Reference Frames for Spinal Proprioception: Limb Endpoint Based or Joint-Level Based?

Abstract

Many sensorimotor neurons in the CNS encode global parameters of limb movement and posture rather than specific muscle or joint parameters. Our investigations of spinocerebellar activity have demonstrated that these second-order spinal neurons also may encode proprioceptive information in a limb-based rather than joint-based reference frame. However, our finding that each foot position was determined by a unique combination of joint angles in the passive limb made it difficult to distinguish unequivocally between a limb-based and a joint-based representation. In this study, we decoupled foot position from limb geometry by applying mechanical constraints to individual hindlimb joints in anesthetized cats. We quantified the effect of the joint constraints on limb geometry by analyzing joint-angle covariance in the free and constrained conditions. One type of constraint, a rigid constraint of the knee angle, both changed the covariance pattern and significantly reduced the strength of joint-angle covariance. The other type, an elastic constraint of the ankle angle, changed only the covariance pattern and not its overall strength. We studied the effect of these constraints on the activity in 70 dorsal spinocerebellar tract (DSCT) neurons using a multivariate regression model, with limb axis length and orientation as predictors of neuronal activity. This model also included an experimental condition indicator variable that allowed significant intercept or slope changes in the relationships between foot position parameters and neuronal activity to be determined across conditions. The result of this analysis was that the spatial tuning of 37/70 neurons (53%) was unaffected by the constraints, suggesting that they were somehow able to signal foot position independently from the specific joint angles. We also investigated the extent to which cell activity represented individual joint angles by means of a regression model based on a linear combination of joint angles. A backward elimination of the insignificant predictors determined the set of independent joint angles that best described the neuronal activity for each experimental condition. Finally, by comparing the results of these two approaches, we could determine whether a DSCT neuron represented foot position, specific joint angles, or none of these variables consistently. We found that 10/70 neurons (14%) represented one or more specific joint-angles. The activity of another 27 neurons (39%) was significantly affected by limb geometry changes, but 33 neurons (47%) consistently elaborated a foot position representation in the coordinates of the limb axis.

Running over rough terrain reveals limb control for intrinsic stability

“…Further, these synergies can correspond to task-level biomechanical functions such as endpoint force or kinematics (18,36). Muscle synergies are encoded at the level of the spinal cord (37) and may integrate proprioceptive signals into whole-limb information, such as limb length and orientation (38). Similar muscle synergies may exist for running and control parameters such as limb retraction, limb length, and k leg ; thereby reducing the complex pattern of muscle activation to a few modules.…”

Cerebellar Contributions to Locomotor Adaptations during Splitbelt Treadmill Walking

“…Error information from sensorimotor feedback is presumed to drive alterations of and continuously update this representation (Ito, 1989(Ito, , 2000Kawato and Gomi, 1992;Imamizu et al, 2000). In the cat, mossy fiber projections from dorsal or ventral spinocerebellar tracts provide the cerebellum with the necessary feedback in several forms, including proprioceptive primary afferents (Lundberg and Oscarsson, 1956;Lundberg and Winsbury, 1960;Eccles et al, 1961) and information integrated across multiple joints of the leg, which may formulate an estimate of the foot endpoint location (Bosco and Poppele, 1997;Bosco et al, 2000). Some feedback is also integrated across both hindlimbs to provide a single cerebellar hemisphere with bilateral limb orientation information, which could be critical for adapting interlimb coordination (Poppele et al, 2003).…”

Development of a kinematic coordination pattern in toddler locomotion: planar covariation

“…Because the degrees of freedom of angular motion of lower limb segments in the sagittal plane are reduced to two by the planar constraint, they match the corresponding degrees of freedom of motion of the foot. Any deviation of foot position from the desired path could be compensated by monitoring a mismatch between an endpoint-related signal and a segment angle-related signal, which could be used to reestablish the appropriate angular covariation (Bosco et al 2000). Recent findings on the functional organization of both sensory systems, such as the dorsal spinocerebellar tract (Bosco and Poppele 1993;Bosco et al 2000), and the primary motor cortex (Kakei et al 1999;Scott and Kalaska 1997) indicate how this could be accomplished.…”

“…The tuning function of another set of neurons instead is affected by the pattern of limb geometry and muscle activity. Bosco et al (2000) have proposed how the spinocerebellar system could help regulating the joint-angle covariance. They argued that if each endpoint-related spinocerebellar cell was matched with a corresponding joint-angle cell that has a congruent endpoint-related activity, then as long as their activities remained congruent, it would indicate a consistent relationship between endpoint and joint-angle covariance.…”

“…Instead, any mismatch in their respective discharges would signal a deviation from the desired joint-angle covariance. The cerebellum, that receives these inputs, could detect the mismatches of signals and could initiate appropriate control actions aimed at reestablishing the desired joint-angle covariance (Bosco et al 2000). Therefore, one may speculate that the developmental changes of the joint-angle covariance plane also reflect the developmental changes of cerebellar control of gait and posture.…”