Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat

Brownstone, Robert M.; Gossard, Jean‐Pierre; Hultborn, Hans

doi:10.1007/bf00232436

Cited by 104 publications

(104 citation statements)

References 30 publications

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“…As motoneurons were depolarized, they reached a threshold where their input was significantly amplified (Brownstone et al, 1994). We did not conclusively determine whether this voltage-dependence was due to activation of PICs, NMDA receptors, or both (Brownstone et al, 1991(Brownstone et al, , 1994. Nevertheless, these experiments demonstrated quite clearly that motoneurons do not simply respond passively to synaptic current during behavior.…”

Section: State-dependence Of Motoneuron Properties: Modulation Duringmentioning

confidence: 85%

“…This prompted a series of experiments with Hultborn in which we demonstrated that the excitatory synaptic input to motoneurons during fictive locomotion activated voltagedependent channels. As motoneurons were depolarized, they reached a threshold where their input was significantly amplified (Brownstone et al, 1994). We did not conclusively determine whether this voltage-dependence was due to activation of PICs, NMDA receptors, or both (Brownstone et al, 1991(Brownstone et al, , 1994.…”

Section: State-dependence Of Motoneuron Properties: Modulation Duringmentioning

confidence: 93%

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Beginning at the end: Repetitive firing properties in the final common pathway

Brownstone

2006

Progress in Neurobiology

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Since the early 20th century, it has been recognized that motoneurons must fire repetitive trains of action potentials to produce muscle contraction. In 1932, Sir John Eccles, together with Hebbel Hoff, found that action potential spike trains in motor axons were produced by "rhythmic centres", which were within the motoneurons themselves. Two decades later, Eccles attended a Cold Spring Harbor Symposium in NY, USA entitled "The Neuron". Two of the many notable presentations at this symposium were juxtaposed: one by Eccles from the University of Otago, Dunedin, NZL, and the other by J. Walter Woodbury and Harry Patton from the University of Washington, Seattle, USA. Both presentations included data obtained using sharp microelectrodes to study the intracellularly recorded potentials of cat motoneurons. In this review, I discuss some of the events leading up to and surrounding this jointly accomplished advance and proceed to discussion of subsequent studies over 5+ decades that have made use of intracellular recordings from motoneurons to study their repetitive firing behavior. This begins with early descriptions of primary and secondary range firing, and continues to the discovery of dendritic persistent inward currents and their relation to plateau potentials, synaptic amplification, and motoneuronal firing. Following a brief description of the possible mechanisms underlying spike frequency adaptation, I discuss the modulation of repetitive firing properties during various motor behaviors. It has become increasingly clear that the central nervous system has exquisite control of the repetitive firing of motoneurons. Eccles' work laid the foundation for the present-day study of these processes.

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Section: State-dependence Of Motoneuron Properties: Modulation Duringmentioning

confidence: 85%

Section: State-dependence Of Motoneuron Properties: Modulation Duringmentioning

confidence: 93%

Beginning at the end: Repetitive firing properties in the final common pathway

Brownstone

2006

Progress in Neurobiology

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“…It is unlikely that voltage dependence of the EPSPs (Brownstone et al 1994) is responsible for the AM of the MLRevoked PSPs during locomotion. To study these EPSPs, it was necessary to either study nonspiking motoneurons or to hyperpolarize the motoneurons, which would not only eliminate the firing but also take the membrane out of the range of activation for voltage-gated channels.…”

Section: Relationship Of Mlr-evoked Psps To Locomotion and Ldpsmentioning

confidence: 99%

“…3F and 4F) and not one indicative of a negative slope conductance. It would be predicted that these EPSPs would in fact also show some voltage dependence once the motoneurone is sufficiently depolarized, as input from locomotor centers to motoneurones is indeed voltage dependent (Brownstone et al 1994). At such membrane potentials, the EPSP amplitude would likely increase fairly suddenly rather than linearly.…”

Section: Relationship Of Mlr-evoked Psps To Locomotion and Ldpsmentioning

confidence: 99%

Mechanism for Activation of Locomotor Centers in the Spinal Cord by Stimulation of the Mesencephalic Locomotor Region

Noga

Kriellaars

Brownstone

et al. 2003

Journal of Neurophysiology

116

117

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Noga, Brian R., Dean J. Kriellaars, Robert M. Brownstone, and Larry M. Jordan. Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region. J Neurophysiol 90: 1464 -1478, 2003. First published March 12, 2003 10.1152/jn.00034.2003. The synaptic pathways of mesencephalic locomotor region (MLR)-evoked excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) recorded from lumbar motoneurons of unanesthetized decerebrate cats during fictive locomotion were analyzed prior to, during, and after cold block of the medial reticular formation (MedRF) or the low thoracic ventral funiculus (VF). As others have shown, electrical stimulation of the MLR typically evoked short-latency excitatory or mixed excitatory/inhibitory PSPs in flexor and extensor motoneurons. The bulbospinal conduction velocities averaged ϳ88 m/s (range: 62-145 m/s) and segmental latencies for EPSPs ranged from 1.2 to 10.9 ms. The histogram of segmental latencies showed three peaks, suggesting di-, tri-, and polysynaptic linkages. Segmental latencies for IPSPs suggested trisynaptic or polysynaptic transmission. Most EPSPs (69/77) were significantly larger during the depolarized phase of the intracellular locomotor drive potential (LDP), and most IPSPs (35/46) were larger during the corresponding hyperpolarized phase. Bilateral cooling of the MedRF reversibly abolished locomotion of both hindlimbs as measured from the electroneurogram (ENG) activity of muscle nerves and simultaneously abolished or diminished the motoneuron PSPs and LDPs. Unilateral cooling of the VF blocked locomotion ipsilaterally and diminished it contralaterally with concomitant loss or decrease the motoneuron PSPs and LDPs. Relative to the side of motoneuron recording, cooling of the ipsilateral VF sometimes uncovered longerlatency EPSPs, whereas cooling of the contralateral VF abolished longer-latency EPSPs. It is concluded that MLR stimulation activates a pathway that relays in the MedRF and descends bilaterally in the VF to contact spinal interneurons that project to motoneurons. Local segmental pathways that activate or inhibit motoneurons during MLRevoked fictive locomotion appear to be both ipsilateral and contralateral.

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“…However, voltage-activated calcium currents in motoneuron dendrites, which generate "persistent inward currents" (PICs), appear to ensure integration of even distal inputs Li and Bennett, 2003). PICs generate plateau potentials (Hounsgaard and Kiehn, 1989;Lee and Heckman, 1996) and amplify synaptic inputs to motoneurons, both excitatory (Brownstone et al, 1994;Bennett et al, 1998;Lee and Heckman, 2000;Jones and Lee, 2006;Powers et al, 2008) and inhibitory (Hultborn et al, 2003;Kuo et al, 2003;Bui et al, 2008a).…”

Section: Introductionmentioning

confidence: 99%

Staircase Currents in Motoneurons: Insight into the Spatial Arrangement of Calcium Channels in the Dendritic Tree

Carlin¹,

Bui²,

Dai³

et al. 2009

J. Neurosci.

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In spinal motoneurons, activation of dendritically located depolarizing conductances can lead to amplification of synaptic inputs and the production of plateau potentials. Immunohistochemical and computational studies have implicated dendritic Ca V 1.3 channels in this amplification and suggest that Ca V 1.3 channels in spinal motoneurons may be organized in clusters in the dendritic tree. Our goal was to provide physiological evidence for the presence of multiple discrete clusters of voltage-gated calcium channels in spinal motoneurons and to explore the spatial arrangement of these clusters in the dendritic tree. We recorded voltage-gated calcium currents from spinal motoneurons in slices of mature mouse spinal cords. We demonstrate that single somatic voltage-clamp steps can elicit multiple inward currents with varying delays to onset, resulting in a current with a "staircase"-like appearance. Recordings from cultured dorsal root ganglion cells at different stages of neurite development provide evidence that these currents arise from the unclamped portions of the dendritic tree. Finally, both voltage-and current-clamp data were used to constrain computer models of a motoneuron. The resultant simulations impose two conditions on the spatial distribution of Ca V channels in motoneuron dendrites: one of asymmetry relative to the soma and another of spatial separation between clusters of Ca V channels. We propose that this compartmentalization would provide motoneurons with the ability to process multiple sources of input in parallel and integrate this processed information to produce appropriate trains of action potentials for the intended motor behavior.

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Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat

Cited by 104 publications

References 30 publications

Beginning at the end: Repetitive firing properties in the final common pathway

Beginning at the end: Repetitive firing properties in the final common pathway

Mechanism for Activation of Locomotor Centers in the Spinal Cord by Stimulation of the Mesencephalic Locomotor Region

Staircase Currents in Motoneurons: Insight into the Spatial Arrangement of Calcium Channels in the Dendritic Tree

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