Monosynaptic excitatory action on motoneurones regenerated to antagonistic muscles

Eccles, John C.; Eccles, Rosamond M.; Magni, F.

doi:10.1113/jphysiol.1960.sp006565

Cited by 42 publications

(15 citation statements)

References 25 publications

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“…This is consistent with previous demonstrations that electrical stimulation of regenerated muscle nerves produces EPSPs in cat motoneurons (Eccles et al, 1960(Eccles et al, , 1962Thulin, 1961;Goldring et al, 1980;Mendell et al, 1995) and H-reflexes in rats (ValeroCabre andNavarro, 2001, 2002). Our observations establish that monosynaptic transmission was operational in the rat.…”

Section: Functional Competence Of Monosynaptic Transmission and Motonsupporting

confidence: 93%

Central Suppression of Regenerated Proprioceptive Afferents

Haftel¹,

Bichler²,

Wang³

et al. 2005

J. Neurosci.

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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.

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Section: Functional Competence Of Monosynaptic Transmission and Motonsupporting

confidence: 93%

Central Suppression of Regenerated Proprioceptive Afferents

Haftel¹,

Bichler²,

Wang³

et al. 2005

J. Neurosci.

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“…At the L5 level, we chose the APFs as one group and the FDL muscle as the other. Homonymous connections within the APF group are strong, whereas inputs from FDL to any of the APF group are quite weak (Eccles et al, 1960).…”

Section: Disruption Of Synaptic Selectivity Between Ia Afferents and mentioning

confidence: 98%

Prenatal Exposure to Elevated NT3 Disrupts Synaptic Selectivity in the Spinal Cord

Wang¹,

Li²,

Taylor³

et al. 2007

J. Neurosci.

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Monosynaptic connections between muscle spindle (Ia) afferents and motoneurons (MNs), the central portion of the stretch reflex circuit, are highly specific, but the mechanisms underlying this specificity are primarily unknown. In this study, we report that embryonic overexpression of neurotrophin-3 (NT3) in muscles disrupts the development of these specific Ia-MN connections, using transgenic (mlc/NT3) mice that express elevated levels of NT3 in muscles during development. In mlc/NT3 mice, there is a substantial increase in the amplitudes of monosynaptic EPSPs evoked by Ia afferents in MNs as measured with extracellular recordings from ventral roots. Despite this increased functional projection of Ia afferents, there is no obvious change in the anatomical density of Ia projections into the ventral horn of the spinal cord. Intracellular recordings from MNs revealed a major disruption in the pattern of Ia-MN connections. In addition to the normal connections between Ia afferents and MNs supplying the same muscle, there were also strong monosynaptic inputs from Ia afferents supplying unrelated muscles, which explains the increase seen in extracellular recordings. There was also a large variability in the strength of Ia input to individual MNs, both from correct and incorrect Ia afferents. Postnatal muscular administration of NT3 did not cause these changes in connectivity. These results indicate that prenatal exposure to elevated levels of NT3 disrupts the normal mechanisms responsible for synaptic selectivity in the stretch reflex circuit.

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“…Electrically evoked IA afferent monosynaptic EPSPs on motoneurons exhibit changes after peripheral nerve injury that parallel the general behavior and time course of synaptic stripping and recovery of excitatory synapses with muscle reinnervation (Eccles et al 1960(Eccles et al , 1962Goldring et al 1980;Haftel et al 2005;Kuno and Llinas 1970;Mendell and Scott 1975;Mendell et al 1995). Logically, changes in IA-motoneuron EPSP amplitude and kinetics were argued to parallel changes in synaptic stripping and recovery of synapses, including IA afferent synapses, in axotomized neurons (Mendell 1988;Titmus and Faber 1990).…”

Section: Functional Implications Of Lost Ia Afferent/vglut1 Input Andmentioning

confidence: 99%

Permanent central synaptic disconnection of proprioceptors after nerve injury and regeneration. I. Loss of VGLUT1/IA synapses on motoneurons

Álvarez

Titus

Bullinger

et al. 2011

Journal of Neurophysiology

123

187

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Motor and sensory proprioceptive axons reinnervate muscles after peripheral nerve transections followed by microsurgical reattachment; nevertheless, motor coordination remains abnormal and stretch reflexes absent. We analyzed the possibility that permanent losses of central IA afferent synapses, as a consequence of peripheral nerve injury, are responsible for this deficit. VGLUT1 was used as a marker of proprioceptive synapses on rat motoneurons. After nerve injuries synapses are stripped from motoneurons, but while other excitatory and inhibitory inputs eventually recover, VGLUT1 synapses are permanently lost on the cell body (75-95% synaptic losses) and on the proximal 100 μm of dendrite (50% loss). Lost VGLUT1 synapses did not recover, even many months after muscle reinnervation. Interestingly, VGLUT1 density in more distal dendrites did not change. To investigate whether losses are due to VGLUT1 downregulation in injured IA afferents or to complete synaptic disassembly and regression of IA ventral projections, we studied the central trajectories and synaptic varicosities of axon collaterals from control and regenerated afferents with IA-like responses to stretch that were intracellularly filled with neurobiotin. VGLUT1 was present in all synaptic varicosities, identified with the synaptic marker SV2, of control and regenerated afferents. However, regenerated afferents lacked axon collaterals and synapses in lamina IX. In conjunction with the companion electrophysiological study [Bullinger KL, Nardelli P, Pinter MJ, Alvarez FJ, Cope TC. J Neurophysiol (August 10, 2011). doi:10.1152/jn.01097.2010], we conclude that peripheral nerve injuries cause a permanent retraction of IA afferent synaptic varicosities from lamina IX and disconnection with motoneurons that is not recovered after peripheral regeneration and reinnervation of muscle by sensory and motor axons.

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Monosynaptic excitatory action on motoneurones regenerated to antagonistic muscles

Cited by 42 publications

References 25 publications

Central Suppression of Regenerated Proprioceptive Afferents

Central Suppression of Regenerated Proprioceptive Afferents

Prenatal Exposure to Elevated NT3 Disrupts Synaptic Selectivity in the Spinal Cord

Permanent central synaptic disconnection of proprioceptors after nerve injury and regeneration. I. Loss of VGLUT1/IA synapses on motoneurons

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