Abstract
The wide variety of animal behaviours that can be observed today arose through the evolution of their underlying neural circuits. Advances in understanding the mechanisms through which neural circuits change over evolutionary timescales have lagged behind our knowledge of circuit function and development. This is particularly true for central neural circuits, which are experimentally less accessible than peripheral circuit elements. However, recent technological developments — including cross-species genetic modifications, connectomics and transcriptomics — have facilitated comparative neuroscience studies with a mechanistic outlook. These advances enable knowledge from two classically separate disciplines — neuroscience and evolutionary biology — to merge, accelerating our understanding of the principles of neural circuit evolution. Here we synthesize progress on this topic, focusing on three aspects of neural circuits that change over evolutionary time: synaptic connectivity, neuromodulation and neurons. By drawing examples from a wide variety of animal phyla, we reveal emerging principles of neural circuit evolution.
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Acknowledgements
The authors thank T. Baden from the University of Sussex, R. Arguello from the University of Lausanne and J. L. Ramos from the L.L.P.-G. laboratory for discussions and comments on the manuscript. They thank J. Brock at the Francis Crick Institute for help with illustrations. R.J.V.R. is supported by a Boehringer Ingelheim Fonds Ph.D. fellowship. L.L.P.-G.’s laboratory is supported by a European Research Council Starting Investigator Grant (802531), an Allen Distinguished Investigator Award, a Human Frontiers Science Grant (RGY0052/2022) and the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001594), the UK Medical Research Council (FC001594) and the Wellcome Trust (FC001594).
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Glossary
- Alleles
-
Different versions of a DNA sequence found in a particular genomic location.
- Alternative splicing
-
The process that, during pre-mRNA processing, rearranges exons (coding sequences) and thus allows a single gene to encode multiple proteins.
- Clades
-
Groups of organisms that are derived from a common ancestor.
- Comparative studies
-
Research work where two or more species are compared side by side to identify differences between them.
- Connectomics
-
The generation of comprehensive synaptic resolution maps of the connections among the neurons of an organism’s nervous system.
- Corollary discharge
-
Internal activity generated by nervous systems that carries information about a motor command and is used to estimate the outcomes of executed movements (for example, to help distinguish between self-generated and externally induced sensory input).
- Evolvability
-
Here, the ability of particular features of a system to facilitate change.
- Extant species
-
Species that can be found alive today, as opposed to species that were extinguished at some time in the past.
- Functomics
-
High-throughput investigation of neuronal circuit function.
- Homologues
-
Structures that share a common ancestral origin.
- Neural circuit blueprint
-
The assembly of characters that determine the general organization of a brain, including the number and/or type of neurons, organization of cell bodies and mesoscale connectivity.
- Phylogenetic distances
-
The amounts of time that elapsed between the divergence of pairs of species from their most recent common ancestor.
- Pleiotropy
-
The phenomenon in which a gene affects multiple unrelated phenotypic traits. In evolution, pleiotropy is considered to limit the potential for change because modifications in a gene could simultaneously affect one trait in an adaptive way but cause maladaptive changes in another.
- RNA editing
-
The process that modifies specific nucleotides of RNAs potentially altering their function.
- Retroelement
-
Genome sequences that can be transcribed into RNA, can be reverse transcribed into DNA and can be inserted at another genome location.
- Single-cell transcriptomics
-
The study of the gene expression of individual cells.
- Terminal differentiation genes
-
Genes that confer cellular properties through their function, rather than influencing the expression of other genes.
- Transcription factor genes
-
Genes that function by regulating the expression of other genes.
- Wiring economy theory
-
A theory that proposes that nervous systems have evolved to minimize neurite length to minimize the energetic cost of the maintenance of neuronal extensions.
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Cite this article
Roberts, R.J.V., Pop, S. & Prieto-Godino, L.L. Evolution of central neural circuits: state of the art and perspectives. Nat Rev Neurosci 23, 725–743 (2022). https://doi.org/10.1038/s41583-022-00644-y
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DOI: https://doi.org/10.1038/s41583-022-00644-y
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