Corticospinal sprouting occurs selectively following dorsal rhizotomy in the macaque monkey

Darian‐Smith, Corinna; Lilak, Alayna; Alarcón, Christina N.

doi:10.1002/cne.23289

Cited by 35 publications

(45 citation statements)

References 36 publications

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“…Somewhat similar results were obtained after localized cervical dorsal root lesions (rhizotomy), which cause both functional cortical reorganization (Darian-Smith and Brown, 2000) and sprouting in the brainstem (Darian-Smith, 2004, 2013). Intriguingly, in this model the reorganization was associated to functional recovery (Darian-Smith and Ciferri, 2006) and to neurogenesis within the spinal cord (Vessal et al, 2007) and in the sensorimotor cortex (Vessal and Darian-Smith, 2010).…”

Section: Cortical Reorganization Depends On Species (Fig 1)supporting

confidence: 69%

Cortical reorganization after spinal cord injury: Always for good?

et al. 2014

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Plasticity constitutes the basis of behavioral changes as a result of experience. It refers to neural network shaping and re-shaping at the global level and to synaptic contacts remodeling at the local level, either during learning or memory encoding, or as a result of acute or chronic pathological conditions. ‘Plastic’ brain reorganization after central nervous system lesions has a pivotal role in the recovery and rehabilitation of sensory and motor dysfunction, but can also be “maladaptive”. Moreover, it is clear that brain reorganization it is not a “static” phenomenon but rather a very dynamic process. Spinal cord injury immediately initiates a change in brain state and starts cortical reorganization. In the long term, the impact of injury – with or without accompanying therapy – on the brain is a complex balance between supraspinal reorganization and spinal recovery. The degree of cortical reorganization after spinal cord injury is highly variable, and can range from no reorganization (i.e. “silencing”) to massive cortical remapping. This variability critically depends on the species, the age of the animal when the injury occurs, the time after the injury has occurred, and the behavioral activity and possible therapy regimes after the injury. We will briefly discuss these dependencies, trying to highlight their translational value. Overall, it is not only necessary to better understand how the brain can reorganize after injury with or without therapy, it is also necessary to clarify when and why brain reorganization can be either “good” or “bad” in terms of its clinical consequences. This information is critical in order to develop and optimize cost-effective therapies to maximize functional recovery while minimizing maladaptive states after spinal cord injury.

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Section: Cortical Reorganization Depends On Species (Fig 1)supporting

confidence: 69%

Cortical reorganization after spinal cord injury: Always for good?

et al. 2014

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“…Unlike the M1 CST, the S1 CST extends few if any collateral branches across the midline in the cervical cord in normal animals, and there is little evidence that this changes significantly following spinal injury either in this or past investigations (see Figure c for rare example of crossing fibers; Darian‐Smith et al, , ). However, the primary somatosensory cortex does project bilaterally to the brainstem reticular formation in our monkeys (Fisher and Darian‐Smith, unpublished), which in turn could drive reticulospinal input to help shape the bilateral sprouting observed.…”

Section: Discussionmentioning

confidence: 71%

Extensive somatosensory and motor corticospinal sprouting occurs following a central dorsal column lesion in monkeys

Fisher

Lilak

Garner

et al. 2018

J of Comparative Neurology

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The corticospinal tract (CST) forms the major descending pathway mediating voluntary hand movements in primates, and originates from ∼nine cortical subdivisions in the macaque. While the terminals of spared motor CST axons are known to sprout locally within the cord in response to spinal injury, little is known about the response of the other CST subcomponents. We previously reported that following a cervical dorsal root lesion (DRL), the primary somatosensory (S1) CST terminal projection retracts to 60% of its original terminal domain, while the primary motor (M1) projection remains robust (Darian-Smith et al., J. Neurosci., 2013). In contrast, when a dorsal column lesion (DCL) is added to the DRL, the S1 CST, in addition to the M1 CST, extends its terminal projections bilaterally and caudally, well beyond normal range (Darian-Smith et al., J. Neurosci., 2014). Are these dramatic responses linked entirely to the inclusion of a CNS injury (i.e., DCL), or do the two components summate or interact? We addressed this directly, by comparing data from monkeys that received a unilateral DCL alone, with those that received either a DRL or a combined DRL/DCL. Approximately 4 months post-lesion, the S1 hand region was mapped electrophysiologically, and anterograde tracers were injected bilaterally into the region deprived of normal input, to assess spinal terminal labeling. Using multifactorial analyses, we show that following a DCL alone (i.e., cuneate fasciculus lesion), the S1 and M1 CSTs also sprout significantly and bilaterally beyond normal range, with a termination pattern suggesting some interaction between the peripheral and central lesions.

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“…Electrophysiological (low threshold unitary) recordings were made to locate the region of digit/paw representation within S1. Recordings were made with a tungsten microelectrode (1.2–1.4 mΩ at 1 kHz) and peripheral stimulation performed with a camel hair brush and Von Fry filaments as described in earlier studies (Darian‐Smith et al, ; Darian‐Smith & Brown, ; Darian‐Smith, Lilak, & Alarcon, ; Fisher et al, ). The anterograde neuronal tracer biotin dextran amine (BDA, 15% aq., Sigma B9139) was injected into the area corresponding to digit 1–3 representation (D1‐3; Figure ).…”

Section: Methodsmentioning

confidence: 99%

“…In the spinal cord, terminal boutons were mapped in coronal section series (every 240 μm) through C1‐T3, using Neurolucida (MicroBrightField, Inc.). An outline was drawn around the terminal distribution area as described previously (Darian‐Smith et al, ; Darian‐Smith et al, ). Results were verified by two separate users blind to the animal test group.…”

Section: Methodsmentioning

confidence: 99%

Somatosensory corticospinal tract axons sprout within the cervical cord following a dorsal root/dorsal column spinal injury in the rat

McCann

Fisher

Ahloy‐Dallaire

et al. 2019

J of Comparative Neurology

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The corticospinal tract (CST) is the major descending pathway controlling voluntary hand function in primates, and though less dominant, it mediates voluntary paw movements in rats. As with primates, the CST in rats originates from multiple (albeit fewer) cortical sites, and functionally different motor and somatosensory subcomponents terminate in different regions of the spinal gray matter. We recently reported in monkeys that following a combined cervical dorsal root/dorsal column lesion (DRL/DCL), both motor and S1 CSTs sprout well beyond their normal terminal range. The S1 CST sprouting response is particularly dramatic, indicating an important, if poorly understood, somatosensory role in the recovery process. As rats are used extensively to model spinal cord injury, we asked if the S1 CST response is conserved in rodents. Rats were divided into sham controls, and two groups surviving post‐lesion for ~6 and 10 weeks. A DRL/DCL was made to partially deafferent one paw. Behavioral testing showed a post‐lesion deficit and recovery over several weeks. Three weeks prior to ending the experiment, S1 cortex was mapped electrophysiologically, for tracer injection placement to determine S1 CST termination patterns within the cord. Synaptogenesis was also assessed for labeled S1 CST terminals within the dorsal horn. Our findings show that the affected S1 CST sprouts well beyond its normal range in response to a DRL/DCL, much as it does in macaque monkeys. This, along with evidence for increased synaptogenesis post‐lesion, indicates that CST terminal sprouting following a central sensory lesion, is a robust and conserved response.

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Corticospinal sprouting occurs selectively following dorsal rhizotomy in the macaque monkey

Cited by 35 publications

References 36 publications

Cortical reorganization after spinal cord injury: Always for good?

Cortical reorganization after spinal cord injury: Always for good?

Extensive somatosensory and motor corticospinal sprouting occurs following a central dorsal column lesion in monkeys

Somatosensory corticospinal tract axons sprout within the cervical cord following a dorsal root/dorsal column spinal injury in the rat

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