Expanding our horizons: central pattern generation in the context of complex activity sequences

Abstract

Central pattern generators (CPGs) are central nervous system (CNS) networks that can generate coordinated output in the absence of patterned sensory input. For decades, this concept was applied almost exclusively to simple, innate, rhythmic movements with essentially identical cycles that repeat continually (e.g. respiration) or episodically (e.g. locomotion). But many natural movement sequences are not simple rhythms, as they include different elements in a complex order, and some involve learning. The concepts and experimental approaches of CPG research have also been applied to the neural control of complex movement sequences, such as birdsong, though this is not widely appreciated. Experimental approaches to the investigation of CPG networks, both for simple rhythms and for complex activity sequences, have shown that: (1) brief activation of the CPG elicits a long-lasting naturalistic activity sequence; (2) electrical stimulation of CPG elements alters the timing of subsequent cycles or sequence elements; and (3) warming or cooling CPG elements respectively speeds up or slows down the rhythm or sequence rate. The CPG concept has also been applied to the activity rhythms of populations of mammalian cortical neurons. CPG concepts and methods might further be applied to a variety of fixed action patterns typically used in courtship, rivalry, nest building and prey capture. These complex movements could be generated by CPGs within CPGs ('nested' CPGs). Stereotypical, non-motor, nonrhythmic neuronal activity sequences may also be generated by CPGs. My goal here is to highlight previous applications of the CPG concept to complex but stereotypical activity sequences and to suggest additional possible applications, which might provoke new hypotheses and experiments.

A re-evaluation of silk measurement by the cecropia caterpillar (Hyalophora cecropia) during cocoon construction reveals use of a silk odometer that is temporally regulated

“…https://doi.org/10.1371/journal.pone.0228453.g007 through the spinneret; the behavioral aspects of the odometer could be viewed as a fixed action pattern because they are stereotyped, complex, species-specific, triggered (see below) and independent of experience [17]. The silk odometer appears to have different OE settings for construction of either the baggy or compact cocoon morphs.…”

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

“…The discovery that both short time-scale and long time-scale subroutines within grooming behavior show periodicity suggests the possibility that they may both be controlled by central pattern generating circuits. The proposal that nested CPGs simplify the control of repetitive motor sequences (Berkowitz, 2019) is an appealing framework to explain rhythmicity in complex behaviors such as grooming that occur on multiple time-scales. We now consider the response of these rhythms to increasing temperature as additional evidence that central pattern generators govern both time-scales, and to determine whether the two levels of the proposed nested CPGs are independent or interlocked.…”

“…In the vertebrate spinal cord, inhibitory and excitatory commissural neurons can cause the CPGs controlling the legs to synchronize for a hopping gait or operate out-of-phase for walking (Kiehn, 2016). This concept of nested CPGs has recently been extended to explain flexible coordination of behaviors ranging from fish swimming to bird song (Berkowitz, 2019). In a recent publication, a very similar nested CPG to the one we are proposing here has been described in the crab stomatogastric ganglion where fast pyloric and slow gastric mill rhythms are coupled (Powell, Haddad, Gorur-Shandilya, & Marder, 2020).…”

“…Central pattern generators (CPGs) are neural circuits that produce rhythmic motor outputs in response to a trigger without requiring ongoing descending drive or patterned sensory inputs (Hooper & Büschges, 2017). CPGs control short stereotypic actions in cat walking, crayfish swimming, locust flight, leech heartbeat, and the stomatogastric and pyloric rhythms of crustaceans (reviewed in (Berkowitz, 2019; Grillner, 2006; Marder & Calabrese, 1996; Mulloney & Smarandache, 2010; Selverston, 2010)). However, CPGs may also contribute to control more complex behaviors.…”

“…Increasingly complex sequences can be assembled from shorter elements, suggesting hierarchical control. When repetitive subroutines are themselves composed of simpler periodic movements, it has been suggested that they may be controlled by nested CPGs, hierarchically organized so that a “high-level” slow CPG controls the behavior on coarse scale and a “lower-level” fast CPG adds the fine structure (Berkowitz, 2019). In other words, the slow CPG controls alternations between subroutines and the fast CPG controls alternations within these subroutines.…”