Evolution of central pattern generators and rhythmic behaviours

Abstract

One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Comparisons of rhythmic movements and the central pattern generators (CPGs) that control them uncover principles about the evolution of behaviour and neural circuits. Over the course of evolutionary history, gradual evolution of behaviours and their neural circuitry within any lineage of animals has been a predominant occurrence. Small changes in gene regulation can lead to divergence of circuit organization and corresponding changes in behaviour. However, some behavioural divergence has resulted from large-scale rewiring of the neural network. Divergence of CPG circuits has also occurred without a corresponding change in behaviour. When analogous rhythmic behaviours have evolved independently, it has generally been with different neural mechanisms. Repeated evolution of particular rhythmic behaviours has occurred within some lineages due to parallel evolution or latent CPGs. Particular motor pattern generating mechanisms have also evolved independently in separate lineages. The evolution of CPGs and rhythmic behaviours shows that although most behaviours and neural circuits are highly conserved, the nature of the behaviour does not dictate the neural mechanism and that the presence of homologous neural components does not determine the behaviour. This suggests that although behaviour is generated by neural circuits, natural selection can act separately on these two levels of biological organization.

Degeneracy in hippocampal physiology and plasticity

“…Healthy and invigorating debates related to the philosophical and the scientific basis of such analyses, with themes ranging from broad discussions on reductionism versus holism (Bennett & Hacker, ; Bickle, ; Jazayeri & Afraz, ; Krakauer, Ghazanfar, Gomez‐Marin, MacIver, & Poeppel, ; Panzeri, Harvey, Piasini, Latham, & Fellin, ) to more focused debates on the specific cellular components that are involved in specific aspects of coding and behavior (Bliss & Collingridge, ; Gallistel, ; Kandel et al, ; Kim & Linden, ; Martin et al, ; Mayford et al, ; Mozzachiodi & Byrne, ; Neves, Cooke, & Bliss, ; Otchy et al, ; Titley, Brunel, & Hansel, ; Zhang & Linden, ), have contributed to our emerging understanding of neural systems and their links to behavior. Several studies have covered the breadth and depth of these debates (Bargmann & Marder, ; Bennett & Hacker, ; Bickle, ; Jazayeri & Afraz, ; Jonas & Kording, ; Kandel et al, ; Katz, ; Kim & Linden, ; Krakauer et al, ; Lazebnik, ; Marder, ; Marder, ; Marder, ; Marder, O'Leary, & Shruti, ; Marder & Thirumalai, ; Mayford et al, ; Panzeri et al, ; Tytell, Holmes, & Cohen, ), and will not be the focus of this review.…”

“…Larger perturbations beyond the black circle, however, would not yield robust functionality. The presence of multiple clusters of red circles in the smaller scale represents degeneracy, where similar functionality is achieved if parameters are within any of those multiple clusters [Color figure can be viewed at wileyonlinelibrary.com] Bickle, 2015;Jazayeri & Afraz, 2017;Jonas & Kording, 2017;Kandel et al, 2014;Katz, 2016;Kim & Linden, 2007;Krakauer et al, 2017;Lazebnik, 2002;Marder, 1998;Marder, 2011;Marder, 2012;Marder, O'Leary, & Shruti, 2014;Marder & Thirumalai, 2002;Mayford et al, 2012;Panzeri et al, 2017;Tytell, Holmes, & Cohen, 2011), and will not be the focus of this review.…”

“…The advantages of biological variability (Foster, Ungar, & Schwaber, ; Gjorgjieva, Drion, & Marder, ; Goldman, Golowasch, Marder, & Abbott, ; Katz, ; Marder, ; Marder & Goaillard, ; Marder, Goeritz, & Otopalik, ; Marder & Taylor, ; O'Leary & Marder, ; Prinz, Bucher, & Marder, ; ), degeneracy (Drion, O'Leary, & Marder, ; Edelman & Gally, ; Leonardo, ; O'Leary, Williams, Caplan, & Marder, ; Whitacre & Bender, ; Whitacre, ) and complexity (Carlson & Doyle, ; Edelman & Gally, ; Stelling, Sauer, Szallasi, Doyle 3rd, & Doyle, ; Tononi, Sporns, & Edelman, ; Tononi, Sporns, & Edelman, ; Weng, Bhalla, & Iyengar, ; Whitacre, ), especially in terms of their roles in achieving robust function, have been widely studied and recognized in several biological process, including those in simple nervous systems. However, this recognition has been very limited in the mammalian neuroscience literature, a literature where the focus is predominantly on explicitly assigning (or implicitly assuming) unique causal mechanistic relationships between constituent components and emergent functions.…”

Introduction to ‘Homology and convergence in nervous system evolution’

“…Drawing from a wealth of studies of circuits that mediate rhythmically patterned motor actions, particularly in gastropod molluscs, Paul Katz [36] shows that comparative studies reveal a common Leitmotif: that of divergent evolution of behaviours resulting from evolutionary modifications of homologous underlying circuits. The author also shows that whereas major rewiring of an ancestral circuit leads to corresponding changes of behaviour, in some instances divergence of wiring has arisen without any observable behavioural alteration.…”

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

“…West-Eberhard, 1983;Kirkpatrick and Ryan, 1991;Gerhardt, 1994), specific changes in the neural circuits responsible for the evolution of signaling have only recently been identified (e.g. Chakraborty and Jarvis, 2015;Katz, 2016). Neural circuits controlling stereotyped courtship behaviors produced by closely related species can reveal these proximate mechanisms (Katz and Harris-Warrick, 1999).…”