Involvement of hormones in olfactory imprinting and homing in chum salmon.

Masahiko Watanabe,Shigeo Tsuchida,Kaoru Inada,Reiichi Murakami,Shingo Nakamura,Takashi Okubo,Taro Nakamura,Kotaro Konno,Yonathan Zohar,Naohiro Furukawa,Hiroshi Ueda

doi:10.1038/srep21102

Masahiko Watanabe, Shigeo Tsuchida + Show 9 more

Open Access

https://doi.org/10.1038/srep21102

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Abstract

The olfactory hypothesis for salmon imprinting and homing to their natal stream is well known, but the endocrine hormonal control mechanisms of olfactory memory formation in juveniles and retrieval in adults remain unclear. In brains of hatchery-reared underyearling juvenile chum salmon (Oncorhynchus keta), thyrotropin-releasing hormone gene expression increased immediately after release from a hatchery into the natal stream, and the expression of the essential NR1 subunit of the N-methyl-D-aspartate receptor increased during downstream migration. Gene expression of salmon gonadotropin-releasing hormone (sGnRH) and NR1 increased in the adult chum salmon brain during homing from the Bering Sea to the natal hatchery. Thyroid hormone treatment in juveniles enhanced NR1 gene activation, and GnRHa treatment in adults improved stream odour discrimination. Olfactory memory formation during juvenile downstream migration and retrieval during adult homing migration of chum salmon might be controlled by endocrine hormones and could be clarified using NR1 as a molecular marker.

Highlights

We show that the gene expression of NR1 and thyrotropin-releasing hormone (TRH) increased during downstream migration to the sea in the juvenile chum salmon brain and that NR1 and salmon gonadotropin-releasing hormone gene expression increased in the brain during adult homing from the Bering Sea to the natal hatchery
Using underyearling juvenile chum salmon reared in a hatchery and released into the Chitose River (Hokkaido, Japan) to allow migration to the sea (Fig. 1), the relationship between brain-pituitary-thyroid (BPT) hormones and natal stream odour imprinting was investigated based on whole-brain mRNA expression of thyrotropin-releasing hormones (TRHa and TRHb; neurohormone in the salmon brain and the leading hormone in the BPT axis) and NR1, upper head thyrotropin β subunit (TSHβ ), thyroid hormones (thyroxine (T4) and triiodothyronine (T3)) isolated in the lower jaw that contained thyroid glands, and the electro-olfactogram response (EOG) to stream water odour
The endocrine control of osmoregulation in relation to seawater adaptability has been intensively studied in teleost fish, including salmon[10,11], and a relationship between the T4 surge and the onset of downstream migration has been reported in juvenile chum salmon[23]

Summary

Introduction

We show that the gene expression of NR1 and thyrotropin-releasing hormone (TRH) increased during downstream migration to the sea in the juvenile chum salmon brain and that NR1 and salmon gonadotropin-releasing hormone (sGnRH) gene expression increased in the brain during adult homing from the Bering Sea to the natal hatchery. Juvenile treatment with thyroid hormone enhanced NR1 gene activation, and adult treatment with GnRHa increased stream odour discrimination ability. This work demonstrates that NR1 expression in the brain plays crucial roles in olfactory memory formation and retrieval that might be controlled by endocrine hormones in juvenile and adult chum salmon, respectively. Investigation of this mechanism will allow researchers to predict responses to altered biochemical environments and provides tools to explain migratory salmon behaviour, including straying rates

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