Modular organization of the multipartite central pattern generator for turtle rostral scratch: knee-related interneurons during deletions

Abstract

Central pattern generators (CPGs) are neuronal networks in the spinal cord that generate rhythmic patterns of motor activity in the absence of movement-related sensory feedback. For many vertebrate rhythmic behaviors, CPGs generate normal patterns of motor neuron activities as well as variations of the normal patterns, termed deletions, in which bursts in one or more motor nerves are absent from one or more cycles of the rhythm. Prior work with hip-extensor deletions during turtle rostral scratch supports hypotheses of hip-extensor interneurons in a hip-extensor module and of hip-flexor interneurons in a hip-flexor module. We present here single-unit interneuronal recording data that support hypotheses of knee-extensor interneurons in a knee-extensor module and of knee-flexor interneurons in a knee-flexor module. Members of knee-related modules are not members of hip-related modules and vice versa. These results in turtle provide experimental support at the single-unit interneuronal level for the organizational concept that the rostral-scratch CPG for the turtle hindlimb is multipartite, that is, composed of more than two modules. This work, when combined with experimental and computational work in other vertebrates, does not support the classical view that the vertebrate limb CPG is bipartite with only two modules, one controlling all the flexors of the limb and the other controlling all the extensors of the limb. Instead, these results support the general principle that spinal CPGs are multipartite.

Elimination of Left-Right Reciprocal Coupling in the Adult Lamprey Spinal Cord Abolishes the Generation of Locomotor Activity

“…Finally, rhythmic hip flexor bursts can occur in the absence of extensor bursts, suggesting that reciprocal inhibition between flexor and extensor modules is not required for rhythmogenesis of hip flexor CPG modules (Stein et al, 1995 , 1998a ). This conclusion was further supported by extracellular recordings from interneurons associated with flexor and extensor motor activity (Stein et al, 2016 ).…”

Central pattern generators in the turtle spinal cord: selection among the forms of motor behaviors

“…Turtle knee-related spinal interneurons with intermediate overlap with hip-flexor activity can be classified according to the correlations of their start-or end-phases with the startphases of knee-extensor motor activity during normal fictive rostral scratch. The transition from knee-flexor to knee-extensor activity occurred near the middle of hip-flexor activity during normal fictive rostral scratch Daniels-McQueen 2003, 2004;Stein et al 2016). Some interneurons with intermediate levels of overlap with hip-flexor motor activity had their activity start-phases correlated with and near the start-phases of knee extensor activities.…”

“…Propriospinal interneurons have their cell body in the spinal cord and an axon that innervates other spinal cord neurons (Berkowitz and Stein 1994c;Berkowitz 2004;Nissen et al 2008). Single-unit recordings from axons of descending propriospinal interneurons were obtained in the white matter at the posterior cut surface of the spinal cord Stein 1994a, 1994b;Currie and Stein 1990;Daniels-McQueen 2002, 2003;Stein et al 2016).…”

“…We also established that the timing of the end-phase of the knee-flexor ENG burst is correlated with the timing of the start-phase of the knee-extensor ENG burst during fictive rostral scratch. A later section describes our use of start-phase timing of knee-extensor ENGs to assist in the identification of candidate knee-related interneurons (Stein and Daniels-McQueen 2003;Stein et al 2016).…”

“…Robertson and Stein (1988) termed this variation an "HR-KF deletion." This variation is now called a "hip-extensor deletion" (Stein 2008;Stein and Daniels-McQueen 2002, 2003Stein et al 1995Stein et al , 1998Stein et al , 2016.…”