Direct and indirect spino-cerebellar pathways: shared ideas but different functions in motor control

Abstract

The impressive precision of mammalian limb movements relies on internal feedback pathways that convey information about ongoing motor output to cerebellar circuits. The spino-cerebellar tracts (SCT) in the cervical, thoracic and lumbar spinal cord have long been considered canonical neural substrates for the conveyance of internal feedback signals. Here we consider the distinct features of an indirect spino-cerebellar route, via the brainstem lateral reticular nucleus (LRN), and the implications of this pre-cerebellar “detour” for the execution and evolution of limb motor control. Both direct and indirect spino-cerebellar pathways signal spinal interneuronal activity to the cerebellum during movements, but evidence suggests that direct SCT neurons are mainly modulated by rhythmic activity, whereas the LRN also receives information from systems active during postural adjustment, reaching and grasping. Thus, while direct and indirect spino-cerebellar circuits can both be regarded as internal copy pathways, it seems likely that the direct system is principally dedicated to rhythmic motor acts like locomotion, while the indirect system also provides a means of pre-cerebellar integration relevant to the execution and coordination of dexterous limb movements.

Graded Arrays of Spinal and Supraspinal V2a Interneuron Subtypes Underlie Forelimb and Hindlimb Motor Control

“…Type I V2a interneurons, enriched in lumbar segments, lack brainstem projections and synapse onto other ventral interneurons (vIN connections simplified in this schematic). Type II V2a interneurons, enriched in cervical segments, project to supraspinal structures, likely sending motor efference copies to the lateral reticular nucleus (LRN), which indirectly feeds back into the spinal cord through descending cortical and reticular tracts among other descending tracts (Alstermark et al, 2007;Jiang et al, 2015). Motor neurons are segmentally organized into columns and pools (gray), whereas V2a IN subtypes are distributed along the spinal cord.…”

Neuronal activity and outcomes from thalamic surgery for spinocerebellar ataxia

“…The sensory information on coordination is conveyed to the cerebellum through the direct and indirect spinocerebellar tracts and may have a differential effect on movement and posture. 49 The spinocerebellar tracts are also involved in providing sensory feedback during movement. 13 Purkinje cells receive afferent fibers originating from the brainstem and spinal cord 11,43 and project to the deep cerebellar nuclei and receive excitatory collateral inputs from mossy and climbing fibers.…”

Structure of long-range direct and indirect spinocerebellar pathways as well as local spinal circuits mediating proprioception

“…When proprioception is lost, gross trajectories are maintained, but coordinated limb movement is impaired (Gordon et al, 1995;Abelew et al, 2000;Windhorst, 2007;Akay et al, 2014). Muscle and tendon information detected by proprioceptive sensory neurons, and touch information detected by cutaneous afferents in the periphery, are integrated by secondary neurons in the spinal cord and relayed to the cerebellum through both direct and indirect spinocerebellar pathways (Oscarsson, 1965;Bosco and Poppele, 2001;Jiang et al, 2015). How these direct and indirect pathways either converge or diverge in the cerebellum and what kind of differential information is processed through these pathways is unclear.…”

“…In addition, anatomically, while gross features of the direct spinocerebellar pathways are known, the structural features of axon collateral projections from this pathway are vague. The direct spinocerebellar pathway is known to consist of the ipsilaterally-projecting dorsal and contralaterallyprojecting ventral spinocerebellar tracts (DSCT and VSCT), deriving from several anatomically and molecularly distinct groups of soma in diverse laminae throughout the spinal cord Sengul et al, 2015;Baek et al, 2019) where they are thought to convey ongoing locomotor activity (Jiang et al, 2015). A major contributor to the DSCT comes from CC neurons, whose soma reside in the medial aspect of the thoracic to upper lumbar spinal cord (Oscarsson, 1965;Baek et al, 2019).…”