Brain injury affecting the frontal motor cortex or its descending axons often causes contralateral upper extremity paresis. Although recovery is variable, the underlying mechanisms supporting favorable motor recovery remain unclear. Since the medial wall of the cerebral hemisphere is often spared following brain injury and recent functional neuroimaging studies in patients indicate a potential role for this brain region in the recovery process, we investigated the long-term effects of isolated lateral frontal motor cortical injury on the corticospinal projection (CSP) from intact, ipsilesional supplementary motor cortex (M2). Following injury to the arm region of the primary motor (M1) and lateral premotor (LPMC) cortices, upper extremity recovery is accompanied by terminal axon plasticity in the contralateral CSP but not the ipsilateral CSP from M2. Furthermore, significant contralateral plasticity occurs only in lamina VII and dorsally within lamina IX. Thus, selective intraspinal sprouting transpires in regions containing interneurons, flexor-related motor neurons and motor neurons supplying intrinsic hand muscles which all play important roles in mediating reaching and digit movements. Following recovery, subsequent injury of M2 leads to reemergence of hand motor deficits. Considering the importance of the CSP in humans and the common occurrence of lateral frontal cortex injury, these findings suggest that spared supplementary motor cortex may serve as an important therapeutic target that should be considered when designing acute and long-term post-injury patient intervention strategies aimed to enhance the motor recovery process following lateral cortical trauma.
We investigated changes across the adult life span of the fingertip forces used to grip and lift objects and their possible causes. Grip force, relative safety margin (grip force exceeding the minimum to avoid slip, as a fraction of slip force), and skin slipperiness increased beginning at age 50 years. Skin slipperiness explained relative safety margin increases until age 60 years. Hence, after age 60 years, additional factors must elevate grip force. We argue that one factor is impaired cutaneous afferent encoding of skin-object frictional properties on the basis of three findings. First, only subjects 60 years and older increased their relative safety margins when the friction of the gripped surfaces was varied randomly versus experiments that varied only object weight. Skin slipperiness did not account for this behavior. Second, these older subjects scaled the initial portion of their force trajectories for the slippery surface during experiments when friction was varied. Third, their grip force adjustments to new surfaces were delayed approximately 100 msec as compared with young subjects. Previous research has demonstrated that friction is signaled locally by fast-adapting afferents (FA I afferents), which decrease in number during old age. By contrast, adjustments triggered by object set-down, an event encoded by FA II afferents throughout the hand and wrist, were not delayed in our old subjects. Other findings included that anticipatory control of fingertip forces using memory of object weight was unimpaired in old age. Finally, old and young adults modulated their fingertip forces with equal smoothness and with similar relative intertrial variability.
Due to the heterogeneous nature of most brain injuries, the contributions of gray and white matter involvement to motor deficits and recovery potential remain obscure. We tested the hypothesis that duration of hand motor impairment and recovery of skilled arm and hand motor function depends on the volume of gray and white matter damage of the frontal lobe. Lesions of the primary motor cortex (M1), M1 + lateral premotor cortex (LPMC), M1 + LPMC + supplementary motor cortex (M2) or multi-focal lesions affecting motor areas and medial prefrontal cortex were evaluated in rhesus monkeys. Fine hand motor function was quantitatively assessed pre-lesion and for 3–12 months post-lesion using two motor tests. White and gray matter lesion volumes were determined using histological and quantitative methods. Regression analyses showed that duration of fine hand motor impairment was strongly correlated (R2 > 0.8) with the volume of gray and white matter lesions, with white matter lesion volume being the primary predictor of impairment duration. Level of recovery of fine hand motor skill was also well correlated (R2 > 0.5) with gray and white matter lesion volume. In some monkeys post-lesion skill exceeded pre-lesion skill in one or both motor tasks demonstrating that continued post-injury task practice can improve motor performance after localized loss of frontal motor cortex. These findings will assist in interpreting acute motor deficits, predicting the time course and expected level of functional recovery, and designing therapeutic strategies in patients with localized frontal lobe injury or neurosurgical resection.
A modified "Klüver" or dexterity board was developed to assess fine control of hand and digit movements by nonhuman primates during the acquisition of small food pellets from wells of different diameter. The primary advantages of the new device over those used previously include standardized positioning of target food pellets and controlled testing of each hand without the need for restraints, thereby allowing the monkey to move freely about the cage. Three-dimensional video analysis of hand motion was used to provide measures of reaching accuracy and grip aperture, as well as temporal measures of reach duration and food-pellet manipulation. We also present a validated performance score based on these measures, which serves as an indicator of successful food-pellet retrieval. Tests in three monkeys show that the performance score is an effective measure with which to study fine motor control associated with learning and handedness. We also show that the device and performance scores are effective for differentiating the effects of localized injury to motor areas of the cerebral cortex.
Old age impairs the ability to form new associations for declarative memory, but the ability to acquire and retain procedural memories remains relatively intact. Thus, it is unclear whether old age affects the ability to learn the visuomotor associations needed to set efficient fingertip forces for handling familiar objects. We studied the ability for human subjects to use visual cues (color) about the mechanical properties (texture or weight) of a grasped object to control fingertip forces during prehension. Old and young adults (mean age 77 years and 22 years, respectively) grasped and lifted an object that varied in texture at the gripped surfaces (experiment 1: sandpaper versus acetate surface materials) or weight (experiment 2: 200 g versus 400 g). The object was color-coded according to the mechanical property in the "visual cue" condition, and the mechanical property varied unpredictably across lifts in the "no visual cue" condition. In experiment 1 (texture), the young adults' grip force (force normal to the gripped surface) when the object lifted from the support surface was 24% smaller when the surfaces were color-coded. The old adults' grip force did not vary between the visual conditions despite their accurate reports of the grip surface colors prior to each lift. Comparable findings were obtained in experiment 2, when object weight was varied and peak grip force rate prior to object lift-off was measured. Furthermore old and young subjects alike used about 2 N of grip force when lifting the 200 g object in experiment 2. Therefore, the old adults' failure to adjust grip force when the color cue was present cannot be attributed to a general inability or unwillingness to use low grip force when handling objects. We conclude that old age affects the associative learning that links visual identification of an object with the fingertip forces for efficiently handling the object. In contrast, old and young subjects' grip force was influenced by the preceding lift, regardless of visual cues, which supports existing theories that multiple internal representations govern predictive control of fingertip forces during prehension.
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