Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry

Martinez, Marina; Delivet-Mongrain, Hugo; Leblond, Hugues; Rossignol, Serge

doi:10.1152/jn.00368.2011

Cited by 60 publications

(81 citation statements)

References 56 publications

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“…Although gross locomotor function recovers in a few weeks after thoracic spinal transection in cats (Barbeau and Rossignol, 1987) and locomotion improves with treadmill training, chronic disruptions in MN receptive fields due to improper interneuronal sensory processing after the loss of descending neuromodulation may interfere with compensatory changes that occur after other types of injuries, such as peripheral neurectomies and incomplete spinal injuries (Goldberger, 1977;Goldberger and Murray, 1980;Martinez et al, 2011). Although various studies have considered the importance of neuromodulation in general (Croul et al, 1998;Kim et al, 1999;Nothias et al, 2005), they have focused on broad activation of the descending monoaminergic systems and their influence on movement parameters.…”

Section: Discussionmentioning

confidence: 99%

Motoneuron Intrinsic Properties, but Not Their Receptive Fields, Recover in Chronic Spinal Injury

Johnson

Kajtaz

Cain³

et al. 2013

J. Neurosci.

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Proper movement execution relies on precise input processing by spinal motoneurons (MNs). Spinal MNs are activated by limb joint rotations. Typically, their movement-related receptive fields (MRRFs) are sharply focused and joint-specific. After acute spinal transection MRRFs become wide, but their manifestation is not apparent, as intrinsic excitability, primarily resulting from the loss of persistent inward currents (PICs), dramatically decreases. PICs undergo a remarkable recovery with time after injury. Here we investigate whether MRRFs undergo a recovery that parallels that of the PIC. Using the chronic spinal cat in acute terminal decerebrate preparations, we found that MRRFs remain expanded 1 month after spinal transaction, whereas PICs recovered to Ͼ80% of their preinjury amplitudes. These recovered PICs substantially amplified the expanded inputs underlying the MRRFs. As a result, we show that single joint rotations lead to the activation of muscles across the entire limb. These results provide a potential mechanism for the propagation of spasms throughout the limb.

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Section: Discussionmentioning

confidence: 99%

Motoneuron Intrinsic Properties, but Not Their Receptive Fields, Recover in Chronic Spinal Injury

Johnson

Kajtaz

Cain³

et al. 2013

J. Neurosci.

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“…First, descending inputs were transmitted via crossed pathways to reach the left side. Functional recovery with an increased connectivity via crossed pathways after SCI have been reported before, including the brainstem (Matsuyama et al, 2004;Maier and Schwab, 2006;van den Brand et al, 2012;Filli et al, 2014;Zörner et al, 2014). Second, the disconnection from the ipsilateral descending pathways for 3 weeks may have induced an intrinsic spinal plasticity resulting in more autonomous activation of the CPG, a situation comparable to the adaptation after a chronic complete spinal cord section (De Leon et al, 1998;Lavrov et al, 2006;.…”

Section: Discussionmentioning

confidence: 76%

“…If the hemisection induced profound changes in spinal cord intrinsic circuitry, then it should remain present even when all supraspinal pathways are removed (Hultborn and Malmsten, 1983a;Hultborn and Malmsten, 1983b;Barrière et al, 2008;Martinez et al, 2011). In this study, we successfully induced fictive locomotion in seven of nine cats with a chronic hemisection after an acute complete section of the cord at T13.…”

Section: Plasticity Revealed By the Acute Complete Sectionmentioning

confidence: 80%

“…In five cats, most of the tissue of the left half of the cord was destroyed. In three cats, there was additional loss on the right side; in one cat, 3/4 of the cord was lost but the right ventral quadrant was intact (Eidelberg et al, 1981;Little et al, 1988;Schucht et al, 2002;Martinez et al, 2011). This last cat showed similar results as the others and was thus included in the group.…”

Section: Patterns Of Fictive Locomotion In the Left And Right Sidementioning

confidence: 84%

“…After a complete spinal transection during an acute experiment, cats with a chronic spinal cord hemisection displayed an enhanced reflex excitability on the side of the lesion leading to left/right asymmetries (Hultborn and Malmsten, 1983a;Hultborn and Malmsten, 1983b). In addition, Rossignol and colleagues investigated the plasticity of the locomotor system by comparing stepping before and after a left lateral hemisection (T10) and after a complete section (T13) 3 weeks later (Barrière et al, 2008;Martinez et al, 2011;Martinez et al, 2012). After the first lesion, cats could gradually recover quadrupedal locomotion over 3 weeks, but an asymmetry in stepping pattern persisted.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Plastic Changes in Lumbar Locomotor Networks after a Partial Spinal Cord Injury in Cats

Gossard

Delivet-Mongrain

Martinez

et al. 2015

Journal of Neuroscience

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After an incomplete spinal cord injury (SCI), we know that plastic reorganization occurs in supraspinal structures with residual descending tracts. However, our knowledge about spinal plasticity is rather limited. Our recent studies point to changes within the spinal cord below the lesion. After a lateral left hemisection (T10), cats recovered stepping with both hindlimbs within 3 weeks. After a complete section (T13) in these cats, bilateral stepping was seen on the next day, a skill usually acquired after several weeks of treadmill training. This indicates that durable plastic changes occurred below the lesion. However, because sensory feedback entrains the stepping rhythm, it is difficult to reveal central pattern generator (CPG) adaptation. Here, we investigated whether lumbar segments of cats with a chronic hemisection were able to generate fictive locomotion-that is, without phasic sensory feedback as monitored by five muscle nerves in each hindlimb. With a chronic left hemisection, the number of muscle nerves displaying locomotor bursts was larger on the left than on the right. In addition, transmission of cutaneous reflexes was relatively facilitated on the left. Later during the acute experiment, a complete spinalization (T13) was performed and clonidine was injected to induce rhythmic activities. There were still more muscle nerves displaying locomotor bursts on the left. The results demonstrate that spinal networks were indeed modified after a hemisection with a clear asymmetry between left and right in the capacity to generate locomotion. Plastic changes in CPG and reflex transmission below the lesion are thus involved in the stepping recovery after an incomplete SCI.

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Locomotor recovery after spinal cord hemisection/contusion injures in bonnet monkeys: Footprint testing—a minireview

Rangasamy

2013

Synapse

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Spinal cord injuries usually produce loss or impairment of sensory, motor and reflex function below the level of damage. In the absence of functional regeneration or manipulations that promote regeneration, spontaneous improvements in motor functions occur due to the activation of multiple compensatory mechanisms in animals and humans following the partial spinal cord injury. Many studies were performed on quantitative evaluation of locomotor recovery after induced spinal cord injury in animals using behavioral tests and scoring techniques. Although few studies on rodents have led to clinical trials, it would appear imperative to use nonhuman primates such as macaque monkeys in order to relate the research outcomes to recovery of functions in humans. In this review, we will discuss some of our research evidences concerning the degree of spontaneous recovery in bipedal locomotor functions of bonnet monkeys that underwent spinal cord hemisection/contusion lesions. To our knowledge, this is the first report to discuss on the extent of spontaneous recovery in bipedal locomotion of macaque monkeys through the application of footprint analyzing technique. In addition, the results obtained were compared with the published data on recovery of quadrupedal locomotion of spinally injured rodents. We propose that the mechanisms underlying spontaneous recovery of functions in spinal cord lesioned monkeys may be correlated to the mature function of spinal pattern generator for locomotion under the impact of residual descending and afferent connections. Moreover, based on analysis of motor functions observed in locomotion in these subjected monkeys, we understand that spinal automatism and development of responses by afferent stimuli from outside the cord could possibly contribute to recovery of paralyzed hindlimbs. This report also emphasizes the functional contribution of progressive strengthening of undamaged nerve fibers through a collateral sprouts/synaptic plasticity formed in partially lesioned cord of monkeys.

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Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry

Abstract: Martinez M, Delivet-Mongrain H, Leblond H, Rossignol S. Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry.

Cited by 60 publications

References 56 publications

Motoneuron Intrinsic Properties, but Not Their Receptive Fields, Recover in Chronic Spinal Injury

Motoneuron Intrinsic Properties, but Not Their Receptive Fields, Recover in Chronic Spinal Injury

Plastic Changes in Lumbar Locomotor Networks after a Partial Spinal Cord Injury in Cats

Locomotor recovery after spinal cord hemisection/contusion injures in bonnet monkeys: Footprint testing—a minireview

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