Deletions of Rhythmic Motoneuron Activity During Fictive Locomotion and Scratch Provide Clues to the Organization of the Mammalian Central Pattern Generator

Abstract

We examined the features of spontaneous deletions of bursts of motoneuron activity that can occur within otherwise rhythmic alternating flexor and extensor activity during fictive locomotion and scratch in adult decerebrate cats. Deletions of activity were observed both in hindlimb flexor and extensor motoneuron pools during brain stem-stimulation-evoked fictive locomotion but only in extensors during fictive scratch. Paired intracellular motoneuron recordings showed that deletions reduced the depolarization of homonymous motoneurons in qualitatively similar ways. Differences occurred in the extent to which activity in synergist motoneuron pools operating at other joints within the limb was reduced during deletions. The timing of the rhythmic activity that followed a deletion was often at an integer multiple of the preexisting locomotor or scratch cycle period. This maintenance of cycle period was also seen during deletions in which there was a complete failure of motoneuron depolarization. The activity of antagonist motoneurons was usually sustained during deletions with some rhythmic modulation at intervals of the preexisting cycle period. We discuss an organization of the central pattern generator for locomotion and scratch that functions as a single rhythm generator with separate and multiple pattern formation modules for controlling the hyper- and depolarization of subsets of motoneurons within the limb.

Organization of mammalian locomotor rhythm and pattern generation

“…A similar conclusion about separation of rhythm and motoneuron activation duties arose from intracellular studies of deletions of scratch reflex activity in the turtle (Robertson and Stein, 1988). Our observations on deletions and on the ability of sensory stimulation to alter phase switching within the ongoing step cycle without changing the phase of the post stimulation rhythm (e.g., Guertin et al, 1995;Perreault et al, 1995;Stecina et al, 2005) led to the proposal for a two-level CPG (Lafreniere-Roula and McCrea, 2005;Rybak et al, 2006a). It was recently suggested that a single-level CPG could produce non-resetting deletions if there were a powerful control mechanism that could regulate synaptic transmission between excitatory CPG interneurons and motoneurons (Kiehn, 2006).…”

“…1F) all of the last order interneurons exciting motoneurons receive sensory input. Accordingly, this might be considered a three-level CPG organization.Our studies had shown that non-resetting deletions were quite common during fictive locomotion and scratch in the decerebrate cat (Lafreniere-Roula and McCrea, 2005). The simple explanation was that some circuitry separate from that involved in rhythm generation was responsible for the rhythmic depolarization and hyperpolarization of motoneurons.…”

Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis

“…2; Lafreniere-Roula and McCrea, 2005;Rybak et al, 2006a,b andRybak, 2008;see Kiehn, 2006 for additional discussion on this point). Although there is much evidence that the last-order, pattern-forming circuitry is organised in half-centre modules (see above), there is little evidence that the rhythm-generating layer follows suit.…”

“…While McCrea and colleagues present some compelling evidence in support of a two-layer model, their evidence that the rhythm-generating layer is organised as half-centres is much less convincing. These investigators rely on spontaneous (Lafreniere-Roula and McCrea, 2005;Rybak et al, 2006a) or evoked (Rybak et al, 2006b) "deletions" of activity in single motor nerves that either are ("resetting" deletions) or are not ("non-resetting" deletions) associated with disruptions of rhythm. They reason that since these non-resetting deletions can be seen in either flexor or extensor muscle nerves, the rhythm-generating layer must excite both the flexor and extensor pattern formation half-centres.…”

“…The difficulty arises from our inability to define the neurones involved in rhythmogenesis, and from the fact that our models rely on data obtained from motoneuronal recordings, which are likely disynaptically "removed" from the neurones involved in rhythm generation. Evidence has been presented in favour of (Duysens, 1977) and opposed to (Lafreniere-Roula and McCrea, 2005) the concept that this is an asymmetric network. This topic has recently been discussed in an exchange of letters to the editor in the Journal of Neurophysiology (Duysens, 2006).…”