Evolution of central pattern generators and rhythmic behaviours

Abstract

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.

Keywords: comparative; homologous neurons; homoplasy; motor pattern; neural circuit; neuromodulation.

Figure 1.

Independence of behaviours and neural mechanisms. This hypothetical tree shows a how behaviours A, B and C and their variations might have evolved. There are three clades (α, β, γ) which have ancestral neural mechanisms a, b and c. See §1b for further explanation. (Online version in colour.)

Figure 2.

Conservative evolution of axial locomotion. (a) The segmental CPG for swimming in lampreys, tadpoles and zebrafish larvae is organized as a half-centre oscillator. The left and right sides are mutually inhibitory through commissural interneurons (CIN). Excitatory and inhibitory interneurons (EIN and IIN) participate in motor pattern generation. EIN synapses on motor neurons (MN) that cause muscle contraction. Each neuron in the diagram represents large pools of heterogeneous neurons. Triangles are excitatory synapses and circles are inhibitory. CPG based on ref. [16]. (b) The lamprey swims with a sinusoidal movement. The left and right sides of the body alternately flex. (c) Salamanders walk using an alternating axial muscle gait with left and right sides in alternation.

Figure 3.

Metamorphosis of Xenopus showing changes in motor patterns. (a) Tadpoles exhibit axial locomotion with left and right sides of the tail alternating. The plot on the right shows an idealized recording of ventral root activity, with alternation between left and right at root one (VR1) and progressive activity down spinal segments on the right side (VR1, 8, 15). (b) In early premetamorphosis, limb buds have emerged, but activity is still strictly axial with left right alternation. Flexors and extensors on hindlimbs are coactive with tail. (c) In late premetamorphosis, the legs are now independent of the tail and two motor patterns exist at the same time, a rapid tail movement and a slower bilaterally symmetric kicking movement. Now, flexors and extensors alternate, but left and right legs are coactive. (d) In the adult frog, the tail has been absorbed and the legs continue to exhibit a bilaterally symmetric kicking movement. Adapted from [20]. (Online version in colour.)

Figure 4.

Single gene mutations cause changes in mammalian gait. (a) When trotting, the legs on the same side move in opposite directions. (b) When pacing, ipsilateral legs move in the same direction. Icelandic horses homozygous for a nonsense mutation in the DMRT3 gene naturally pace. (c) In typical fictive locomotion from a neonatal mouse spinal cord, regular rhythmic activity occurs in the left (l) and right (r) lumber (L) roots from spinal ventral roots 2 and 5. (d) In mice lacking Dmrt3 expression, the fictive motor pattern is irregular. (e) Neurons expressing the ephrin receptor A4 (EphA4, black) normally are repelled by the ephrin ligand B3 (EphrinB3, dark grey). In EphA4 knock-out mice, these neurons can cross the midline. (f) Schematic of the fictive motor pattern from a wild-type mouse shows normal left–right alternation. (g) In EphA4 knockout mice, left and right flexors burst synchronously and out of phase with extensors, producing a hopping gait. (a–d) Adapted with permission from [24]; (e) based upon Kiehn [25]. (Online version in colour.)

Figure 5.

Different feeding neural circuitry in two nematodes. (a) The nematodes C. elegans and P. pacificus have different feeding behaviours. In C. elegans, a terminal bulb structure called the grinder mechanically breaks up bacteria. The grinder is missing in P. pacificus, which instead has a predatory dorsal tooth that breaks open prey items. The picture shows P. pacificus feeding on C. elegans. (b) Schematic of the C. elegans and P. pacificus feeding neural networks showing massive rewiring of neurons and their connections to muscles and other outputs such as epithelial cells and glands. Lines curve clockwise from presynaptic to postsynaptic targets. Line width indicates weight according to the number of synaptic connections observed in serial electron microscopic images. Based on Bumbarger et al. [33]. (Online version in colour.)

Figure 6.

Divergent CPGs underlying homologous behaviours. (a) Dendronotus iris swims with left–right whole body flexions. (b) The CPG underlying this behaviour has a simple half-centre organization with the left and right Si2 inhibiting each other. Si1 does not make or receive any contralateral inhibition. (c) Simultaneous intracellular recordings show that Si1 fires irregularly, whereas the two contralateral Si2 burst in alternation during the swim motor pattern. (d) Melibe leonina swims in the same manner as Dendronotus. (e) The swim CPG in Melibe is more complicated than that of Dendronotus. Si1, Si2 and the contralateral Si4 are electrically coupled and each inhibits its own contralateral counterpart (represented by the grey dashed circle). The left and right Si3 inhibit each other and have complex synaptic interactions with the other CPG neurons. (f) Simultaneous intracellular microelectrode recordings show that the ipsilateral Si1 and Si2 fire in bursts of action potentials in alternation with the contralateral Si2. The contralateral Si3 follows Si2. Filled circles represent inhibitory synapses, triangles represent excitatory synapses and mixtures of the two represent multicomponent synapses. Resistor symbols represent electrical connections. Based on Sakurai et al. [45] and Sakurai & Katz [46]. (Online version in colour.)

Figure 7.

Parallel evolution of neuromodulatory actions may occur under independent evolution of behaviour. Tritonia diomedea (a,b) and P. californica (c,d) swim with alternating dorsal and ventral body flexions. C2 and DSI, members of the swim CPG, fire rhythmic bursts of action potentials during swim motor patterns evoked by stimulation of a body wall nerve (BWN). DSI stimulation increases the size of EPSPs evoked by C2 in a follower neuron (FN) (bottom). Hermissenda crassicornis (e,f) does not swim with dorsal ventral flexions and BWN stimulation does not cause bursting in the C2 and DSI homologues. Although the DSIs are serotonergic, DSI stimulation also does not increase the size of C2-evoked EPSPs. Based on Lillvis & Katz [70]. (Online version in colour.)

Figure 8.

Leeches and nematodes have independently evolved sinusoidal locomotor behaviours using different CPG circuit motifs. (a) Top image is of a leech swimming, the bottom is a series of traces from a movie, showing the sinusoidal dorsal–ventral movements (adapted from [79]). (b) The nematode C. elegans also moves using sinusoidal dorsal–ventral movements (adapted from [80]). (c) The leech segmental CPG has neurons that fire in three phases of activity, represented at per cent of the period (0%, 33%, 67%). Although most connections are inhibitory, there is no half-centre motif (based on Mullins et al. [79]). (d) A hypothetical computational model of the C. elegans locomotor CPG suggests that it could be located in the head. It contains mostly excitatory connections with inhibitory feedback. There are also inhibitory inputs to muscles that help set up the alternating movements. Note that the neurons in this model, which is based on Karbowski et al. [81] are hypothetical and do not follow the C. elegans nomenclature.