Time course of functional changes in locomotor and sensory systems after spinal cord lesions in lamprey

Abstract

Changes in motor and sensory properties occur either side of spinal cord lesion sites from lower vertebrates to humans. We have previously examined these changes in the lamprey, a model system for studying recovery after spinal cord injury. These analyses were performed 8–12 wk after complete spinal cord lesions, a time when most animals have recovered good locomotor function. However, anatomical analyses have been performed at earlier and later times than this. Because there have been no functional studies at these times, in this study we have examined changes between 2 and 24+ wk after lesioning. Functional changes developed at different times in different regions of the spinal cord. Spinal cord excitability was significantly reduced above and below the lesion site less than 6 wk after lesioning but showed variable region-specific changes at later times. Excitatory synaptic inputs to motor neurons were increased above the lesion site during the recovery phase (2–8 wk after lesioning) but only increased below the lesion site once recovery had occurred (8 wk and later). These synaptic effects were associated with lesion-induced changes in connectivity between premotor excitatory interneurons. Sensory inputs were potentiated at 8 wk and later after lesioning but were markedly reduced at earlier times. There are thus time- and region-specific changes in motor and sensory properties above and below the lesion site. Although animals typically recover good locomotor function by 8 wk, there were further changes at 24+ wk. With the assumption that these changes can help to compensate for the reduced descending input to the spinal cord, effects at later times may reflect ongoing modifications as regeneration continues. NEW & NOTEWORTHY The lamprey is a model system for studying functional recovery and regeneration after spinal cord injury. We show that changes in spinal cord excitability and sensory inputs develop at different times above and below the lesion site during recovery. These changes may occur in response to the lesion-induced removal of descending inputs and may subsequently help to compensate for the reduction of the descending drive to allow locomotor recovery. Changes also continue once animals have recovered locomotor function, potentially reflecting adaptations to further regeneration at later recovery times.