Training the "less-affected" forelimb after unilateral cortical infarcts interferes with functional recovery of the impaired forelimb in rats
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Abstract:
Unilateral lesions of the sensorimotor cortex (SMC) in adult rats cause major behavioral changes in the ipsilesional, "less-affected" forelimb. An increase in function and reliance on this forelimb can aid compensation for contralesional impairments, but may also promote disuse and reduced functionality of the impaired forelimb. We hypothesized that training focused on the ipsilesional forelimb following a unilateral SMC lesion would reduce the efficacy of later motor rehabilitative training of the impaired forelimb.Rats with ischemic SMC lesions were trained on a skilled reaching task with the ipsilesional forelimb (PriorT) or received control procedures (Cont) for 10 days. Both groups were then trained with the impaired forelimb on the same reaching task for 10 days.In comparison with Cont, PriorT rats had little improvement on the reaching task with the impaired forelimb and had a more enduring disuse of the impaired forelimb for postural support behaviors. Lesion sizes were similar between groups.Behavioral experience with the less-affected forelimb early after unilateral SMC lesions has the potential to increase disuse and dysfunction of the impaired forelimb, consistent with a training-induced exacerbation of learned non-use. These findings are suggestive of competitive processes in experience-dependent neural restructuring after brain damage.Keywords:
Forelimb
Dogs were trained for tonic forelimb flexion fixed to a lever in order to hold a cup with meat during eating, when the head was bent down to a foodwell. Before learning, the forelimb flexion is accompanied by the anticipatory lifting of the head bent down to the foodwell; following lowering of the head leads to an extension of the flexed forelimb. Simultaneous holding of the flexed forelimb and lowered head is achieved by learning. During the original learning, the innate head-forelimb coordination was rearranged into the opposite one. After the initial instrumental learning, the "working" forelimb was changed to test whether a transfer of the learned head-forelimb coordination would occur. It was shown that the execution of the instrumental reaction by the untrained forelimb was impossible, because the innate coordination between the head and this forelimb persisted. It could also be rearranged by learning. The involvement of the motor cortex in the unilateral rearrangement of the innate head-forelimb movement coordination is discussed.
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Lever
Tonic (physiology)
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Background: Advanced age is a leading risk factor for stroke and is associated with worse recovery. The goal of post-stroke rehabilitative therapies is to enhance neuroplasticity to support the recovery of motor function. Recent studies indicate that vagus nerve stimulation (VNS) paired with rehabilitative training drives robust plasticity and results in significantly enhanced recovery of forelimb function in multiple models of brain injury in young rats. Advanced age may interfere with the benefits of VNS by reducing the capacity for plasticity. Here were evaluate the ability of VNS to drive neuroplasticity and improve forelimb recovery after stroke in aged subjects, and we examine mechanisms that may underlie recovery. Methods: In the first set of experiments, aged (16 mo. old) rats performed an automated forelimb task and then were trained for 5 days with (n = 2) or without VNS (n = 2) paired with forelimb movement. Movement representations were then assayed using ICMS. In the second set of experiments, aged rats were trained on the isometric force task and then received a cortical ischemic lesion and VNS cuff electrode. Rats underwent 6 weeks of rehabilitative training with (n = 8) or without paired VNS (n = 9). At the end of testing, rats received an injection of biotinylated dextran amine into the contralesional motor cortex to label corticospinal tract (CST) projections from the unlesioned hemisphere. Results: Early findings suggest that VNS paired with motor training results in a 244 ± 104% increase in forelimb representation compared to training alone in the motor cortex of aged rats. After stroke, VNS paired with rehabilitative results in significantly enhanced motor recovery compared to extensive rehabilitative training without VNS in aged rats. Rats that receive VNS+Rehab display 100 ± 7% recovery of forelimb strength compared to a 56 ± 14% recovery in rats that receive Rehab alone. Preliminary results indicate that VNS promotes increased connectivity of the CST from the unlesioned hemisphere to the denervated side of the spinal cord. Conclusions: VNS significantly enhances neuroplasticity and post-stroke recovery in aged rats. The VNS-dependent increase in recovery may be supported by reorganization of CST projections from the unlesioned motor cortex.
Forelimb
Stroke
Corticospinal tract
Vagus Nerve Stimulation
Biotinylated dextran amine
Stroke Recovery
Brain stimulation
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Traumatic injury to the adult human spinal cord most frequently occurs at the mid-to-low cervical segments and produces tetraplegia. To investigate treatments for improving upper extremity function after cervical spinal cord injury (SCI), three behavioral tests were examined for their potential usefulness in evaluating forelimb function in an adult rat model that mimics human low cervical SCI. Testing was conducted pre- and up to 4 weeks post-operation in adult female rats subjected to either contusion injury at the C7 spinal cord segment or sham-surgery. Modified Forelimb Tarlov scales revealed significant proximal and distal forelimb extension dysfunction in lesion rats at l-to-4 weeks post-cervical SCI. The Forelimb Grip Strength Test showed a significant decrease in forelimb grip strength of lesion rats throughout the 4 weeks post-cervical SCI. Significant deficits in reach and pellet retrieval by lesion rats were measured at l-to-4 weeks post-cervical SCI with the conditioned pellet retrieval Staircase Test. The results demonstrate that these qualitative and quantitative forelimb behavioral tests can be used to evaluate forelimb function following low cervical SCI and may be useful to investigate treatments for improving forelimb function in these lesions.
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Forelimb
Rhizotomy
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Forelimb skeletal muscle and skin glucose uptake during Escherichia coli endotoxin shock in the dog.
We previously demonstrated an increase in gracilis muscle glucose uptake during endotoxin shock in the dog. The present study was completed to investigate this phenomenon in forelimb skeletal muscle and skin. The isolated forelimb preparation was used. Mongrel dogs were anesthetized with nembutal and heparinized. Shock was induced by i.v. infusion of E. coli endotoxin. When isolated forelimb temperature was maintained at contralateral intact forelimb temperature (which was always the same as core temperature), forelimb skeletal muscle and skin glucose uptake increased by 30 minutes of shock, and remained above control for the 4 hour shock period. Total forelimb blood flow decreased and the limb became severely hypoxic (mean venous PO2 = 24 mmHg). However, when the isolated forelimb temperature was not artificially maintained at contralateral intact forelimb temperature (same as core temperature), the isolated forelimb temperature fell approximately 3 degrees C and the elevation of glucose uptake was not observed. Although forelimb blood flow decreased to the same level as in the temperature controlled group, the forelimbs were only moderately hypoxic. This study emphasizes the important influence of temperature on tissue metabolism and the recognition of its importance in experimental data interpretation, especially when metabolic variables are involved. It also demonstrates that changes in glucose uptake during shock are similar in dog forelimb skeletal muscle, provided that changes in muscle temperature are similar.
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Gracilis muscle
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Unilateral injury to the forelimb representation area of the sensorimotor cortex (FL-SMC) in adult rats causes over-reliance on the unimpaired forelimb for postural-motor movements, as well as overgrowth of layer V pyramidal cell dendrites in the homotopic cortex of the noninjured hemisphere. The overgrowth appears to be use-dependent because it can be prevented by restricting movements of the unimpaired forelimb. Additionally, restricting the unimpaired forelimb in animals with FL-SMC damage results in significantly greater behavioral dysfunction when examined 2 d after cast removal (compared to that after impaired-limb immobilization, or no limb immobilization). In the present study, the long-term behavioral and anatomical effects of limb immobilization were examined. Animals with FL-SMC lesions were fitted with casts immediately after the lesion that immobilized the impaired forelimb, the unimpaired forelimb, or neither forelimb for 15 d. Immobilization of the nonimpaired forelimb resulted in chronic prevention of dendritic growth and severe and chronic behavioral deficits. In addition, immobilization of the nonimpaired forelimb resulted in a dramatic exaggeration of the neuronal injury, presumably attributable to forced overuse of the impaired limb. Immobilization of the impaired forelimb resulted in no detectable neural changes and in only slightly increased and longer-lasting behavioral asymmetries (compared to nonimmobilized, lesioned animals), presumably attributable to mild disuse of the impaired limb. Immobilization of a single forelimb in nonlesioned rats resulted in no significant behavioral or anatomical changes. Together, these results suggest that although behavioral experience can enhance neural growth after brain injury, the region surrounding the injury may be vulnerable to behavioral pressure during the early postlesion period.
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Unilateral lesions of the sensorimotor cortex (SMC) in adult rats cause major behavioral changes in the ipsilesional, "less-affected" forelimb. An increase in function and reliance on this forelimb can aid compensation for contralesional impairments, but may also promote disuse and reduced functionality of the impaired forelimb. We hypothesized that training focused on the ipsilesional forelimb following a unilateral SMC lesion would reduce the efficacy of later motor rehabilitative training of the impaired forelimb.Rats with ischemic SMC lesions were trained on a skilled reaching task with the ipsilesional forelimb (PriorT) or received control procedures (Cont) for 10 days. Both groups were then trained with the impaired forelimb on the same reaching task for 10 days.In comparison with Cont, PriorT rats had little improvement on the reaching task with the impaired forelimb and had a more enduring disuse of the impaired forelimb for postural support behaviors. Lesion sizes were similar between groups.Behavioral experience with the less-affected forelimb early after unilateral SMC lesions has the potential to increase disuse and dysfunction of the impaired forelimb, consistent with a training-induced exacerbation of learned non-use. These findings are suggestive of competitive processes in experience-dependent neural restructuring after brain damage.
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Abstract Earlier studies in primates have demonstrated a double representation of the distal forelimb in area 4. In this study intracortical stimulation was used to map the representation of the forelimb in area 4 of the cat. Maps of individual animals revealed two spatially separate representations for the distal forelimb in area 4. Two “digit zones.” regions in which threshold stimulation evoked contractions limited to digit musculature, were seen in all animals. Although the absolute location of the two digit zones varied among animals, the zones were always separated by a field in which more proximal musculature was represented. In some experiments EMG activity was monitored from selected forelimb muscles in order to determine the muscles represented in the two zones. Activity of the same digit muscle could be evoked by stimulation in each digit zone. This analysis demonstrated that some digit muscles were represented in both the digit zones. Thus, this study demonstrates that multiple representation of the distal forelimb in area 4 is not an isolated species‐specific phenomenon, but is likely to be a generalized pattern of motor cortex organization.
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Numerical digit
Representation
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