for the acquisition of imprinting. However, it remained unclear whether the intrinsic thyroid hormone level just before hatching affects imprinting. Here, we examined the effect of temporal thyroid hormone decrease on embryonic day 20 on approach behavior during imprinting training and preference for the imprinting object. To this end, methimazole (MMI; a thyroid hormone biosynthesis inhibitor) was administered to the embryos once a day on days 18–20. Serum thyroxine (T(4)) was measured to evaluate the effect of MMI. In the MMI-administered embryos, the T(4) concentration was transiently reduced on embryonic day 20 but recovered to the control level on post-hatch day 0. At the beginning of imprinting training on post-hatch day 1, control chicks approached the imprinting object only when the object was moving. In the late phase of training, control chicks subsequently approached towards the static imprinting object. On the other hand, in the MMI-administered chicks, the approach behavior decreased during the repeated trials in the training, and the behavioral responses to the imprinting object were significantly lower than those of control chicks. This indicates that their persistent responses to the imprinting object were impeded by a temporal thyroid hormone decrease just before hatching. Consequently, the preference scores of MMI-administered chicks were significantly lower than those of control chicks. Furthermore, the preference score on the test was significantly correlated with the behavioral responses to the static imprinting object in the training. These results indicate that the intrinsic thyroid hormone level immediately before hatching is crucial for the learning process of imprinting.
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spelling pubmed-99785232023-03-03 Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks Serizawa, Shouta Aoki, Naoya Mori, Chihiro Fujita, Toshiyuki Yamaguchi, Shinji Matsushima, Toshiya Homma, Koichi J. Front Physiol Physiology Thyroid hormones play a critical role in the initiation of the sensitive period of filial imprinting. The amount of thyroid hormones in the brains of chicks increases intrinsically during the late embryonic stages and peaks immediately before hatching. After hatching, a rapid imprinting-dependent inflow of circulating thyroid hormones into the brain occurs via vascular endothelial cells during imprinting training. In our previous study, inhibition of hormonal inflow impeded imprinting, indicating that the learning-dependent inflow of thyroid hormones after hatching is critical for the acquisition of imprinting. However, it remained unclear whether the intrinsic thyroid hormone level just before hatching affects imprinting. Here, we examined the effect of temporal thyroid hormone decrease on embryonic day 20 on approach behavior during imprinting training and preference for the imprinting object. To this end, methimazole (MMI; a thyroid hormone biosynthesis inhibitor) was administered to the embryos once a day on days 18–20. Serum thyroxine (T(4)) was measured to evaluate the effect of MMI. In the MMI-administered embryos, the T(4) concentration was transiently reduced on embryonic day 20 but recovered to the control level on post-hatch day 0. At the beginning of imprinting training on post-hatch day 1, control chicks approached the imprinting object only when the object was moving. In the late phase of training, control chicks subsequently approached towards the static imprinting object. On the other hand, in the MMI-administered chicks, the approach behavior decreased during the repeated trials in the training, and the behavioral responses to the imprinting object were significantly lower than those of control chicks. This indicates that their persistent responses to the imprinting object were impeded by a temporal thyroid hormone decrease just before hatching. Consequently, the preference scores of MMI-administered chicks were significantly lower than those of control chicks. Furthermore, the preference score on the test was significantly correlated with the behavioral responses to the static imprinting object in the training. These results indicate that the intrinsic thyroid hormone level immediately before hatching is crucial for the learning process of imprinting. Frontiers Media S.A. 2023-02-16 /pmc/articles/PMC9978523/ /pubmed/36875018 http://dx.doi.org/10.3389/fphys.2023.1084816 Text en Copyright © 2023 Serizawa, Aoki, Mori, Fujita, Yamaguchi, Matsushima and Homma. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Serizawa, Shouta
Aoki, Naoya
Mori, Chihiro
Fujita, Toshiyuki
Yamaguchi, Shinji
Matsushima, Toshiya
Homma, Koichi J.
Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
title Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
title_full Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
title_fullStr Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
title_full_unstemmed Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
title_short Temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
title_sort temporal hampering of thyroid hormone synthesis just before hatching impeded the filial imprinting in domestic chicks
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9978523/
https://www.ncbi.nlm.nih.gov/pubmed/36875018
http://dx.doi.org/10.3389/fphys.2023.1084816
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