Central Pattern Generators

Abstract

Essential behaviours such as walking or breathing are rhythmic, that is, characterised by repetitive activation of muscles in a specific temporal sequence. A basic version of the underlying neural activity is generated in the central nervous system by networks called central pattern generators (CPGs). CPGs can produce these patterns even in the absence of inputs that carry specific timing information. The core rhythmic activity can be based on intrinsic oscillatory properties of pacemaker neurons or emerge from the synaptic connectivity of nonoscillatory neurons. In both cases, other neurons are recruited into this rhythmic activity to generate a whole pattern. Neuronal and synaptic properties underlying the precise temporal patterning of sequential bursting activity are shaped by neuromodulators to generate different versions of motor patterns. The circuitry controlling rhythmic behaviours of a whole animal is organised in modules that control different body parts and can be coordinated in different ways to generate different behaviours.

Key Concepts

  • Essentially all rhythmic motor behaviours are based on CPGs.
  • CPGs can produce patterned activity in the absence of patterned input.
  • Rhythm generation can be based on intrinsically rhythmic neurons or network interactions.
  • The speed, strength and specific temporal sequence in which CPG neurons fire arise from complex interactions of synaptic and intrinsic neuronal properties governed by diverse types of ion channels.
  • CPG activity is modified by sensory feedback to adapt the motor pattern to changing environmental parameters.
  • CPGs can be activated and reshaped by neuromodulators that adjust neuronal excitability by modifying or suppressing existing ionic currents or adding new currents and changing the properties of synapses.
  • Neuromodulation provides flexibility of motor pattern generation to adjust output to changing behavioural demands.
  • The central networks controlling rhythmic behaviours are inherently modular and allow different coordination of body parts for different behaviours or different versions of the same behaviour.

Keywords: fictive motor pattern; pacemaker; half‐centre oscillator; neuromodulation; unit oscillator

Figure 1. The basic version of rhythmic neural activity underlying repetitive motor behaviours is generated in the central nervous system by central pattern generators (CPGs). (a) Originally, rhythmic motor patterns were thought to arise from chains of reflexes (left panels). In this model, contraction of a muscle, for example, one that controls flexion of a leg joint, leads to proprioceptor signalling that activates the antagonistic extensor muscle through reflex pathways (red). The resulting extension then reflexively activates the flexor again and so forth. It is now clear that such motor patterns are actually based on CPG networks (right panels) that can produce rhythmic activity in the absence of timing information from sensory feedback, for example, through mutually inhibitory connections between neurons controlling different agonists. SN: sensory neuron; MN: motor neuron; eIN: excitatory interneuron, iIN: inhibitory interneuron. (b) Fictive behaviours, that is, activity patterns recorded in the isolated central nervous system that resemble the motor output of the intact animal, are the ultimate proof of the existence of a CPG. A preparation of the rodent brain stem and spinal cord will spontaneously express rhythmic motor activity in electrophysiological recordings of the phrenic nerve, which would lead to inspiratory movements of the diaphragm in the intact animal. When properly pharmacologically activated, this preparation will also show walking‐like motor activity in recordings of ventral roots in the lumbar spinal cord.
Figure 2. Mechanisms underlying rhythm generation. Rhythmic neuron activity in the intact network (left) and after synaptic isolation (right). (a) Rhythm generation can be based on endogenous oscillatory properties of a neuron (red). This neuron continues to burst in synaptic isolation, while an electrically coupled member of the ‘pacemaker group’ (pink) and a follower neuron (green) fall silent or are tonically active. (b) In half‐centre oscillations or other network‐based rhythm generation, bursting activity is usually not based on intrinsic oscillatory properties of neurons but emerges purely from synaptic network interactions. In synaptic isolation, all network neurons therefore fall silent or are tonically active. (c) In some cases, stable and regular rhythm generation may strongly depend on network interactions such as half‐centre oscillations despite the presence of intrinsic bursting properties. In such cases, synaptically isolated neurons may burst endogenously, but at slow frequencies and with irregular periods.
Figure 3. Common membrane properties of CPG neurons. (a) Endogenous oscillations (pacemaker properties). Current inputs can reset rhythmic activity, either by advancing or delaying the next burst. (b) Spike frequency adaptation is the waning of spike frequency during constant depolarizing input. (c) Postinhibitory rebound is the ability to produce activity as a result of prior inhibition. It is often accompanied by a sag potential, that is, an escape from ongoing inhibition. The delay to the onset of the rebound burst can be increased by fast potassium currents such as IA. (d) Plateau potentials are relatively long‐lasting firing responses to sufficiently large but short depolarisations. They can either self‐terminate or end in response to brief hyperpolarizing input.
Figure 4. Neuromodulation of CPGs. (a) Sources of neuromodulation include modulatory projection neurons that release neuromodulators (colours) in a paracrine manner into the local brain area containing the CPG. Projection neurons often co‐release two or more transmitters/modulators. Neuromodulators can also be released by CPG neurons (intrinsic modulation) or reach the CPG as neurohormones (arrows) via the circulatory system or cerebrospinal fluid. (b) Divergent neuromodulatory actions at the cellular level and the resulting changes in network activity, as found for biogenic amine neuromodulators in the pyloric network of the crustacean stomatogastric nervous system. All neurons express receptors (GPCRs) to both modulators (1 and 2, corresponding colours). However, each modulator targets multiple ion channels in a cell type‐specific manner. The effects on neuronal excitability are therefore different across different neurons and different modulators (small network diagrams, colours correspond to target ion channels) and result in different network activity patterns. (c) Cellular convergence and network divergence, as found for a number of neuropeptide modulators in the pyloric network. Each modulator (3, 4 and 5, corresponding colours) targets the same ion channel (red). However, not every receptor is expressed in all neurons. Therefore, each modulator affects a different subset of neurons, resulting in different network activity patterns.
Figure 5. Modular organisation of motor patterns. (a) Unit pattern generators controlling different body parts have to be coordinated to produce meaningful behaviour. Coordination can be achieved through local connectivity or descending commands in the central nervous system or through sensory feedback. Sensory feedback from one body part can directly affect a unit pattern generator controlling a different one or rely on mechanical coupling between two parts. (b) In walking animals, each leg joint has to be controlled by coordinating flexion and extension movements. All joints within one leg have to be coordinated to achieve stepping movements in the proper sequence for stance and swing. All legs have to be coordinated to produce meaningful gaits.
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Bucher, Dirk, Haspel, Gal, Golowasch, Jorge, and Nadim, Farzan(Dec 2015) Central Pattern Generators. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000032.pub2]