Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).

Comparative studies are imperative for understanding the evolution of adaptive neurobiological processes such as neural plasticity, cognition, and emotion. Previously we have reported that prolonged omission of expected rewards (OER, or 'frustrative nonreward') causes increased aggression...

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Published in:PLoS ONE
Main Authors: Vindas, Marco A, Sørensen, Christina, Johansen, Ida, Folkedal, Ole, Höglund, Erik, Khan, Uniza W, Stien, Lars H, Kristiansen, Tore, Braastad, Bjarne O, Overli, Oyvind
Format: Article in Journal/Newspaper
Language:English
Published: 2014
Subjects:
Online Access:https://orbit.dtu.dk/en/publications/b2718a1c-ad39-4bcc-8c26-749a01e3c5a1
https://doi.org/10.1371/journal.pone.0085543
https://backend.orbit.dtu.dk/ws/files/88519700/fetchObject.action.pdf
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spelling ftdtupubl:oai:pure.atira.dk:publications/b2718a1c-ad39-4bcc-8c26-749a01e3c5a1 2024-06-23T07:51:21+00:00 Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.). Vindas, Marco A Sørensen, Christina Johansen, Ida Folkedal, Ole Höglund, Erik Khan, Uniza W Stien, Lars H Kristiansen, Tore Braastad, Bjarne O Overli, Oyvind 2014 application/pdf https://orbit.dtu.dk/en/publications/b2718a1c-ad39-4bcc-8c26-749a01e3c5a1 https://doi.org/10.1371/journal.pone.0085543 https://backend.orbit.dtu.dk/ws/files/88519700/fetchObject.action.pdf eng eng https://orbit.dtu.dk/en/publications/b2718a1c-ad39-4bcc-8c26-749a01e3c5a1 info:eu-repo/semantics/openAccess Vindas , M A , Sørensen , C , Johansen , I , Folkedal , O , Höglund , E , Khan , U W , Stien , L H , Kristiansen , T , Braastad , B O & Overli , O 2014 , ' Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.). ' , PloS one. , vol. 9 , no. 1 , pp. e85543 . https://doi.org/10.1371/journal.pone.0085543 article 2014 ftdtupubl https://doi.org/10.1371/journal.pone.0085543 2024-06-04T15:06:29Z Comparative studies are imperative for understanding the evolution of adaptive neurobiological processes such as neural plasticity, cognition, and emotion. Previously we have reported that prolonged omission of expected rewards (OER, or 'frustrative nonreward') causes increased aggression in Atlantic salmon (Salmo salar). Here we report changes in brain monoaminergic activity and relative abundance of brain derived neurotrophic factor (BDNF) and dopamine receptor mRNA transcripts in the same paradigm. Groups of fish were initially conditioned to associate a flashing light with feeding. Subsequently, the expected food reward was delayed for 30 minutes during two out of three meals per day in the OER treatment, while the previously established routine was maintained in control groups. After 8 days there was no effect of OER on baseline brain stem serotonin (5-HT) or dopamine (DA) activity. Subsequent exposure to acute confinement stress led to increased plasma cortisol and elevated turnover of brain stem DA and 5-HT in all animals. The DA response was potentiated and DA receptor 1 (D1) mRNA abundance was reduced in the OER-exposed fish, indicating a sensitization of the DA system. In addition OER suppressed abundance of BDNF in the telencephalon of non-stressed fish. Regardless of OER treatment, a strong positive correlation between BDNF and D1 mRNA abundance was seen in non-stressed fish. This correlation was disrupted by acute stress, and replaced by a negative correlation between BDNF abundance and plasma cortisol concentration. These observations indicate a conserved link between DA, neurotrophin regulation, and corticosteroid-signaling pathways. The results also emphasize how fish models can be important tools in the study of neural plasticity and responsiveness to environmental unpredictability. Article in Journal/Newspaper Atlantic salmon Salmo salar Technical University of Denmark: DTU Orbit PLoS ONE 9 1 e85543
institution Open Polar
collection Technical University of Denmark: DTU Orbit
op_collection_id ftdtupubl
language English
description Comparative studies are imperative for understanding the evolution of adaptive neurobiological processes such as neural plasticity, cognition, and emotion. Previously we have reported that prolonged omission of expected rewards (OER, or 'frustrative nonreward') causes increased aggression in Atlantic salmon (Salmo salar). Here we report changes in brain monoaminergic activity and relative abundance of brain derived neurotrophic factor (BDNF) and dopamine receptor mRNA transcripts in the same paradigm. Groups of fish were initially conditioned to associate a flashing light with feeding. Subsequently, the expected food reward was delayed for 30 minutes during two out of three meals per day in the OER treatment, while the previously established routine was maintained in control groups. After 8 days there was no effect of OER on baseline brain stem serotonin (5-HT) or dopamine (DA) activity. Subsequent exposure to acute confinement stress led to increased plasma cortisol and elevated turnover of brain stem DA and 5-HT in all animals. The DA response was potentiated and DA receptor 1 (D1) mRNA abundance was reduced in the OER-exposed fish, indicating a sensitization of the DA system. In addition OER suppressed abundance of BDNF in the telencephalon of non-stressed fish. Regardless of OER treatment, a strong positive correlation between BDNF and D1 mRNA abundance was seen in non-stressed fish. This correlation was disrupted by acute stress, and replaced by a negative correlation between BDNF abundance and plasma cortisol concentration. These observations indicate a conserved link between DA, neurotrophin regulation, and corticosteroid-signaling pathways. The results also emphasize how fish models can be important tools in the study of neural plasticity and responsiveness to environmental unpredictability.
format Article in Journal/Newspaper
author Vindas, Marco A
Sørensen, Christina
Johansen, Ida
Folkedal, Ole
Höglund, Erik
Khan, Uniza W
Stien, Lars H
Kristiansen, Tore
Braastad, Bjarne O
Overli, Oyvind
spellingShingle Vindas, Marco A
Sørensen, Christina
Johansen, Ida
Folkedal, Ole
Höglund, Erik
Khan, Uniza W
Stien, Lars H
Kristiansen, Tore
Braastad, Bjarne O
Overli, Oyvind
Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).
author_facet Vindas, Marco A
Sørensen, Christina
Johansen, Ida
Folkedal, Ole
Höglund, Erik
Khan, Uniza W
Stien, Lars H
Kristiansen, Tore
Braastad, Bjarne O
Overli, Oyvind
author_sort Vindas, Marco A
title Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).
title_short Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).
title_full Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).
title_fullStr Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).
title_full_unstemmed Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.).
title_sort coping with unpredictability: dopaminergic and neurotrophic responses to omission of expected reward in atlantic salmon (salmo salar l.).
publishDate 2014
url https://orbit.dtu.dk/en/publications/b2718a1c-ad39-4bcc-8c26-749a01e3c5a1
https://doi.org/10.1371/journal.pone.0085543
https://backend.orbit.dtu.dk/ws/files/88519700/fetchObject.action.pdf
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Vindas , M A , Sørensen , C , Johansen , I , Folkedal , O , Höglund , E , Khan , U W , Stien , L H , Kristiansen , T , Braastad , B O & Overli , O 2014 , ' Coping with unpredictability: Dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.). ' , PloS one. , vol. 9 , no. 1 , pp. e85543 . https://doi.org/10.1371/journal.pone.0085543
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container_issue 1
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