Formation of new synapses in the cat motor cortex following lesions of the deep cerebellar nuclei.

The effects of unilateral lesions of the deep cerebellar nuclei on the corticocortical (CC) projection from the somatosensory to the motor cortex were studied in adult cats, utilizing electrophysiological and electron microscopical methods. Axon terminals in the motor cortex belonging to CC afferents were labeled by degeneration induced by lesions of the somatosensory cortex; neurons in the motor cortex were labeled by the Golgi/EM method. In each cat, data from the motor cortex (MCx) contralateral (experimental) and ipsilateral (control) to the cerebellar lesion were compared. Cerebellar lesions produced marked motor deficits, which receded gradually and disappeared after 30 to 40 days. Subsequent lesions of the somatosensory cortex (area 2) contralateral to the cerebellar lesions resulted in the reappearance of the cerebellar symptoms. The number of CC synapses per unit area in experimental MCx was significantly higher than in control MCx. The increase in the number of CC synapses was apparent throughout layers II-V of the MCx, but was most prominent in layers II/III. The increase in the number of CC synapses in experimental MCx was due mainly to an increase of axon terminals synapsing with dendritic spines belonging to pyramidal neurons. In comparison, the numbers and spatial distribution of CC synapses with aspinous, nonpyramidal neurons from both experimental and control MCx were similar. Field potentials in the experimental MCx, evoked by stimulation of area 2, were altered following cerebellar lesions. In experimental MCx, the polarity of the early component of the field potentials reversed at cortical depths corresponding to layers II-III, whereas this reversal was not observed in control MCx. These findings suggest that lesions of the cerebellar nuclei induced sprouting of axon terminals in the MCx to establish a new function. The results provide the first anatomical evidence for the generation of new synapses in the adult CNS which is not induced by elimination of existing synapses.