Emergence of Deletions during Treadmill Locomotion as a Function of Supraspinal and Sensory Inputs

Abstract

During locomotion, alternating activity of flexor and extensor muscles is largely regulated by a spinal neuronal network, the central pattern generator, the activity of which is modulated by peripheral and supraspinal inputs. In the absence of these modulatory inputs, for example during fictive locomotion after spinalization and curarization, spontaneous failures of motor activation (deletions) in a muscle can occur without perturbing the rhythmic cycle structure of the antagonists on the same side or the contralateral side. This suggests that the central pattern generator can maintain the locomotor period when motoneuron discharges fail in a given pool of motoneurons. Here we first examined whether such deletions could occur during real locomotion on a treadmill and determined their consequences on the overt locomotor pattern. We also evaluated the role of supraspinal and sensory inputs in modulating the occurrence of failures of rhythmic activity by comparing the same cats in the intact state, then after a partial spinal cord injury (SCI), and finally after a complete SCI at different treadmill speeds. We showed that deletions: (1) are absent in intact animals and occur only after SCI; (2) affect only flexor muscle activity; (3) neither perturb the timing of rhythmic activity of these muscles in subsequent cycles nor interfere with the timing of the ipsilateral and contralateral agonists and antagonists; (4) do not affect significantly the locomotor pattern kinematics; and (5) are sensitive to treadmill speed and lesion severity, suggesting a role for sensory and supraspinal inputs in stabilizing rhythmic output activity.

Effect of Hindlimb Unloading on Hamstring Muscle Activity in Rats

“…The non-resetting (not leading to a premature new step) deletions of the BFp flexor burst activity accompanied by the increase of the ST flexor burst activity in the first steps may also reflect changes in supraspinal control after HU. It is worth noting that such non-resetting deletions were never observed previously in intact animals; rather, they were found in some flexors after spinal cord injuries in cats, proposedly due to altered supraspinal control [39]. The maintenance of locomotor rhythm despite such deletions strongly supports the hypothesis of multilevel organization of the central pattern generator [40].…”

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

“…Studies of deletions provide support for hypotheses of multipartite modular organization of spinal CPGs (Britz et al 2015;Duysens 1977;Griener et al 2013;Grillner and Zangger 1979;Lafreniere-Roula and McCrea 2005;Markin et al 2012;Martinez et al 2013;McCrea and Rybak 2008;Rybak et al 2006;Stein 2005Stein , 2008Stein , 2010Daniels-McQueen 2002, 2004;Turkin and Hamm 2004;Zhong et al 2012). In the spinal turtle, the motor patterns of the normal rostral scratch and the hip-extensor deletion variation of the rostral scratch have been extensively studied (Robertson and Stein 1988;Stein 2005Stein , 2008Stein , 2010Stein et al 1982Stein et al , 1995Stein et al , 1998Stein and Daniels-McQueen 2002, 2003Stein and Grossman 1980).…”

Lumbar multiunit activity power spectrum during air stepping in the spinal cat: evidence for a flexor-dominated rostrocaudally distributed locomotor center

“…The two-level model of the central pattern generator proposed by McCrea and Rybak ( 19 ) was formulated to explain gaps in the half-center hypothesis such as bifunctional muscle activation patterns and nonresetting deletions, whereby motor neuron activity disappears, but flexor and extensor timing is maintained upon the reappearance of the rhythm ( 20 , 21 ). The first level is described by two excitatory rhythm-generating subunits that set the phasic information for extensor and flexor premotor populations through mutual inhibition between the subunits, the “half-center” model.…”