Abstract

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.

Highlights

  • The evolution of complex neural phenomena such as cognition and emotion has received increasing scientific attention in the last few decades

  • Growth rates and plasma cortisol An initial avoidance response to the conditioned stimulus (CS) was observed upon exposure to the conditioning regime, but the fish quickly started accumulating in the CS/unconditioned stimulus (US) area in response to expected food delivery (Figure 1, and see [19] for detailed time-course data)

  • Dihydroxyphenylacetic acid (DOPAC) concentrations and the DOPAC/ DA ratio were not significantly different between treatment groups under unstressed conditions. Both treatment groups responded with increased DOPAC/DA ratios to acute confinement stress, while only OER fish had significantly increased DOPAC levels after confinement stress

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Summary

Introduction

The evolution of complex neural phenomena such as cognition and emotion has received increasing scientific attention in the last few decades. Comparative studies on teleost fish models have questioned whether the existence of cognitive abilities (i.e. attention, perception, memory formation) in these animals render them capable of consciously experiencing affective states such as stress, pain and frustration. Vital to forming appropriate behavioral responses is behavioral plasticity; the ability to respond differently to the same stimulus depending on experience, sensory information and internal state [7,8]. In fishes as well as in mammals, the biological basis of behavioral plasticity is neural plasticity [8,9,10,11], which can be categorized into two main forms: Biochemical switching, including modulation of the neural output to a stimulus by neuromodulators such as monoamine neurotransmitters; and structural reorganization of neural networks including longterm potentiation (LTP), neurogenesis and dendritic arborization [7,8,10]

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