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Plastic changes in brain morphology in relation to learning and environmental enrichment in the guppy (Poecilia reticulata)
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-2233-9262
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0003-3473-1402
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Number of Authors: 52019 (English)In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 222, no 10, article id UNSP jeb200402Article in journal (Refereed) Published
Abstract [en]

Despite the common assumption that the brain is malleable to surrounding conditions mainly during ontogeny, plastic neural changes can occur also in adulthood. One of the driving forces responsible for alterations in brain morphology is increasing environmental complexity that may demand enhanced cognitive abilities (e.g. attention, memory and learning). However, studies looking at the relationship between brain morphology and learning are scarce. Here, we tested the effects of both learning and environmental enrichment on neural plasticity in guppies (Poecilia reticulata), by means of either a reversal-learning test or a spatial-learning test. Given considerable evidence supporting environmentally induced plastic alterations, two separate control groups that were not subjected to any cognitive test were included to account for potential changes induced by the experimental setup alone. We did not find any effect of learning on any of our brain measurements. However, we found strong evidence for an environmental effect, where fish given access to the spatial-learning environment had larger relative brain size and optic tectum size in relation to those exposed to the reversal-learning environment. Our results demonstrate the plasticity of the adult brain to respond adaptively mainly to environmental conditions, providing support for the environmental enhancement theory.

Place, publisher, year, edition, pages
2019. Vol. 222, no 10, article id UNSP jeb200402
Keywords [en]
Brain plasticity, Cognition, Reversal learning, Spatial learning
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-170206DOI: 10.1242/jeb.200402ISI: 000469868900011PubMedID: 31053644OAI: oai:DiVA.org:su-170206DiVA, id: diva2:1337631
Available from: 2019-07-16 Created: 2019-07-16 Last updated: 2022-02-26Bibliographically approved
In thesis
1. Brain morphology and behaviour in the guppy (Poecilia reticulata): Effects of plasticity and mosaic brain evolution
Open this publication in new window or tab >>Brain morphology and behaviour in the guppy (Poecilia reticulata): Effects of plasticity and mosaic brain evolution
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Understanding how brains have evolved and subsequently culminated in the huge variation in brain morphology among contemporary vertebrate species has fascinated researchers for many decades. It has been recognized that brain morphology is both genetically and environmentally determined. Adaptations to ecological challenges, for one, has been proposed to be a major force in brain diversification processes. Considering the large energetic costs of neural tissue, it is believed that brain evolution is a highly complex process, involving a delicate balance between the corresponding costs and benefits. 

Using the guppy (Poecilia reticulata) as the model organism, I first examined the conditions under which diversity in brain morphology is generated. This was done by investigating factors known to exert an influence on brain plasticity, namely environmental and cognitive effects (Paper I). Existing studies generally indicate that the provision of environmental enrichment lead to the enlargement of specific brain structures. While plastic alterations in brain morphology was found to respond to environmental complexity in my study, successful performance in two cognitive tasks did not produce any significant changes. 

I next assessed the feasibility of the mosaic brain evolution hypothesis by artificially selecting for an increase and decrease in the relative size of the telencephalon (Paper II). Telencephalon size was shown to respond rapidly to divergent selection pressures, with no substantial changes in any of the other brain regions. A comparison with wild fish revealed that fish from the unselected control treatment had telencephalon sizes most similar to that of wild populations, whereas both up-selected and down-selected fish had considerably larger and smaller telencephalon, respectively. 

I tested fish from the artificial selection lines in a test battery to determine if known differences in telencephalon size affects boldness (Paper III). Individuals were subjected to an emergence test, an open field test and a novel object test. I found no differences in boldness levels across selection treatments, but distinct sex differences were noted whereby males were more active and bolder. 

The cognitive benefits associated with a larger telencephalon were examined in males in a test of self-control (Paper IV). Guppies from the up-selected lines attained a steeper learning curve and made more correct detours compared to their down-selected conspecifics. 

In conclusion, I provide experimental evidence for the mosaic brain evolution hypothesis by showing that a specific brain region (telencephalon) can evolve rapidly and independently under directed selection. Future tests on other cognitive benefits as well as implicated costs, together with underlying neuronal changes would help to further unravel the factors governing brain evolution.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2020. p. 38
Keywords
brain plasticity, cognition, reversal learning, spatial learning, directed selection, mosaic brain, heritability, brain morphology, boldness, relative telencephalon size, inhibitory control, detour task, Poecilia reticulata
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-186357 (URN)978-91-7911-348-3 (ISBN)978-91-7911-349-0 (ISBN)
Public defence
2020-12-17, online via Zoom, public link is available at the department web site, Stockholm, 10:00 (English)
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Supervisors
Available from: 2020-11-24 Created: 2020-11-02 Last updated: 2022-02-25Bibliographically approved

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Fong, StephanieBuechel, Séverine D.Boussard, AnnikaKotrschal, AlexanderKolm, Niclas

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