Sparing of skilled forelimb reaching and corticospinal projections after neonatal motor cortex removal or hemidecortication in the rat: support for the Kennard doctine

Whishaw, Ian Q.; Kolb, Bryan

doi:10.1016/0006-8993(88)90753-6

Cited by 131 publications

(46 citation statements)

References 46 publications

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“…1 and 2) as previously described (19,21). Starting from a pellet retrieval success rate of ∼20% during initial testing, animals improved to a mean proficiency of 70% over 12 d of intensive training (Fig.…”

Section: Resultsmentioning

confidence: 76%

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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Section: Resultsmentioning

confidence: 76%

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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“…[36][37][38] During training the rat learns to approach a small opening in the front of the recording chamber, determine whether a sucrose pellet is available on the shelf and, if so, reach through the opening to retrieve the pellet with its preferred paw. In some previous studies rats were trained in short (10-15 min) daily sessions across 1-2 weeks.…”

Section: Single Pellet Reaching Taskmentioning

confidence: 99%

Effects of Skilled Training on Sleep Slow Wave Activity and Cortical Gene Expression in the Rat

Hanlon

Faraguna

Vyazovskiy

et al. 2009

Sleep

141

131

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SO FAR. IN MAMMALS, THE BEST CHARACTERIZED marker of sleep homeostasis is slow wave activity (SWA), the power density in the electroencephalogram (EEG) between 0.5 and 4 Hz during NREM sleep. SWA is high at sleep onset and declines during sleep, suggesting that it may reflect the accumulation of sleep pressure as a function of duration and/or intensity of prior waking. 1,2 Why and how SWA should reflect sleep homeostasis, however, is still unclear.We hypothesized that SWA is high at sleep onset because it reflects the occurrence, during waking, of widespread synaptic potentiation in cortical and subcortical areas. 3,4 This increase would be detrimental in the long term, because stronger synapses need more energy, space, and cellular supplies, and may lead to saturation of the ability to learn. Sleep would thus be crucial to renormalize synaptic strength to an energetically sustainable level. Molecular and electrophysiological markers of synaptic potentiation increase after waking in rat cortex and hippocampus, while markers of synaptic depression do so after sleep. 5,6 Moreover, in rats and humans, procedures presumably leading to synaptic potentiation or depression result in SWA increases and decreases, respectively. 7-12 More specifically, a study in humans using highdensity EEG found that performing a visuomotor learning task produced a local increase in SWA during subsequent sleep. 7 The increase was restricted to the right parietal cortical areas presumably modified by learning. 13 Moreover, it was specific for NREM sleep, reversible within the first 90 minutes of sleep, and correlated with the improvement in performance after sleep. 7 However, there is no direct evidence that the motor adaptation task used in that study activates neurons in parietal cortex, nor that it causes synaptic potentiation specifically in that region.Previous studies have suggested that activity-dependent genes activated during a specific waking experience may be reactivated during sleep, perhaps to potentiate the same synapses previously engaged during waking. 14 Ribeiro and colleagues found that the exposure to a new environment for 3 hours 15 results in the immediate cortical and hippocampal induction, during waking, of plasticity-related gene zif-268, 16 followed by its downregulation during NREM sleep, and then again by its increased expression during REM sleep (relative to NREM sleep). Intriguingly ~ 3 min of NREM sleep were enough to downregulate waking-induced zif-268 expression, and ~ 2 min of REM sleep were sufficient to detect its selective reinduction, even if both NREM and REM rats were awake during the last 30 min before sacrifice. Another study 17 recently found, using fluorescent in situ hybridization, that the number of hippocampal CA1 neurons showing induction of Arc and/or Homer1a was similar during "rest" periods before and after the exploration of a new environment. However, more cells were active during both exploration and post-task rest than during exploration and pre-task rest. Based on these findings, it h...

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“…Although less dexterous than the intact forelimb, their reaching and grasping movements with the forelimb contralateral to the lesion were fairly good (Takahashi et al 2009). This is in marked contrast to the poor functional recovery of animals whose sensorimotor cortex (SMC) was lesioned in adulthood (Alaverdashvili et al 2008;Barth and Stanfield 1990;Belayev et al 1996;Bland et al 2000;Chen et al 2002;Emerick et al 2003;D'Amato 1970, 1975;Johansson and Ohlsson 1996;Jolkkonen et al 2000;Lindner et al 2003;Markus et al 2005;Roof et al 2001;Schallert et al 2000;Whishaw and Kolb 1988;Yager et al 2006).…”

Section: Introductionmentioning

confidence: 99%

Formation of Descending Pathways Mediating Cortical Command to Forelimb Motoneurons in Neonatally Hemidecorticated Rats

Umeda

Takahashi

Isa

et al. 2010

Journal of Neurophysiology

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Neonatally hemidecorticated rats show fairly normal reaching and grasping behaviors of the forelimb contralateral to the lesion at the adult stage. Previous experiments using an anterograde tracer showed that the corticospinal fibers originating from the sensorimotor cortex of the intact side projected aberrant collaterals to the spinal gray matter on the ipsilateral side. The present study used electrophysiological methods to investigate whether the aberrant projections of the corticospinal tract mediated the pyramidal excitation to the ipsilateral forelimb motoneurons and, if so, which pathways mediate the effect in the hemidecorticated rats. Electrical stimulation to the intact medullary pyramid elicited bilateral negative field potentials in the dorsal horn of the spinal cord. In intracellular recordings of forelimb motoneurons, oligosynaptic pyramidal excitation was detected on both sides of the spinal cord in the hemidecorticated rats, whereas pyramidal excitation of motoneurons on the side ipsilateral to the stimulation was much smaller in normal rats. By lesioning the dorsal funiculus at the upper cervical level, we clarified that the excitation was transmitted to the ipsilateral motoneurons by at least two pathways: one via the corticospinal tract and spinal interneurons and the other via the cortico-reticulo-spinal pathways. These results suggested that in the neonatally hemidecorticated rats, the forelimb movements on the side contralateral to the lesion were modulated by motor commands through the indirect ipsilateral descending pathways from the sensorimotor cortex of the intact side either via the spinal interneurons or reticulospinal neurons.

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Sparing of skilled forelimb reaching and corticospinal projections after neonatal motor cortex removal or hemidecortication in the rat: support for the Kennard doctine

Cited by 131 publications

References 46 publications

Rehabilitation drives enhancement of neuronal structure in functionally relevant neuronal subsets

Rehabilitation drives enhancement of neuronal structure in functionally relevant neuronal subsets

Effects of Skilled Training on Sleep Slow Wave Activity and Cortical Gene Expression in the Rat

Formation of Descending Pathways Mediating Cortical Command to Forelimb Motoneurons in Neonatally Hemidecorticated Rats

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