Spatiotemporal Maps of Proprioceptive Inputs to the Cervical Spinal Cord During Three-Dimensional Reaching and Grasping

Abstract

<jats:title>Abstract</jats:title><jats:p>Proprioceptive feedback is a critical component of voluntary movement planning and execution. Neuroprosthetic technologies aiming at restoring movement must interact with it to restore accurate motor control. Optimization and design of such technologies depends on the availability of quantitative insights into the neural dynamics of proprioceptive afferents during functional movements. However, recording proprioceptive neural activity during unconstrained movements in clinically relevant animal models presents formidable challenges. In this work, we developed a computational framework to estimate the spatiotemporal patterns of proprioceptive inputs to the cervical spinal cord during three-dimensional arm movements in monkeys. We extended a biomechanical model of the monkey arm with ex-vivo measurements, and combined it with models of mammalian group-Ia, Ib and II afferent fibers. We then used experimental recordings of arm kinematics and muscle activity of two monkeys performing a reaching and grasping task to estimate muscle stretches and forces with computational biomechanics. Finally, we projected the simulated proprioceptive firing rates onto the cervical spinal roots, thus obtaining spatiotemporal maps of spinal proprioceptive inputs during voluntary movements. Estimated maps show complex and markedly distinct patterns of neural activity for each of the fiber populations spanning the spinal cord rostro-caudally. Our results indicate that reproducing the proprioceptive information flow to the cervical spinal cord requires complex spatio-temporal modulation of each spinal root. Our model can support the design of neuroprosthetic technologies as well as in-silico investigations of the primate sensorimotor system.</jats:p>

Contrasting action and posture coding with hierarchical deep neural network models of proprioception

“…For various anatomical and experimental reasons, recording proprioceptive activity during natural movements is technically challenging (3, 47). Furthermore, “presenting” particular proprioceptive-only stimuli is difficult, which poses substantial challenges for systems identification approaches.…”

“…While we used spindle Ia and II models, it is known that multiple receptors, namely cutaneous, joint, and muscle receptors play a role for limb localization and kinesthesia (3, 55–58). For instance, a recent simulation study by Kibleur et al highlighted the complex spatio-temporal structure of proprioceptive information at the level of the cervical spinal cord (47). Furthermore, due to fusimotor drive receptor activity can be modulated by other modalities, e.g., vision (59).…”

“…How-ever it is known that multiple receptors, namely cutaneous, joint, and muscle receptors play a role for limb localization and kinesthesia (3,(53)(54)(55)(56). For instance, a recent simulation study by Kibleur et al highlighted the complex spatiotemporal structure of proprioceptive information at the level of the cervical spinal cord (42). In the future, models for slow-adapting type II afferents, golgi tendon organ as well as cutaneous receptors can be added, to study their role in the context of various tasks.…”

Neural population dynamics reveals disruption of spinal circuits’ responses to proprioceptive input during electrical stimulation of sensory afferents

“… 8 , 25 , 29 Therefore, cutaneous afferents are recruited concurrently, along with larger-diameter afferents. 30 These fibers converge on interneurons in the spinal cord, where they undergo the first layer of sensory processing, representing a highly shared sensory network node.…”

Neural population dynamics reveals disruption of spinal sensorimotor computations during electrical stimulation of sensory afferents

“…In consequence, since fibers of different diameters are densely packed within nerve fascicles, practical implementation of electrical neurostimulation systems would always result, at least partially, in the recruitment of mixed diameter fiber distributions, hence, different sensory modalities 28,32,33 . Therefore, cutaneous receptors are recruited concurrently to larger diameter afferents such as golgi (Ib) and spindle (Ia) afferents 34 . These fibers converge to interneurons in the spinal cord where they undergo the first layer of sensory processing, and project to the gracilis (lower limb) or cuneate (upper limb) nuclei in the medulla oblungata, thalamus and then cortex 35 .…”