Swimming exercise enhances brain plasticity in fish.

Daan Mes,Christiaan V Henkel,Ian Mayer,Arjan P Palstra,Marco A Vindas

doi:10.1098/rsos.191640

Abstract

It is well-established that sustained exercise training can enhance brain plasticity and boost cognitive performance in mammals, but this phenomenon has not received much attention in fish. The aim of this study was to determine whether sustained swimming exercise can enhance brain plasticity in juvenile Atlantic salmon. Brain plasticity was assessed by both mapping the whole telencephalon transcriptome and conducting telencephalic region-specific microdissections on target genes. We found that 1772 transcripts were differentially expressed between the exercise and control groups. Gene ontology (GO) analysis identified 195 and 272 GO categories with a significant overrepresentation of up- or downregulated transcripts, respectively. A multitude of these GO categories was associated with neuronal excitability, neuronal signalling, cell proliferation and neurite outgrowth (i.e. cognition-related neuronal markers). Additionally, we found an increase in proliferating cell nuclear antigen (pcna) after both three and eight weeks of exercise in the equivalent to the hippocampus in fish. Furthermore, the expression of the neural plasticity markers synaptotagmin (syt) and brain-derived neurotrophic factor (bdnf) were also increased due to exercise in the equivalent to the lateral septum in fish. In conclusion, this is the first time that swimming exercise has been directly linked to increased telencephalic neurogenesis and neural plasticity in a teleost, and our results pave the way for future studies on exercise-induced neuroplasticity in fish.

Highlights

There is ample evidence in the mammalian literature that exercise training leads to increased neurogenesis and synaptic plasticity and that this is associated with increased cognition
A pilot study conducted by Luchiari & Chacon [7] demonstrated that exhaustive swimming exercise in zebrafish (Danio rerio) improved their learning performance in a conditioning test within several days
We here report that sustained swimming exercise increases the expression of neuroplasticity- and cell proliferation-related genes in the telencephalon transcriptome of juvenile Atlantic salmon

Summary

Introduction

There is ample evidence in the mammalian literature that exercise training leads to increased neurogenesis and synaptic plasticity and that this is associated with increased cognition. Performance of rodents in spatial tasks [1,2] This effect is strongly associated with increased neurogenesis 2 and synaptic plasticity in the hippocampus, in the dentate gyrus, mediated by an increased abundance of growth factors, neurotransmitters and neurotrophic factors, the exact mechanisms are yet to be elucidated [2,3,4]. Even though the link between exercise, neural plasticity and cognition is well-described in mammals, this phenomenon has not received much attention in other vertebrates, such as fish In this context, fish species are a promising model to study neurobiological mechanisms, those associated with neurogenesis, since fish display neurogenesis in a multitude of proliferation zones throughout their entire lives and rates of cell proliferation in the teleost brain are one to two orders of magnitude higher than in the mammalian brain [5]. A 10-day swim training regime promoted the expression of neurogenesis markers in the brain of zebrafish larvae [8]

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