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We have studied the locomotor development of kittens that received complete low thoracic spinal cord transections and embryonic spinal cord transplants as newborns. Embryonic spinal cord (E21-E26) transplanted into the site of a transection integrated well with the host spinal cord and promoted the development of overground locomotion. Spinalized kittens with transplants were first distinguished from spinalized kittens during the 2nd and 3rd postnatal weeks when kittens with transplants positioned their hindlimbs underneath their bodies which promoted support of the hindquarters. By postnatal Week 6, kittens with transplants exhibited overground locomotion characterized by full weight support and moderate balance control. By 20 weeks of age, as many as 96% of the step cycles showed full weight support and as few as 2% of the step cycles were interrupted by a fall. Most kittens also showed coordination between the forelimbs and the hindlimbs. They differed from normal in the precocious onset of reflex stepping and in the less precise interlimb coordination and more precarious balance during overground locomotion. The overground locomotor performance of kittens with transplants greatly exceeded that of spinal kittens without transplants since few spinalized kittens showed any full-weight-supported step cycles and none showed coordination between the forelimbs and the hindlimbs. In the absence of a transplant, no fibers could grow across the lesion site. In the presence of a transplant, fibers grew across the lesion site and established anatomical connectivity with the host. Host segmental systems identified by the presence of calcitonin gene-related peptide- and substance P-immunoreactive fibers were found throughout the transplants. Descending host systems of supraspinal origin were identified by serotonin- and dopamine beta-hydroxylase-immunoreactive fibers throughout the transplants. The growth of supraspinal axons into the transplant, and in one case into the caudal host spinal cord, provided a possible anatomical basis for the development of coordinated overground locomotion.

The development of bipedal treadmill locomotion and overground locomotion has previously been studied in the kitten; the development of quadrupedal treadmill locomotion has not. We evaluated and compared all three forms of locomotion in the normal kitten and present quantitative data comparing the development of quadrupedal treadmill and overground locomotion. Overground locomotion was studied from the day of birth to 5 months of age and quadrupedal treadmill locomotion was studied in the same animals from 9 weeks to 5 months of age. Treadmill locomotion was initiated postweaning, since it could not be reliably elicited without a food reward. Three locomotor characteristics (weight support, balance, and coordination between the forelimbs and the hindlimbs) were evaluated quantitatively. Kittens first consistently demonstrated overground steps with the ventral surface of their bodies supported above the walking surface throughout the entire step cycle during the second and third postnatal weeks. By 4 weeks of age, overground locomotion consistently showed full weight support and midline positioning of the hindquarters. Coordination between the forelimbs and the hindlimbs developed differently in the two forms of quadrupedal locomotion evaluated. During overground locomotion, the kittens initially used a single pattern in which only one limb was in swing at any time. As the kittens' weight support and trunk control improved, additional swing phase coordination patterns emerged and these patterns were correlated with the animals' ability to change speeds during locomotion. The consistency with which a dominant interlimb swing phase pattern was used at a particular speed increased with age and, by 6 weeks, the frequency of each speed-related dominant pattern approached 100% during overground locomotion. At 6 weeks, interlimb coordination also was evident in the nearly consistent interlimb phase interval present between the forelimb's initiation of the first extension subphase and the ipsilateral hindlimb's initiation of the flexion phase. The consistent patterns appeared to be fostered by maturation of weight support and balance. In contrast, the interlimb phase interval was inconsistent during quadrupedal treadmill locomotion until 20 weeks of age. Moreover, the interlimb swing phase patterns used during quadrupedal treadmill locomotion differed from those used during overground locomotion. The differences in the developmental time course and patterns of interlimb coordination between overground and quadrupedal treadmill locomotion suggest that different mechanisms regulate the control of interlimb coordination during these two different forms of quadrupedal locomotion.

This study was undertaken to determine the locomotor capability of kittens whose spinal cords were transected at birth. The postnatal development of reflex and goal-directed locomotion was examined during the first 5 postnatal months in kittens that received low thoracic spinal cord transections as newborns. Some spinal kittens developed aberrant quadrupedal forms of locomotion. The onset of quadrupedal locomotion, however, was delayed by 2-3 months compared to the normal kitten (42) and deteriorated by 5 months of age. Qualitative and quantitative analyses demonstrated that the quadrupedal locomotion was abnormal. Although some step cycles were characterized by full weight support, the typical hindlimb step cycle of the best performing cat showed inadequate weight support and balance. No spinal cat was able to coordinate the hindlimbs with the forelimbs during overground locomotion on a runaway or during quadrupedal locomotion on a treadmill. Neuroanatomical tracing with WGA-HRP and immunocytochemical techniques showed no axonal regeneration or growth into or across the lesion sites. The aberrant form of quadrupedal locomotion developed without descending input to the caudal spinal cord. The variability in performance among animals suggested that compensatory strategies were important factors in the spinal kitten's achievement of quadrupedal locomotion. Hindlimb weight-supported stepping during quadrupedal locomotion in some animals underscored the capacity of the isolated caudal spinal cord to generate both rhythmical stepping movements and weight support. The maintenance of developmentally immature, but functional, hindlimb postures suggested that the development of the isolated caudal spinal cord was arrested in the absence of descending input.