Stimulation of a Restricted Region in the Midline Cerebellar White Matter Evokes Coordinated Quadrupedal Locomotion in the Decerebrate Cat

Abstract

In the reflexively standing acute decerebrate cat, we have previously shown that pulse train microstimulation of the hook bundle of Russel in the midline of the cerebellar white matter, through which crossed fastigiofugal fibers decussate, augments the postural tone of neck, trunk, fore-, and hindlimb extensor muscles. In the present study we examined the possible role of such stimulation in evoking locomotion as the animal is supported by a rubber hammock with its feet contacting the moving surface of a treadmill. We were able to provoke well-coordinated, bilaterally symmetrical, fore- and hindlimb movements, whose cycle time and pattern were controlled by appropriate changes in stimulus intensity and treadmill speed. We carefully and systematically mapped this cerebellar locomotor region (CLR) through repeated dorsoventral penetrations with a glass-coated tungsten microelectrode in a single animal and between animals. We found that the optimal locus for evoking locomotion was centered on the midline, at Horsley-Clarke coordinates H0 and P7.0, and extended over a rostrocaudal and dorsolateral range of approximately 0.5 mm. The lowest effective stimulus intensity at the optimal site was in the range of 5-8 microA. Along penetration tracks to left or right of the midline, effective stimulus intensity increased and evoked locomotor patterns were no longer symmetrical, but rather shifted toward the contralateral limbs. In the same animals, controlled locomotion was evoked by stimulating the mesencephalic locomotor region (MLR). With concomitant stimulation of the optimal sites in the CLR and the MLR, each at subthreshold strength, locomotor movements identical to those seen with suprathreshold stimulation of each site alone were evoked. With concomitant stimulation at suprathreshold strength for each site, locomotion became vigorous, with a shortened cycle time. After making ablative lesions at either the CLR or MLR (unilateral or bilateral), controlled locomotion was still evoked at the prior stimulus strength by stimulating the remaining site. Together, these results demonstrate that selective stimulation of the hook bundle of Russel in the midsagittal plane of the cerebellar white matter evokes "controlled" locomotion identical to that evoked by stimulating the MLR. We have shown that the fastigial nucleus is one of the supraspinal locomotion inducing sites and that it can independently and simultaneously trigger brain stem and spinal locomotor subprograms formerly believed to be the domain of various brain stem regions including the MLR and the subthalamic locomotor region.

Coordination of the Bladder Detrusor and the External Urethral Sphincter in a Rat Model of Spinal Cord Injury: Effect of Injury Severity

“…Importantly, most of these animals did not recover weightbearing locomotion, as measured by the BBB (Fig. 1 B), which is believed to require supraspinal control (Grillner and Dubuc, 1988;Mori et al, 1999). In contrast, the 12.5 mm SCI group recovered coordinated weight-bearing locomotion (Fig.…”

“…1 B, BBB) showed significant differences between the 12.5 mm group, which attained weight-bearing locomotion, and the 25 and 50 mm groups, which on average did not. This is an important distinction, because voluntary overground locomotion with full weight support requires supraspinal control (Grillner and Dubuc, 1988;Mori et al, 1999).…”

On the Role of the Pedunculopontine Nucleus and Mesencephalic Reticular Formation in Locomotion in Nonhuman Primates

“…Indeed, in primate, the spino-mesencephalic tractus and part of the spinoreticular tractus were found to reach different sites in the brainstem, including the caudal mesencephalon (Wiberg et al, 1987;Yezierski, 1988;Craig, 1995). Another origin of this passive response could be related to the close proximity with the SCP (Hazrati and Parent, 1992), which conveys information from the deep cerebellar nuclei, which is considered to be another locomotor center (Mori et al, 1999). The SCP also contains the ventral spino-cerebellar tractus thought to convey information about premotoneuronal activity in the cord.…”

Molecular, Topographic, and Functional Organization of the Cerebellar Nuclei: Analysis by Three-Dimensional Mapping of the Olivonuclear Projection and Aldolase C Labeling

“…That is, each compartment identified in the CN is proposed to be involved in the same function that has been proposed for its corresponding olivocerebellar group. To give an example, different functions such as control of locomotion (Mori et al, 1999), saccade and other eye movements (Ohtsuka and Noda, 1991), and posture and head orientation (Wilden et al, 2002) have been reported in the FN. The subdivisions of the FN into the rostrodorsal aldolase C-negative part (group III-spinal), centrodorsocaudal part (group IIb-collicular), and centrocaudal part (group IIa-vestibular) in the present study may be directly related to the above functions (locomotion, eye movements, and head orientation).…”