Local Loss of Proprioception Results in Disruption of Interjoint Coordination During Locomotion in the Cat

Abelew, Thomas A.; Miller, Merry N.; Cope, Timothy C.; Nichols, T. Richard

doi:10.1152/jn.2000.84.5.2709

Cited by 110 publications

(106 citation statements)

References 17 publications

Supporting

Mentioning

101

Contrasting

Order By: Relevance

“…These results demonstrate that the stretch reflex is virtually absent long after a cut nerve reinnervates its original muscle. In addition, the findings are comparable with those from cat (Abelew et al, 2000;Huyghues-Despointes et al, 2003), suggesting that the inability to recover stretch reflexes after nerve section can be generalized across mammalian species.…”

Section: Stretch Reflex Is Virtually Absent In Reinnervated Rat Musclesupporting

confidence: 70%

“…Loss of the stretch reflex, even when restricted to only a few muscles, is associated with deficits in limb movement, including reduction in weight support and loss of interjoint coordination in locomoting cats (Abelew et al, 2000). Loss of sensory feedback from muscle stretch is also likely to result in altered proprioception and in problems with controlling limb position observed in human subjects with large fiber neuropathies (Rothwell et al, 1982;Sainburg et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Central Suppression of Regenerated Proprioceptive Afferents

Haftel¹,

Bichler²,

Wang³

et al. 2005

J. Neurosci.

View full text Add to dashboard Cite

Long after a cut peripheral nerve reinnervates muscle and restores force production in adult cats, the muscle does not respond reflexively to stretch. Motivated by the likelihood that stretch areflexia is related to problems with sensing and controlling limb position after peripheral neuropathies, we sought to determine the underlying mechanism. Electrophysiological and morphological measurements were made in anesthetized rats having one of the nerves to the triceps surae muscles either untreated or cut and immediately rejoined surgically many months earlier. First, it was established that reinnervated muscles failed to generate stretch reflexes, extending observations of areflexia to a second species. Next, multiple elements in the sensorimotor circuit of the stretch reflex were examined in both the PNS and CNS. Encoding of muscle stretch by regenerated proprioceptive afferents was remarkably similar to normal, although we observed some expected abnormalities, e.g., increased length threshold. However, the robust stretch-evoked sensory response that arrived concurrently at the CNS in multiple proprioceptive afferents produced synaptic responses that were either smaller than normal or undetectable. Muscle stretch failed to evoke detectable synaptic responses in 13 of 22 motoneurons, although electrical stimulation generated monosynaptic excitatory postsynaptic potentials that were indistinguishable from normal. The ineffectiveness of muscle stretch was not attributable therefore to dysfunction at synapses made between regenerated Ia afferents and motoneurons. Among multiple candidate mechanisms, we suggest that centrally controlled neural circuits may actively suppress the sensory information encoded by regenerated proprioceptive afferents to prevent recovery of the stretch reflex.

show abstract

Section: Stretch Reflex Is Virtually Absent In Reinnervated Rat Musclesupporting

confidence: 70%

Section: Introductionmentioning

confidence: 99%

Central Suppression of Regenerated Proprioceptive Afferents

Haftel¹,

Bichler²,

Wang³

et al. 2005

J. Neurosci.

View full text Add to dashboard Cite

show abstract

“…Current consensus holds that this poor outcome is the result of connection errors made by regenerating sensory and motor axons with peripheral targets. Certainly, targeting errors hinder recovery after injury to major nerve trunks; however, functional impairments are also observed following injuries to terminal nerve branches and after reinnervation of the correct muscle (Abelew et al, 2000;Maas et al, 2007;Sabatier et al, 2011). In this case, targeting errors are not possible and a different mechanism is needed to explain the permanency of disorders in gait, balance, and controlled reaching.…”

Section: Introductionmentioning

confidence: 99%

Normal Distribution of VGLUT1 Synapses on Spinal Motoneuron Dendrites and Their Reorganization after Nerve Injury

et al. 2014

View full text Add to dashboard Cite

Peripheral nerve injury induces permanent alterations in spinal cord circuitries that are not reversed by regeneration. Nerve injury provokes the loss of many proprioceptive IA afferent synapses (VGLUT1-IR boutons) from motoneurons, the reduction of IA EPSPs in motoneurons, and the disappearance of stretch reflexes. After motor and sensory axons successfully reinnervate muscle, lost IA VGLUT1 synapses are not re-established and the stretch reflex does not recover; however, electrically evoked EPSPs do recover. The reasons why remaining IA synapses can evoke EPSPs on motoneurons, but fail to transmit useful stretch signals are unknown. To better understand changes in the organization of VGLUT1 IA synapses that might influence their input strength, we analyzed their distribution over the entire dendritic arbor of motoneurons before and after nerve injury. Adult rats underwent complete tibial nerve transection followed by microsurgical reattachment and 1 year later motoneurons were intracellularly recorded and filled with neurobiotin to map the distribution of VGLUT1 synapses along their dendrites. We found in control motoneurons an average of 911 VGLUT1 synapses; ϳ62% of them were lost after injury. In controls, VGLUT1 synapses were focused to proximal dendrites where they were grouped in tight clusters. After injury, most synaptic loses occurred in the proximal dendrites and remaining synapses were declustered, smaller, and uniformly distributed throughout the dendritic arbor. We conclude that this loss and reorganization renders IA afferent synapses incompetent for efficient motoneuron synaptic depolarization in response to natural stretch, while still capable of eliciting EPSPs when synchronously fired by electrical volleys.

show abstract

“…The self-reinnervated muscle regains full efferent motor function with a permanent disruption of the shortlatency, proprioceptive reflex pathways from the reinnervated muscle commonly referred to as the monosynaptic stretch reflex. This peripheral nerve injury results in increased ankle joint flexion, or yield, during the initial weight-bearing portion of the stance phase of gait when the muscle is in the paralytic stage (Abelew et al, 2000;Maas et al, 2007). After self-reinnervation, measurable joint-level deficits can persist for years after the injury, particularly during down-slope walking when engaging the shortlatency pathways are more critical to joint function.…”

Section: Introductionmentioning

confidence: 99%

Whole limb kinematics are preferentially conserved over individual joint kinematics after peripheral nerve injury

Chang

Auyang

Scholz

et al. 2009

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

SUMMARYBiomechanics and neurophysiology studies suggest whole limb function to be an important locomotor control parameter. Inverted pendulum and mass-spring models greatly reduce the complexity of the legs and predict the dynamics of locomotion, but do not address how numerous limb elements are coordinated to achieve such simple behavior. As a first step, we hypothesized whole limb kinematics were of primary importance and would be preferentially conserved over individual joint kinematics after neuromuscular injury. We used a well-established peripheral nerve injury model of cat ankle extensor muscles to generate two experimental injury groups with a predictable time course of temporary paralysis followed by complete muscle selfreinnervation. Mean trajectories of individual joint kinematics were altered as a result of deficits after injury. By contrast, mean trajectories of limb orientation and limb length remained largely invariant across all animals, even with paralyzed ankle extensor muscles, suggesting changes in mean joint angles were coordinated as part of a long-term compensation strategy to minimize change in whole limb kinematics. Furthermore, at each measurement stage (pre-injury, paralytic and self-reinnervated) step-bystep variance of individual joint kinematics was always significantly greater than that of limb orientation. Our results suggest joint angle combinations are coordinated and selected to stabilize whole limb kinematics against short-term natural step-by-step deviations as well as long-term, pathological deviations created by injury. This may represent a fundamental compensation principle allowing animals to adapt to changing conditions with minimal effect on overall locomotor function.

show abstract

Local Loss of Proprioception Results in Disruption of Interjoint Coordination During Locomotion in the Cat

Cited by 110 publications

References 17 publications

Central Suppression of Regenerated Proprioceptive Afferents

Central Suppression of Regenerated Proprioceptive Afferents

Normal Distribution of VGLUT1 Synapses on Spinal Motoneuron Dendrites and Their Reorganization after Nerve Injury

Whole limb kinematics are preferentially conserved over individual joint kinematics after peripheral nerve injury

Contact Info

Product

Resources

About