Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity

Minassian, Karen; Persy, I.; Rattay, Frank; Pinter, Michaela M.; Kern, Helmut; Dimitrijevič, Milan R.

doi:10.1016/j.humov.2007.01.005

Cited by 185 publications

(170 citation statements)

References 51 publications

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“…However, the relative changes in the EMG amplitudes and patterns in the flexors and extensors change disproportionately with changes in frequency of ES, i.e., the effects of the stimulus are dependent upon the stimulation patterns as well as the accessibility to sensory information associated with a weight-bearing stepping. ES at frequencies < 10 Hz produces a constant EMG amplitude response to each stimulus in the leg muscles of individuals with a complete SCI injury, but does not evoke locomotor-like activity (Dimitrijevic et al, 1998a;Minassian et al, 2007). Frequencies of ES between 30-40 Hz were optimal for inducing locomotor-like EMG activity in these patients (Fig.…”

Section: Frequency Of Esmentioning

confidence: 92%

“…The networks that produce this rhythmical output are known as the spinal locomotor central pattern generators (CPG) (Grillner and Zangger, 1979). Recently it was shown that locomotor-like movements can be induced by epidural spinal cord stimulation (ES) in adult cats (Iwahara et al, 1991;Gerasimenko et al, 2002aGerasimenko et al, , 2003 and rats (Ichiyama et al, 2005;Lavrov et al, 2006) after a complete thoracic spinal cord transection (ST) as well as in individuals with a complete spinal cord injury (SCI) (Dimitrijevic et al, 1998a;Gerasimenko et al, 2001;Shapkova, 2004;Minassian et al, 2007). In each of these preparations, those intraspinal neurons that generate locomotor-like patterns remain intact, but unlike in CPG all sensory information from the hindlimbs can functionally project to this intraspinal network after the complete loss of supraspinal input.…”

Section: Introductionmentioning

confidence: 99%

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Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans

Gerasimenko

Roy

Edgerton

2008

Experimental Neurology

161

108

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Although epidural stimulation is a technique that has been used for a number of years to treat individuals with a spinal cord injury, the intended outcome has been to suppress plasticity and pain. Over the last decade considerable progress has been made in realizing the potential of epidural stimulation to facilitate posture and locomotion in subjects with severe spinal cord injury who lack the ability to stand or to step. This progress has resulted primarily from experiments with mice, rats and cats having a complete spinal cord transection at a mid-thoracic level and in humans with a complete spinal cord injury. This review describes some of these experiments performed after the complete elimination of supraspinal input that demonstrate that the circuitry necessary to control remarkably normal locomotion appears to reside within the lumbosacral region of the spinal cord. These experiments, however, also demonstrate the essential role of processing proprioceptive information associated with weight-bearing stepping or standing by the spinal circuitry. For example, relatively simple tonic signals provided to the dorsum of the spinal cord epidurally can result in complex and highly adaptive locomotor patterns. Experiments emphasizing a significant complementary effect of epidural stimulation when combined with pharmacological facilitation, e.g., serotonergic agonists, and/or chronic step training also are described. Finally, a major point emphasized in this review is the striking similarity of the lumbosacral circuitry controlling locomotion in the rat and in the human.

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Section: Frequency Of Esmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans

Gerasimenko

Roy

Edgerton

2008

Experimental Neurology

161

108

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“…Intraspinal microstimulation in cats spinalized 5-7 d before testing produces stepping at 2-6 Hz (Barthélemy et al, 2007). The optimum frequency for initiation of rhythmic movements with epidural stimulation in human is between 30 and 40 Hz (Dimitrijevic et al, 1998;Minassian et al, 2007) and is correlated with the appearance of long-latency components in the EMG bursts . Although this variability in the optimum stimulation frequency for facilitating or inducing stepping can be attributed to multiple factors, our observations suggest that the specific spinal circuits activated determine the optimal frequency.…”

Section: Why Is Frequency Of Epidural Stimulation An Important Factormentioning

confidence: 99%

Epidural Stimulation Induced Modulation of Spinal Locomotor Networks in Adult Spinal Rats

Lavrov

Fong

et al. 2008

Journal of Neuroscience

140

123

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The importance of the in vivo dynamic nature of the circuitries within the spinal cord that generate locomotion is becoming increasingly evident. We examined the characteristics of hindlimb EMG activity evoked in response to epidural stimulation at the S1 spinal cord segment in complete midthoracic spinal cord-transected rats at different stages of postlesion recovery. A progressive and phasedependent modulation of monosynaptic (middle) and long-latency (late) stimulation-evoked EMG responses was observed throughout the step cycle. During the first 3 weeks after injury, the amplitude of the middle response was potentiated during the EMG bursts, whereas after 4 weeks, both the middle and late responses were phase-dependently modulated. The middle-and late-response magnitudes were closely linked to the amplitude and duration of the EMG bursts during locomotion facilitated by epidural stimulation. The optimum stimulation frequency that maintained consistent activity of the long-latency responses ranged from 40 to 60 Hz, whereas the shortlatency responses were consistent from 5 to 130 Hz. These data demonstrate that both middle and late evoked potentials within a motor pool are strictly gated during in vivo bipedal stepping as a function of the general excitability of the motor pool and, thus, as a function of the phase of the step cycle. These data demonstrate that spinal cord epidural stimulation can facilitate locomotion in a time-dependent manner after lesion. The long-latency responses to epidural stimulation are correlated with the recovery of weight-bearing bipedal locomotion and may reflect activation of interneuronal central pattern-generating circuits.

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“…1,2 However, this procedure is invasive, because it requires surgical electrode implantation into the epidural space for the delivery of electrical impulses that can elicit a brief bout of alternating leg movements in paraplegic persons. 3 The appearance of such locomotor-like episodes has been attributed to the reactivation of functionally impaired spinal neuronal circuits by inputs from dorsal root (DR) afferents. 4 Because of recent upgrades in hardware technology, that is, grouping 16 electrodes into an epidural array, such a paradigm together with rehabilitative training is reported to facilitate voluntary motor control plus conferring other functional benefits in complete spinal cord-injured persons.…”

Section: Introductionmentioning

confidence: 99%

Staggered multi-site low-frequency electrostimulation effectively induces locomotor patterns in the isolated rat spinal cord

et al. 2015

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Study design: Experimental animal study. Objectives: Epidural stimulation has been used to activate locomotor patterns after spinal injury and typically employs synchronous trains of high-frequency stimuli delivered directly to the dorsal cord, thereby recruiting multiple afferent nerve roots. Here we investigate how spinal locomotor networks integrate multi-site afferent input and address whether frequency coding is more important than amplitude to activate locomotor patterns. Setting: Italy and Belgium. Methods: To investigate the importance of input intensity and frequency in eliciting locomotor activity, we used isolated neonatal rat spinal cords to record episodes of fictive locomotion (FL) induced by electrical stimulation of single and multiple dorsal roots (DRs), employing different stimulating protocols. Results: FL was efficiently induced through staggered delivery (delays 0.5 to 2 s) of low-frequency pulse trains (0.33 and 0.67 Hz) to three DRs at intensities sufficient to activate ventral root reflexes. Delivery of the same trains to a single DR or synchronously to multiple DRs remained ineffective. Multi-site staggered trains were more efficient than randomized pulse delivery. Weak trains simultaneously delivered to DRs failed to elicit FL. Locomotor rhythm resetting occurred with single pulses applied to various distant DRs. Conclusion: Electrical stimulation recruited spinal networks that generate locomotor programs when pulses were delivered to multiple sites at low frequency. This finding might help devising new protocols to optimize the increasingly more common use of epidural implantable arrays to treat spinal dysfunctions.

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Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity

Cited by 185 publications

References 51 publications

Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans

Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans

Epidural Stimulation Induced Modulation of Spinal Locomotor Networks in Adult Spinal Rats

Staggered multi-site low-frequency electrostimulation effectively induces locomotor patterns in the isolated rat spinal cord

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