Developmental plasticity of the rubrospinal tract in the North American opossum

Abstract We have shown previously that rubral axons can grow caudal to a lesion of their pathway at thoracic levels of the spinal cord in the developing opossum, Didelphis virginiana. In the present report we expand on that observation and present evidence which suggests that the critical period for plasticity of the rubrospinal tract ends earlier at cervical than at thoracic levels. In addition, we show that most rubrospinal neurons die as a result of axotomy during early stages of the critical period. The opossum was chosen for study because the development of its rubrospinal tract occurs after birth. In one set of experiments the area containing the rubrospinal tract was lesioned at cervical or thoracic levels and after 30 days or more, retrograde transport techniques were used to determine if rubral axons had grown caudal to the lesion. When the lesions were made at rostral cervical levels between estimated postnatal day 26 and maturity, neurons could not be labeled in the contralateral red nucleus by injections of retrograde markers ipsilateral to the lesion and caudal to it. We were not able to obtain adequate survival after cervical lesions made prior to estimated postnatal day 26. When the lesions were made at mid to caudal thoracic levels between estimated postnatal days 19 and 26, neurons could be labeled in the contralateral red nucleus. When comparable lesions were made at estimated postnatal day 40, there was usually a decrease in the number of labeled neurons, and when they were made at estimated postnatal day 54, none was labeled. In selected cases, operated at estimated postnatal day 19, cell counts provided evidence for loss of neurons in the red nucleus contralateral to the lesion. In orthograde transport experiments performed on animals with thoracic lesions of the rubrospinal tract made between estimated postnatal days 18 and 33, rubral axons could be labeled caudal to the lesion, and they seemed to take the most direct route around it. Although they sometimes assumed abnormal positions caudal to the lesion, rubral axons appeared to reach areas of the gray matter appropriate to them. When lesions were made at estimated postnatal day 54 or in older animals, labeled axons could be traced to the lesion site but not caudal to it. In still other experiments rubrospinal neurons were labeled by caudal thoracic or rostral lumbar injections of Fast Blue at estimated postnatal day 26 and 3–4 days later the injected animals were subjected to a lesion of the rubrospinal tract three segments rostral to the injection and ipsilateral to it. They were killed 30–34 days after the lesion so that the red nucleus contralateral to it could be examined for labeled neurons. The results showed that only a few rubrospinal neurons survived axotomy, suggesting that the growth of new axons around the lesion is a major factor in plasticity.