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Allocating structure to function: the strong links between neuroplasticity and natural selection

A central question in brain evolution is how species-typical behaviors, and the neural function-structure mappings supporting them, can be acquired and inherited. Advocates of brain modularity, in its different incarnations across scientific subfields, argue that natural selection must target domain...

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Autores principales: Anderson, Michael L., Finlay, Barbara L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3882658/
https://www.ncbi.nlm.nih.gov/pubmed/24431995
http://dx.doi.org/10.3389/fnhum.2013.00918
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author Anderson, Michael L.
Finlay, Barbara L.
author_facet Anderson, Michael L.
Finlay, Barbara L.
author_sort Anderson, Michael L.
collection PubMed
description A central question in brain evolution is how species-typical behaviors, and the neural function-structure mappings supporting them, can be acquired and inherited. Advocates of brain modularity, in its different incarnations across scientific subfields, argue that natural selection must target domain-dedicated, separately modifiable neural subsystems, resulting in genetically-specified functional modules. In such modular systems, specification of neuron number and functional connectivity are necessarily linked. Mounting evidence, however, from allometric, developmental, comparative, systems-physiological, neuroimaging and neurological studies suggests that brain elements are used and reused in multiple functional systems. This variable allocation can be seen in short-term neuromodulation, in neuroplasticity over the lifespan and in response to damage. We argue that the same processes are evident in brain evolution. Natural selection must preserve behavioral functions that may co-locate in variable amounts with other functions. In genetics, the uses and problems of pleiotropy, the re-use of genes in multiple networks have been much discussed, but this issue has been sidestepped in neural systems by the invocation of modules. Here we highlight the interaction between evolutionary and developmental mechanisms to produce distributed and overlapping functional architectures in the brain. These adaptive mechanisms must be robust to perturbations that might disrupt critical information processing and action selection, but must also recognize useful new sources of information arising from internal genetic or environmental variability, when those appear. These contrasting properties of “robustness” and “evolvability” have been discussed for the basic organization of body plan and fundamental cell physiology. Here we extend them to the evolution and development, “evo-devo,” of brain structure.
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spelling pubmed-38826582014-01-15 Allocating structure to function: the strong links between neuroplasticity and natural selection Anderson, Michael L. Finlay, Barbara L. Front Hum Neurosci Neuroscience A central question in brain evolution is how species-typical behaviors, and the neural function-structure mappings supporting them, can be acquired and inherited. Advocates of brain modularity, in its different incarnations across scientific subfields, argue that natural selection must target domain-dedicated, separately modifiable neural subsystems, resulting in genetically-specified functional modules. In such modular systems, specification of neuron number and functional connectivity are necessarily linked. Mounting evidence, however, from allometric, developmental, comparative, systems-physiological, neuroimaging and neurological studies suggests that brain elements are used and reused in multiple functional systems. This variable allocation can be seen in short-term neuromodulation, in neuroplasticity over the lifespan and in response to damage. We argue that the same processes are evident in brain evolution. Natural selection must preserve behavioral functions that may co-locate in variable amounts with other functions. In genetics, the uses and problems of pleiotropy, the re-use of genes in multiple networks have been much discussed, but this issue has been sidestepped in neural systems by the invocation of modules. Here we highlight the interaction between evolutionary and developmental mechanisms to produce distributed and overlapping functional architectures in the brain. These adaptive mechanisms must be robust to perturbations that might disrupt critical information processing and action selection, but must also recognize useful new sources of information arising from internal genetic or environmental variability, when those appear. These contrasting properties of “robustness” and “evolvability” have been discussed for the basic organization of body plan and fundamental cell physiology. Here we extend them to the evolution and development, “evo-devo,” of brain structure. Frontiers Media S.A. 2014-01-07 /pmc/articles/PMC3882658/ /pubmed/24431995 http://dx.doi.org/10.3389/fnhum.2013.00918 Text en Copyright © 2014 Anderson and Finlay. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Anderson, Michael L.
Finlay, Barbara L.
Allocating structure to function: the strong links between neuroplasticity and natural selection
title Allocating structure to function: the strong links between neuroplasticity and natural selection
title_full Allocating structure to function: the strong links between neuroplasticity and natural selection
title_fullStr Allocating structure to function: the strong links between neuroplasticity and natural selection
title_full_unstemmed Allocating structure to function: the strong links between neuroplasticity and natural selection
title_short Allocating structure to function: the strong links between neuroplasticity and natural selection
title_sort allocating structure to function: the strong links between neuroplasticity and natural selection
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3882658/
https://www.ncbi.nlm.nih.gov/pubmed/24431995
http://dx.doi.org/10.3389/fnhum.2013.00918
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