Identification of a critical period for motor development in neonatal rats

Abstract

Manipulation of the developing nervous system has provided valuable insights into nervous system function. One important concept to arise from this type of study has been the identification of specific “critical periods” for the development of various functions. A critical period has been most clearly shown for the visual system where monocular eye closure for a few weeks led to functionally significant changes in visually guided behaviors and the connectivity of the visual cortex. 11,25 Critical periods have also been defined for other sensory systems.13,20 Although studies of the effect of manipulating sensory systems during development are sometimes difficult to interpret (e.g. Ref. 7), this difficulty is compounded in the case of the motor system. Problems arise because manipulations of the postnatal motor system are difficult to implement and usually require invasive procedures such as tenotomy,4,10 neurotomy,1,6,21 and nerve crush 15,16 review, see Ref. 17). We have approached the problem of manipulating the motor environment by adapting a paradigm widely used to study the experimental effects of simulated weightlessness in adult rats: namely, tail suspension. 8 This method has several advantages for manipulating the motor system: (i) because it is noninvasive, it is less discomforting than neurotomy, tenotomy or nerve crush; (ii) it does not immobilize the animals, they move about the cage and extend and flex their hindlimbs; and (iii) it specifically examines the importance of load-bearing on the development of antigravity muscles and their neuronal circuits. Following this non-invasive procedure motor performance is significantly impaired after only one day of suspension; the severity and duration of impairment is related to the age at which the animals are suspended and the length of suspenson. Using swimming and walking as measures of motor performance we have found the five-day-period extending from postnatal days 8–13 to be a “critical period” during which animals are most sensitive to hindlimb unloading. Animals suspended on postnatal day 8 cannot swim by postnatal day 11. Equally dramatic results were found in animals suspended from postnatal days 13–31 in which abnormal walking patterns remained into adulthood (postnatal day 76); i.e. the effects of tail suspension on motor development are apparently permanent.