Mechanical entrainment of fictive locomotion in the decerebrate cat

Abstract

1. We examined the ability of muscular and joint afferents from the hip region to entrain fictive locomotion evoked by stimulation of the mesencephalic locomotor region in the decerebrate cat by mechanically imposed, sinusoidal hip flexion and extension movements. 2. A method is presented for qualitative and quantitative analysis of entrainment. 3. Hip joint capsular afferents were shown by denervation experiments to be unnecessary for mediating locomotor entrainment. 4. As the population of muscular afferents was progressively decreased by selective denervation, the strength of entrainment concomitantly decreased, even though a few as two small intrinsic hip muscles were still effective in producing entrainment. The ability to entrain locomotion was abolished with complete ipsilateral denervation. 5. Entrainment was observed with low amplitude hip angular displacement of 5-20 degrees, which would be expected to activate low-threshold, stretch-sensitive muscle afferents. 6. The extensor burst activity occurred during the period of imposed hip flexion, which corresponded to passive stretching and loading of the extensor muscles, while the flexor burst activity occurred during the latter portion of the imposed hip extension, which corresponded to passive stretching of the flexor muscles (when attached) and release of the extensors. During harmonic entrainment, the match of hip cycle duration and step cycle duration was accomplished by a variation in extensor electroneurogram (ENG) burst duration. These results are consistent with a positive feedback mechanism where low-threshold afferent activity from the extensor musculature is used by the rhythm generator to prolong the extension phase of locomotion. 7. A hip cycle frequency-dependent phase shift of ENG activity was observed. This may indicate that the locomotor rhythm generator is dependent on more than just static positional or threshold load information for modulation of the step cycle frequency and switching between flexion and extension phases. 8. Subharmonic forms of entrainment were observed when the number of innervated muscles was markedly reduced. The occurrence of subharmonic entrainment characterizes the locomotor rhythm generator as a nonlinear oscillator. 9. To modulate the stepping frequency, the afferent pathways responsible for entrainment must be directly connected to the neural circuitry responsible for rhythm generation. The rhythm generating interneurons must receive a high degree of convergence from afferents arising from a variety of muscles spanning the hip joint.

Organization of mammalian locomotor rhythm and pattern generation

“…Such an organization was suggested to explain the independence between changes in burst duration and cycle timing during paw shake (Koshland and Smith, 1989;Stein and Smith 1997). A similar separation of CPG function was suggested to explain how sensory stimulation could alter locomotor cycle timing without altering the level of motoneuron activity (Kriellaars et al, 1994). In the latter scheme the CPG was divided into a half-center rhythm generator and "reciprocity modules" each of which was responsible for the depolarization and hyperpolarization of subsets of motoneurons (Jordan, 1991).…”

“…Finally, a regulatory scheme affecting synaptic transmission would have difficulty accounting for the independent control of rhythm and motoneuron recruitment. The rhythm can be slowed or accelerated by sensory stimulation without altering the level of motoneuron activity (e.g., Kriellaars et al, 1994) and motoneuron activation can be altered without affecting cycle timing Guertin et al, 1995;Stecina et al, 2005) As discussed below, a two-level CPG can explain both the sensory control of locomotion and the occurrence of resetting and nonresetting deletions. …”

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

“…Little is known of the mechanisms of speed control in mammals (Kriellaars et al, 1994;Orlovsky and Shik, 1976). Recently, however, studies in newborn mice revealed that the cycle period of locomotor output lengthened when neurones of V1 lineage were silenced (Fig.…”

Single joint perturbation during gait: Preserved compensatory response pattern in spinal cord injured subjects

“…This perturbation occurred just before the swing-to-stance transition. This appears to be a period when the system is particularly sensitive to information related to afferent input such as hip position (Grillner and Rossignol, 1978;Kriellaars et al, 1994). In young infants (Pang and Yang, 2002) a perturbation applied during the stance phase has the greatest influence on the subsequent step cycle when the perturburbation is timed to occur near the stance-to-swing transition.…”