Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: A retrograde carbocyanine dye analysis

McKenna, John E.; Prusky, Glen T.; Whishaw, Ian Q.

doi:10.1002/(sici)1096-9861(20000410)419:3<286::aid-cne2>3.0.co;2-3

Cited by 137 publications

(123 citation statements)

References 72 publications

(80 reference statements)

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“…Ipsilaterally, the C 5 bursts alternated with the C 8 's and segmentally both the C 5 and C 8 roots alternated with each other. Although there has been no corresponding work in the mouse, data from the rat show that the triceps (forelimb extensor) motoneurons are located in more rostral segments compared with the biceps (forelimb flexor) (McKenna et al 2000). Therefore it is reasonable to hypothesize that the pattern we observed likely reflects an alternating locomotor pattern.…”

Section: Rhythmogenic Capability Of Cervicothoracic Regionsmentioning

confidence: 68%

“…Such activity would be expected to consist of alternating flexor-extensor activity that can be resolved by recording alternating bursts from C 5 and C 8 segments (Figs. 1 and 2) (Ballion et al 2001;McKenna et al 2000). To test the hypothesis that cervical segments were producing locomotor-like activity, we evoked locomotor-like rhythms via cauda equina stimulation as previously described and recorded from the ipsilateral C 5 , C 8 , T 10 , L 2 , and L 5 ventral roots (Fig.…”

Section: Cauda Equina Activation Of Thoracocervical Segments Does Notmentioning

confidence: 99%

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Interaction Between Developing Spinal Locomotor Networks in the Neonatal Mouse

Gordon¹,

Dunbar²,

Vanneste³

et al. 2008

Journal of Neurophysiology

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Gordon IT, Dunbar MJ, Vanneste KJ, Whelan PJ. Interaction between developing spinal locomotor networks in the neonatal mouse. J Neurophysiol 100: 117-128, 2008. First published April 24, 2008 doi:10.1152/jn.00829.2007. At birth, thoracosacral spinal cord networks in mouse can produce a coordinated locomotor-like pattern. In contrast, less is known about the cervicothoracic networks that generate forelimb locomotion. Here we show that cervical networks can produce coordinated rhythmic patterns in the brain stem-spinal cord preparation of the mouse. Segmentally the C 5 and C 8 neurograms were each found to be alternating left-right, and the ipsilateral C 5 and C 8 neurograms also alternated. Collectively these patterns were suggestive of locomotor-like activity. This pattern was not dependent on the presence of thoracosacral segments because they could be evoked following a complete transection of the spinal cord at T 5 . We next demonstrated that activation of thoracosacral networks either pharmacologically or by stimulation of sacrocaudal afferents could produce rhythmic activity within the C 5 and C 8 neurograms. On the other hand, pharmacological activation of cervical networks did not evoke alternating cervical rhythmic activity either in isolated cervicothoracic or -sacral preparations. Under these conditions, we found that activation of cervicothoracic networks could alter the timing of thoracosacral locomotor-like patterns. When thoracosacral networks were not activated pharmacologically but received rhythmic drive from cervicothoracic networks, a pattern of slow bursts with superimposed fast synchronous oscillations became the dominant lumbar neurogram pattern. Our data suggest that in neonatal mice the cervical CPG is capable of producing coordinated rhythmic patterns in the absence of input from lumbar segments, but caudorostral drive contributes to cervical patterns and rhythm stability.

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Section: Rhythmogenic Capability Of Cervicothoracic Regionsmentioning

confidence: 68%

Section: Cauda Equina Activation Of Thoracocervical Segments Does Notmentioning

confidence: 99%

Interaction Between Developing Spinal Locomotor Networks in the Neonatal Mouse

Gordon¹,

Dunbar²,

Vanneste³

et al. 2008

Journal of Neurophysiology

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“…Before behavioral training, all subjects underwent injections of retrogradely transportable tracers into the spinal cord to identify cortical motor neurons projecting to specific spinal segments. In rats, the C8 spinal cord segment contains lower motor neurons that activate muscles controlling distal forelimb movements required for grasping (11), whereas lower motor neuron pools located in the C4 spinal segment are associated with control of proximal forelimb, shoulder and neck musculature (11,12). To selectively identify layer V corticospinal populations providing innervation to spinal segments associated with distal forelimb movements, subjects received injections of red fluorescent latex microspheres within the dorsal gray matter of the C8 spinal segment.…”

Section: Resultsmentioning

confidence: 99%

Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain

Wang

Conner

Rickert

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

102

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Cortical networks undergo adaptations during learning, including increases in dendritic complexity and spines. We hypothesized that structural elaborations during learning are restricted to discrete subsets of cells preferentially activated by, and relevant to, novel experience. Accordingly, we examined corticospinal motor neurons segregated on the basis of their distinct descending projection patterns, and their contribution to specific aspects of motor control during a forelimb skilled grasping task in adult rats. Learningmediated structural adaptations, including extensive expansions of spine density and dendritic complexity, were restricted solely to neurons associated with control of distal forelimb musculature required for skilled grasping; neurons associated with control of proximal musculature were unchanged by the experience. We further found that distal forelimb-projecting and proximal forelimbprojecting neurons are intermingled within motor cortex, and that this distribution does not change as a function of skill acquisition. These findings indicate that representations of novel experience in the adult motor cortex are associated with selective structural expansion in networks of functionally related, active neurons that are distributed across a single cortical domain. These results identify a distinct parcellation of cortical resources in support of learning.cell filling | corticospinal neurons | morphology | sensorimotor cortex P rior studies have documented alterations of neuronal structure in response to experience and learning (1-6), raising the possibility that these structural modifications might serve as a basis for long-term memory. Within randomly sampled layer V pyramidal neurons of the motor cortex, dendritic branching and arborization (1, 2) and synapse number (5, 7, 8) increase in rats undergoing skilled motor training. New spines reportedly form rapidly after training (9), are stabilized by repeated training, and can persist for extended times beyond the experience (10). Collectively, these observations support the concept that newly formed connections may provide a basis for long-term maintenance of experience.However, studies examining modifications of neuronal architecture in the context of learning and experience have not focused exclusively on neurons specifically engaged by the experience; instead, random sampling of neurons has been used across the broader cortical functional unit (e.g., forelimb motor cortex or visual cortex). To reach a greater level of understanding regarding the nature of experiential representation in the learning adult brain, it is necessary to examine structural modifications in functionally distinct subsets of neurons based on their relevance to the learning experience. In the present study, taking advantage of specific output patterns of the motor system, we attempt to achieve this level of resolution using a combination of behavioral training and retrograde filling of cortical motor neurons projecting to distinct spinal segments that act as effectors of...

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“…To label corticospinal neurons projecting to the C8 cervical spinal segment, which contains lower motor neurons that activate muscles controlling distal forelimb movements that are required for grasping (36), the dura between C7 and T1 was visualized, a small puncture in the dura was made using a 25-gauge needle, and a glass micropipette (tip <50 μm) containing red fluorescent latex microspheres (Lumafluor) was inserted into the dorsal horn of the spinal cord (depth of 0.25 mm and 0.3 mm lateral to midline). Using a Picospritzer II (General Valve, Inc.), 100 nL fluorescent latex microspheres were injected into each side of the spinal cord.…”

Section: Methodsmentioning

confidence: 99%

Rehabilitation drives enhancement of neuronal structure in functionally relevant neuronal subsets

Wang

Conner

Nagahara

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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We determined whether rehabilitation after cortical injury also drives dynamic dendritic and spine changes in functionally distinct subsets of neurons, resulting in functional recovery. Moreover, given known requirements for cholinergic systems in mediating complex forms of cortical plasticity, including skilled motor learning, we hypothesized that cholinergic systems are essential mediators of neuronal structural and functional plasticity associated with motor rehabilitation. Adult rats learned a skilled forelimb grasping task and then, underwent destructive lesions of the caudal forelimb region of the motor cortex, resulting in nearly complete loss of grasping ability. Subsequent intensive rehabilitation significantly enhanced both dendritic architecture and spine number in the adjoining rostral forelimb area compared with that in the lesioned animals that were not rehabilitated. Cholinergic ablation markedly attenuated rehabilitation-induced recovery in both neuronal structure and motor function. Thus, rehabilitation focused on an affected limb robustly drives structural compensation in perilesion cortex, enabling functional recovery.cell filling | corticospinal neurons | cholinergic | morphology | plasticity S tudies over the past decade have indicated that the adult brain is structurally dynamic (1-3). Indeed, dendritic spines dynamically turn over in the adult brain (3, 4), and learning of novel tasks is associated with further increases in spine turnover (4). Moreover, total and stable increases in spine number together with enhanced dendritic complexity can be detected when analyses are focused specifically on neuronal subpopulations that are functionally related to a newly learned motor skill (5). For example, we recently reported that cortical layer V pyramidal neurons, which project to spinal segment C8 and are specifically engaged when learning a skilled forelimb grasping task, elaborate a 22% increase in apical dendritic spines and exhibit significant increases in dendritic branching and total dendritic length (5); an adjoining control population of cortical layer V pyramidal neurons that project to C4, which are not specifically shaped by the skilled motor task, exhibits no change in spines or dendritic complexity when the same task is learned (5). The detection of stable structural increases in neurons engaged by skilled motor learning in contrast to a lack of change in adjacent neurons that are not engaged by learning advances our understanding of mechanisms underlying experience-dependent cortical plasticity.Damage to the adult CNS also generates adaptive brain plasticity. For example, focal cortical lesions evoke cortical map plasticity (6, 7), extension of new axonal connections (7,8), and neurogenesis (9). A very important and unresolved question in the neural plasticity and injury fields is whether rehabilitation-that is, specific retraining of injured neural circuits-can drive, alter, or enhance neural plasticity subsequent to brain lesions. Whereas extensive literature has shown that rehab...

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Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: A retrograde carbocyanine dye analysis

Cited by 137 publications

References 72 publications

Interaction Between Developing Spinal Locomotor Networks in the Neonatal Mouse

Interaction Between Developing Spinal Locomotor Networks in the Neonatal Mouse

Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain

Rehabilitation drives enhancement of neuronal structure in functionally relevant neuronal subsets

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