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 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.
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
Marco A
MA
Vindas
Department of Biosciences, University of Oslo, Oslo, Norway.
Christina
C
Sørensen
Department of Biosciences, University of Oslo, Oslo, Norway.
Ida B
IB
Johansen
Department of Animal Welfare, Institute of Marine Research, Matredal, Norway.
Ole
O
Folkedal
Department of Marine Ecology and Aquaculture, Danish Institute for Fisheries Research, Hirtshals, Denmark.
Erik
E
Höglund
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
Uniza W
UW
Khan
Department of Animal Welfare, Institute of Marine Research, Matredal, Norway.
Lars H
LH
Stien
Department of Animal Welfare, Institute of Marine Research, Matredal, Norway.
Tore S
TS
Kristiansen
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
Bjarne O
BO
Braastad
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
Øyvind
Ø
Øverli
D000223:Adaptation, Psychological; D000704:Analysis of Variance; D000818:Animals; D001522:Behavior, Animal; D015306:Biogenic Monoamines / Q000378:metabolism; D001921:Brain / Q000378:metabolism; D019208:Brain-Derived Neurotrophic Factor / Q000235:genetics / Q000378:metabolism; D003213:Conditioning, Psychological; D059290:Dopaminergic Neurons / Q000378:metabolism*; D005786:Gene Expression Regulation; D006854:Hydrocortisone / Q000097:blood; D009414:Nerve Growth Factors / Q000378:metabolism*; D018809:Proliferating Cell Nuclear Antigen / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D017447:Receptors, Dopamine D1 / Q000235:genetics / Q000378:metabolism; D017448:Receptors, Dopamine D2 / Q000235:genetics / Q000378:metabolism; D012201:Reward; D020317:Salmo salar / Q000097:blood / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D013312:Stress, Physiological / Q000235:genetics
D015306:Biogenic Monoamines; D019208:Brain-Derived Neurotrophic Factor; D009414:Nerve Growth Factors; D018809:Proliferating Cell Nuclear Antigen; D012333:RNA, Messenger; D017447:Receptors, Dopamine D1; D017448:Receptors, Dopamine D2; D006854:Hydrocortisone