New Corticopontine Connections in the Primate Brain: Contralateral Projections From the Arm/Hand Area of the Precentral Motor Region (original) (raw)
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The Journal of Neuroscience, 2018
We tested the hypothesis that arm/hand motor recovery after injury of the lateral sensorimotor cortex is associated with upregulation of the corticoreticular projection (CRP) from the supplementary motor cortex (M2) to the gigantocellular reticular nucleus of the medulla (Gi). Three groups of rhesus monkeys of both genders were studied: five controls, four cases with lesions of the arm/hand area of the primary motor cortex (M1) and the lateral premotor cortex (LPMC; F2 lesion group), and five cases with lesions of the arm/hand area of M1, LPMC, S1, and anterior parietal cortex (F2P2 lesion group). CRP strength was assessed using high-resolution anterograde tracers injected into the arm/hand area of M2 and stereology to estimate of the number of synaptic boutons in the Gi. M2 projected bilaterally to the Gi, primarily targeting the medial Gi subsector and, to a lesser extent, lateral, dorsal, and ventral subsectors. Total CRP bouton numbers were similar in controls and F2 lesion cases but F2P2 lesion cases had twice as many boutons as the other two groups (p ϭ 0.0002). Recovery of reaching and fine hand/digit function was strongly correlated with estimated numbers of CRP boutons in the F2P2 lesion cases. Because we previously showed that F2P2 lesion cases experience decreased strength of the M2 corticospinal projection (CSP), whereas F2 lesion monkeys experienced increased strength of the M2 CSP, these results suggest one mechanism underlying arm/hand motor recovery after F2P2 injury is upregulation of the M2 CRP. This M2-CRP response may influence an important reticulospinal tract contribution to upper-limb motor recovery following frontoparietal injury.
Journal of comparative neurology, 2015
Upper extremity hemiplegia is a common consequence of unilateral cortical stroke. Understanding the role of the unaffected cerebral hemisphere in the motor recovery process has been encouraged, in part, by the presence of ipsilateral corticospinal projections. We examined the neuroplastic response of the ipsilateral corticospinal projection (iCSP) from the contralesional primary motor cortex (cM1) hand/arm area to spinal levels C5-T1 after spontaneous long-term recovery from isolated frontal lobe injury and isolated frontoparietal injury. High-resolution tract tracing, stereological, and behavioral methodologies were applied. Recovery from frontal motor injury resulted in enhanced numbers of terminal labeled boutons in the iCSP from cM1 compared to controls. Increases occurred in lamina VIII and the adjacent ventral sectors of lamina VII, which are involved in axial/proximal limb sensorimotor processing. Larger frontal lobe lesions were associated with greater numbers of terminal boutons than smaller frontal lobe lesions. In contrast, frontoparietal injury blocked this response, as total bouton number was similar to controls, demonstrating that disruption of somatosensory input to one hemisphere has a suppressive effect on the iCSP from the non-lesioned hemisphere. However, compared to controls, elevated bouton numbers occurred in lamina VIII, at the expense of lamina VII bouton labeling. Lamina IX boutons were also elevated in two frontoparietal lesion cases with extensive cortical injury. Since lamina VIII and IX collectively harbor axial, proximal, and distal motoneurons, therapeutic
Dexterous Hand Movements and Their Recovery After Central Nervous System Injury
Annual Review of Neuroscience, 2019
Hand dexterity has uniquely developed in higher primates and is thought to rely on the direct corticomotoneuronal (CM) pathway. Recent studies have shown that rodents and carnivores lack the direct CM pathway but can control certain levels of dexterous hand movements through various indirect CM pathways. Some homologous pathways also exist in higher primates, and among them, propriospinal (PrS) neurons in the mid-cervical segments (C3-C4) are significantly involved in hand dexterity. When the direct CM pathway was lesioned caudal to the PrS and transmission of cortical commands to hand motoneurons via the PrS neurons remained intact, dexterous hand movements could be significantly recovered. This recovery model was intensively studied, and it was found that, in addition to the compensation by the PrS neurons, a large-scale reorganization in the bilateral cortical motor-related areas and mesolimbic structures contributed to recovery. Future therapeutic strategies should target these ...
Experimental Brain Research, 2019
We tested the hypothesis that injury to frontoparietal sensorimotor areas causes greater initial impairments in performance and poorer recovery of ipsilesional dexterous hand/finger movements than lesions limited to frontal motor areas in rhesus monkeys. Reaching and grasping/manipulation of small targets with the ipsilesional hand were assessed for 6-12 months post-injury using two motor tests. Initial post-lesion motor skill and long-term recovery of motor skill were compared in two groups of monkeys: (1) F2 group-five cases with lesions of arm areas of primary motor cortex (M1) and lateral premotor cortex (LPMC) and (2) F2P2 group-five cases with F2 lesions + lesions of arm areas of primary somatosensory cortex and the anterior portion of area 5. Initial post-lesion reach and manipulation skills were similar to or better than pre-lesion skills in most F2 lesion cases in a difficult fine motor task but worse than pre-lesion skill in most F2P2 lesion cases in all tasks. Subsequently, reaching and manipulation skills improved over the post-lesion period to higher than pre-lesion skills in both groups, but improvements were greater in the F2 lesion group, perhaps due to additional task practice and greater ipsilesional limb use for daily activities. Poorer and slower post-lesion improvement of ipsilesional upper limb motor skill in the F2P2 cases may be due to impaired somatosensory processing. The persistent ipsilesional upper limb motor deficits frequently observed in humans after stroke are probably caused by greater subcortical white and gray matter damage than in the localized surgical injuries studied here.
The Journal of comparative neurology, 2015
Concurrent damage to the lateral frontal and parietal cortex is common following middle cerebral artery infarction, leading to upper extremity paresis, paresthesia, and sensory loss. Motor recovery is often poor, and the mechanisms that support or impede this process are unclear. Since the medial wall of the cerebral hemisphere is commonly spared following stroke, we investigated the spontaneous long-term (6 and 12 month) effects of lateral frontoparietal injury (F2P2 lesion) on the terminal distribution of the corticospinal projection (CSP) from intact, ipsilesional supplementary motor cortex (M2) at spinal levels C5 to T1. Isolated injury to the frontoparietal arm/hand region resulted in a significant loss of contralateral corticospinal boutons from M2 compared with controls. Specifically, reductions occurred in the medial and lateral parts of lamina VII and the dorsal quadrants of lamina IX. There were no statistical differences in the ipsilateral CSP. Contrary to isolated latera...
Proceedings of the National Academy of Sciences of the United States of America, 2017
The direct cortico-motoneuronal connection is believed to be essential for the control of dexterous hand movements, such as precision grip in primates. It was reported, however, that even after lesion of the corticospinal tract (CST) at the C4-C5 segment, precision grip largely recovered within 1-3 mo, suggesting that the recovery depends on transmission through intercalated neurons rostral to the lesion, such as the propriospinal neurons (PNs) in the midcervical segments. To obtain direct evidence for the contribution of PNs to recovery after CST lesion, we applied a pathway-selective and reversible blocking method using double viral vectors to the PNs in six monkeys after CST lesions at C4-C5. In four monkeys that showed nearly full or partial recovery, transient blockade of PN transmission after recovery caused partial impairment of precision grip. In the other two monkeys, CST lesions were made under continuous blockade of PN transmission that outlasted the entire period of post...
Cortical Reorganization Allows for Motor Recovery after Crossed Cerebrocerebellar Atrophy
Journal of Neuroimaging, 2004
The authors report the case of a 33-year-old woman who exhibited, at the age of 17, a left-sided hemiplegia, which was followed by good motor recovery, though with a permanent deficit in fine finger movements. She had a widespread loss of neural tissue in the right hemisphere (crossed cerebrocerebellar atrophy), including marked atrophy and thinning of the precentral and postcentral gyri; (2) widespread deep white matter destruction, including the corticospinal tract; and (3) crossed cerebellar atrophy. Except over the supplementary motor area (SMA), transcranial magnetic stimulation did not elicit motor evoked potentials in the affected hand. Nevertheless, during opening and closing of the affected hand, functional magnetic resonance imaging
The Journal of Comparative Neurology, 2009
To examine neuroanatomical mechanisms underlying fine motor control of the primate hand, adult Rhesus monkeys underwent injections of biotinylated dextran amine (BDA) into the right motor cortex. Spinal axonal anatomy was examined using detailed serial-section reconstruction and modified stereological quantification. 87% of corticospinal tract (CST) axons decussated in the medullary pyramids and descended through the contralateral dorsolateral tract of the spinal cord. 11% of CST axons projected through the dorsolateral CST ipsilateral to the hemisphere of origin, and 2% of axons projected through the ipsilateral ventromedial CST. Notably, corticospinal axons decussated extensively across the spinal cord midline. Remarkably, nearly twofold more CST axons decussated across the cervical spinal cord midline (~12,000 axons) than were labeled in all descending components of the CST (~6,700 axons). These findings suggest that CST axons extend multiple segmental collaterals. Furthermore, serial-section reconstructions revealed that individual axons descending in either the ipsilateral or contralateral dorsolateral CST can: 1) terminate in the gray matter ipsilateral to the hemisphere of origin; 2) terminate in the gray matter contralateral to the hemisphere of origin; or 3) branch in the spinal cord and terminate on both sides of the spinal cord. These results reveal a previously unappreciated degree of bilaterality and complexity of corticospinal projections in the primate spinal cord. This bilaterality is more extensive than that of the rat CST, and may resemble human CST organization. Thus, augmentation of sprouting of these extensive bilateral CST projections may provide a novel target for enhancing recovery after spinal cord injury.
Contralesional Hemisphere Control of the Proximal Paretic Upper Limb following Stroke
Cerebral Cortex, 2012
Cathodal transcranial direct current stimulation (c-tDCS) can reduce excitability of neurons in primary motor cortex (M1) and may facilitate motor recovery after stroke. However, little is known about the neurophysiological effects of tDCS on proximal upper limb function. We hypothesized that suppression of contralesional M1 (cM1) excitability would produce neurophysiological effects that depended on the severity of upper limb impairment. Twelve patients with varying upper limb impairment after subcortical stroke were assessed on clinical scales of upper limb spasticity, impairment, and function. Magnetic resonance imaging was used to determine lesion size and fractional anisotropy (FA) within the posterior limbs of the internal capsules indicative of corticospinal tract integrity. Excitability within paretic M1 biceps brachii representation was determined from motor-evoked potentials during selective isometric tasks, after cM1 sham stimulation and after c-tDCS. These neurophysiological data indicate that c-tDCS improved selective proximal upper limb control for mildly impaired patients and worsened it for moderate to severely impaired patients. The direction of the neurophysiological after effects of c-tDCS was strongly related to upper limb spasticity, impairment, function, and FA asymmetry between the posterior limbs of the internal capsules. These results indicate systematic variation of cM1 for proximal upper limb control after stroke and that suppression of cM1 excitability is not a ''one size fits all'' approach.
Experimental Neurology, 2015
The corticospinal and rubrospinal tracts are the predominant tracts for controlling skilled hand function. Injuries to these tracts impair grasping but not gross motor functions such as overground locomotion. The aim of the present study was to determine whether or not, after damage to both the corticospinal and rubrospinal tracts, other spared subcortical motor pathway can mediate the recovery of skilled hand function. Adult rats received a bilateral injury to the corticospinal tract at the level of the medullar pyramids and a bilateral ablation of the rubrospinal axons at C4. One group of rats received, acutely after injury, two injections of chondroitinase-ABC at C7, and starting at 7 days post-injury were enrolled in daily reaching and grasping rehabilitation (CHASE group, n = 5). A second group of rats received analogous injections of ubiquitous penicillinase, and did not undergo rehabilitation (PEN group, n = 5). Compared to rats in the PEN group, CHASE rats gradually recovered the ability to reach and grasp over 42 days after injury. Overground locomotion was mildly affected after injury and both groups followed similar recovery. Since the reticulospinal tract plays a predominant role in motor control, we further investigated whether or not plasticity of this pathway could contribute to the animal's recovery. Reticulospinal axons were anterogradely traced in both groups of rats. The density of reticulospinal processes in both the normal and ectopic areas of the grey ventral matter of the caudal segments of the cervical spinal cord was greater in the CHASE than PEN group. The results indicate that after damage to spinal tracts that normally mediate the control of reaching and grasping in rats other complementary spinal tracts can acquire the role of those damaged tracts and promote task-specific recovery.