Neural plasticity is affected by stress and heritable variation in stress coping style

Johansen, Ida Beitnes; Sørensen, Christina; Sandvik, Guro K.; Nilsson, Göran; Höglund, Erik; Bakken, Morten; Øverli, Øyvind

doi:10.1016/j.cbd.2012.01.002

Cited by 41 publications

(48 citation statements)

References 95 publications

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“…Several authors have proposed that regulating adult neurogenesis may enable animals to alter their behaviour in response to novel environments [22,47,48]. In some animals, brain cell proliferation and subsequent neurogenesis is causally linked to increased cognitive function (memory and learning) and behavioural performance [49].…”

Section: Discussion (A) Predation Pressure Correlates Negatively Withmentioning

confidence: 99%

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

et al. 2016

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Compared with laboratory environments, complex natural environments promote brain cell proliferation and neurogenesis. Predators are one important feature of many natural environments, but, in the laboratory, predatory stimuli tend to inhibit brain cell proliferation. Often, laboratory predatory stimuli also elevate plasma glucocorticoids, which can then reduce brain cell proliferation. However, it is unknown how natural predators affect cell proliferation or whether glucocorticoids mediate the neurogenic response to natural predators. We examined brain cell proliferation in six populations of the electric fish, Brachyhypopomus occidentalis, exposed to three forms of predator stimuli: (i) natural variation in the density of predatory catfish; (ii) tail injury, presumably from predation attempts; and (iii) the acute stress of capture. Populations with higher predation pressure had lower density of proliferating (PCNAþ) cells, and fish with injured tails had lower proliferating cell density than those with intact tails. However, plasma cortisol did not vary at the population level according to predation pressure or at the individual level according to tail injury. Capture stress significantly increased cortisol, but only marginally decreased cell proliferation. Thus, it appears that the presence of natural predators inhibits brain cell proliferation, but not via mechanisms that depend on changes in basal cortisol levels. This study is the first demonstration of predator-induced alteration of brain cell proliferation in a free-living vertebrate.

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Section: Discussion (A) Predation Pressure Correlates Negatively Withmentioning

confidence: 99%

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

et al. 2016

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“…lower post-stress cortisol), as well as lower brain serotonergic and higher dopaminergic activity, while reactive individuals exhibit the opposite behavioural and physiological profile (Koolhaas et al, 2007(Koolhaas et al, , 2010(Koolhaas et al, , 1999. Notably, while differences between coping styles in terms of behaviour, hypothalamic-pituitary-interrenal (HPI) axis reactivity (the fish's HPA equivalent) and monoaminergic activity in multifunctional brain regions, such as the telencephalon, hypothalamus and brainstem, have been reported in fish (Johansen et al, 2012;Schjolden et al, 2006;Silva et al, 2014;Øverli et al, 2001, 2007, a more precise, region-specific, characterisation of telencephalic areas is still lacking. Region-specific studies of functional subdivisions and limbic nuclei are notoriously difficult in fish, as a result of their relatively small size.…”

Section: Introductionmentioning

confidence: 99%

How do individuals cope with stress? Behavioural, physiological and neuronal differences between proactive and reactive coping styles in fish

Vindas

Gorissen

Höglund

et al. 2017

Journal of Experimental Biology

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Despite the use of fish models to study human mental disorders and dysfunctions, knowledge of regional telencephalic responses in nonmammalian vertebrates expressing alternative stress coping styles is poor. As perception of salient stimuli associated with stress coping in mammals is mainly under forebrain limbic control, we tested regionspecific forebrain neural (i.e. mRNA abundance and monoamine neurochemistry) and endocrine responses under basal and acute stress conditions for previously characterised proactive and reactive Atlantic salmon. Reactive fish showed a higher degree of the neurogenesis marker proliferating cell nuclear antigen ( pcna) and dopamine activity under basal conditions in the proposed hippocampus homologue (Dl) and higher post-stress plasma cortisol levels. Proactive fish displayed higher post-stress serotonergic signalling (i.e. higher serotonergic activity and expression of the 5-HT 1A receptor) in the proposed amygdala homologue (Dm), increased expression of the neuroplasticity marker brain-derived neurotropic factor (bdnf ) in both Dl and the lateral septum homologue (Vv), as well as increased expression of the corticotropin releasing factor 1 (crf 1 ) receptor in the Dl, in line with active coping neuro-profiles reported in the mammalian literature. We present novel evidence of proposed functional equivalences in the fish forebrain with mammalian limbic structures.

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“…Similarly, zebra fish exposed to an enhanced physical environment simultaneously displayed increased plasma cortisol and forebrain cell proliferation [von Krogh et al, 2010]. Interestingly, in trout (O. mykiss), short-term stress caused by an aggressive conspecific increased forebrain and hypothalamic cell proliferation, and genetic lines selected for high stress responsiveness showed elevated rates of forebrain (and hypothalamic) neurogenesis compared to those with low stress responsiveness [Johansen et al, 2012;Sorensen et al, 2013]. So, in fish, it appears that cortisol sometimes contributes positively to the environmental enhancement of cell proliferation or neurogenesis.…”

Section: Are Environmentally Induced Changes In Brain Cell Proliferatmentioning

confidence: 99%

“…However, in socially interacting fish, this correlation disappeared, suggesting that the influence of the social environment overrides the background connection between overall growth and brain cell proliferation. Regional specificity within the brain was not examined in this study, but similar long-term exposure to subordination reduced the cell proliferation (PCNA mRNA expression) in the hypothalamus, cere- 162 bellum, and optic tectum, but not in the telencephalon, and it reduced neurogenesis (NeuroD mRNA expression) only in the cerebellum [Johansen et al, 2012]. Researchers have proposed that the variability in the proliferative response to social interaction (negative effect vs. no effect) is part of a biphasic effect of stress on the brain, with the severity and duration of stress determining the direction and magnitude of the altered brain cell plasticity [Sorensen et al, 2013].…”

Section: Social Environmentmentioning

confidence: 99%

Fish Neurogenesis in Context: Assessing Environmental Influences on Brain Plasticity within a Highly Labile Physiology and Morphology

Dunlap¹

2016

Brain Behav Evol

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Fish have unusually high rates of brain cell proliferation and neurogenesis during adulthood, and the rates of these processes are greatly influenced by the environment. This high level of cell proliferation and its responsiveness to environmental change indicate that such plasticity might be a particularly important mechanism underlying behavioral plasticity in fish. However, as part of their highly labile physiology and morphology, fish also respond to the environment through processes that affect cell proliferation but that are not specific to behavioral change. For example, the environment has nonspecific influences on cell proliferation all over the body via its effect on body temperature and growth rate. In addition, some fish species also have an unusual capacity for sex change and somatic regeneration, and both of these processes likely involve widespread changes in cell proliferation. Thus, in evaluating the possible behavioral role of adult brain cell proliferation, it is important to distinguish regionally specific responses in behaviorally relevant brain nuclei from global proliferative changes across the whole brain or body. In this review, I first highlight how fish differ from other vertebrates, particularly birds and mammals, in ways that have a bearing on the interpretation of brain plasticity. I then summarize the known effects of the physical and social environment, sex change, and predators on brain cell proliferation and neurogenesis, with a particular emphasis on whether the effects are regionally specific. Finally, I review evidence that environmentally induced changes in brain cell proliferation and neurogenesis in fish are mediated by hormones and play a role in behavioral responses to the environment.

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Neural plasticity is affected by stress and heritable variation in stress coping style

Cited by 41 publications

References 95 publications

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

How do individuals cope with stress? Behavioural, physiological and neuronal differences between proactive and reactive coping styles in fish

Fish Neurogenesis in Context: Assessing Environmental Influences on Brain Plasticity within a Highly Labile Physiology and Morphology

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