A trans-spinal loop between neurones in the reticular formation and in the cerebellum

Non-technical summary Voluntary limb movements are initiated in the brain but the neurones responsible for activating the muscles (motoneurones and interneurones) are located in the spinal cord. The spinal cord also contains neurones that provide the brain, and especially the cerebellum, with continuous information on effects of the descending commands. We show that one population of such neurones provide the cerebellum with information on how likely the brain's commands (mediated by descending reticulospinal neurones) are to be executed as planned, depending on the degree of inhibition of motoneurones. They may therefore play an important role in preventing errors in activation of motoneurones and thereby help the brain to correct its signals to the spinal cord before such errors have been committed.The study aimed to investigate the role that four populations of spinocerebellar neurones play in forwarding information on descending commands relayed by feline reticulospinal neurones. Both intracellular and extracellular recording was used from medially located ventral spinocerebellar tract (VSCT) neurones as well as from spinal border (SB) subpopulation of VSCT neurones and from dorsal spinocerebellar tract neurones located in Clarke's column (CC DSCT) and in the dorsal horn (dh DSCT) in the lumbosacral enlargement. Axons of reticulospinal neurones were stimulated within the ipsilateral and contralateral medial longitudinal fascicle (MLF). We found striking differences in synaptic input from reticulospinal neurones to these four populations of spinocerebellar neurones. Both monosynaptic and disynaptic excitatory input was found in VSCT and SB neurones, only disynaptic in CC DSCT neurones and none in dh DSCT neurones. Discharges of VSCT and SB neurones were potently modulated by inhibitory actions of group I and II afferents. Following application of single stimuli to peripheral nerves these neurones ceased to respond for about 5 ms and thereafter discharged at a lower incidence rate. As inhibition of spinocerebellar neurones and of alpha-motoneurones is evoked by the same premotor interneurones, VSCT neurones may provide the cerebellum with information on the likely outcome of reticulospinal actions on motoneurones depending on the degree to which they are inhibited. They may thereby enable the cerebellum to adjust descending commands relayed by reticulospinal neurones to the requirements of a given situation and thus prevent errors in the centrally initiated movements.