Stressor controllability modulates the stress response in fish

Bibliographic Details
Main Author: Cerqueira, Marco
Publication Date: 2021
Other Authors: Millot, Sandie, Silva, Tomé, Félix, Ana S., Castanheira, Maria Filipa, Rey, Sonia, MacKenzie, Simon, Oliveira, Gonçalo A., Oliveira, Catarina, Oliveira, Rui F.
Format: Article
Language: eng
Source: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Download full: http://hdl.handle.net/10400.1/16915
Summary: Background In humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax). Results Fish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used. Conclusions These results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).
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spelling Stressor controllability modulates the stress response in fishStressControllabilityCortisolImmediate early genesDorsolateral palliumFish welfareBackground In humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax). Results Fish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used. Conclusions These results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).BioMed CentralSapientiaCerqueira, MarcoMillot, SandieSilva, ToméFélix, Ana S.Castanheira, Maria FilipaRey, SoniaMacKenzie, SimonOliveira, Gonçalo A.Oliveira, CatarinaOliveira, Rui F.2021-09-01T09:49:32Z2021-08-042021-09-01T03:25:00Z2021-08-04T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.1/16915eng10.1186/s12868-021-00653-0info:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2025-02-18T17:14:45Zoai:sapientia.ualg.pt:10400.1/16915Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-28T20:15:06.112056Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse
dc.title.none.fl_str_mv Stressor controllability modulates the stress response in fish
title Stressor controllability modulates the stress response in fish
spellingShingle Stressor controllability modulates the stress response in fish
Cerqueira, Marco
Stress
Controllability
Cortisol
Immediate early genes
Dorsolateral pallium
Fish welfare
title_short Stressor controllability modulates the stress response in fish
title_full Stressor controllability modulates the stress response in fish
title_fullStr Stressor controllability modulates the stress response in fish
title_full_unstemmed Stressor controllability modulates the stress response in fish
title_sort Stressor controllability modulates the stress response in fish
author Cerqueira, Marco
author_facet Cerqueira, Marco
Millot, Sandie
Silva, Tomé
Félix, Ana S.
Castanheira, Maria Filipa
Rey, Sonia
MacKenzie, Simon
Oliveira, Gonçalo A.
Oliveira, Catarina
Oliveira, Rui F.
author_role author
author2 Millot, Sandie
Silva, Tomé
Félix, Ana S.
Castanheira, Maria Filipa
Rey, Sonia
MacKenzie, Simon
Oliveira, Gonçalo A.
Oliveira, Catarina
Oliveira, Rui F.
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Sapientia
dc.contributor.author.fl_str_mv Cerqueira, Marco
Millot, Sandie
Silva, Tomé
Félix, Ana S.
Castanheira, Maria Filipa
Rey, Sonia
MacKenzie, Simon
Oliveira, Gonçalo A.
Oliveira, Catarina
Oliveira, Rui F.
dc.subject.por.fl_str_mv Stress
Controllability
Cortisol
Immediate early genes
Dorsolateral pallium
Fish welfare
topic Stress
Controllability
Cortisol
Immediate early genes
Dorsolateral pallium
Fish welfare
description Background In humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax). Results Fish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used. Conclusions These results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).
publishDate 2021
dc.date.none.fl_str_mv 2021-09-01T09:49:32Z
2021-08-04
2021-09-01T03:25:00Z
2021-08-04T00:00:00Z
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dc.relation.none.fl_str_mv 10.1186/s12868-021-00653-0
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dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
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