Impaired reach-to-grasp kinematics in parkinsonian patients relates to dopamine-dependent, subthalamic beta bursts.
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ABSTRACT:
SUBMITTER: Vissani M
PROVIDER: S-EPMC8242004 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundExaggerated oscillatory activity in the beta frequency band in the subthalamic nucleus has been suggested to be related to bradykinesia in Parkinson's disease (PD). However, studies seeking correlations between such activity in the local field potential and motor performance have been limited to the immediate postoperative period, which may be confounded by a stun effect that leads to the temporary alleviation of PD deficits.MethodsLocal field potentials were recorded simultaneously with motor performance in PD patients several months after neurostimulator implantation. This was enabled by the chronic implantation of a pulse generator with the capacity to record and transmit local field potentials from deep brain stimulation electrodes. Specifically, we investigated oscillatory beta power dynamics and objective measures of bradykinesia during an upper limb alternating pronation and supination task in 9 patients.ResultsAlthough beta power was suppressed during continuously repeated movements, this suppression progressively diminished over time in tandem with a progressive decrement in the frequency and amplitude of movements. The relationship between changes within local field potentials and movement parameters was significant across patients, and not present for theta/alpha frequencies (5-12 Hz). Change in movement frequency furthermore related to beta power dynamics within patients.ConclusionsChanges in beta power are linked to changes in movement performance and the sequence effect of bradykinesia months after neurostimulator implantation. These findings provide further evidence that beta power may serve as a biomarker for bradykinesia and provide a suitable substrate for feedback control in chronic adaptive deep brain stimulation. © 2017 The Authors. Movement Disorders published by Wiley Periodicals, Inc. on behalf of International Parkinson and Movement Disorder Society.
| S-EPMC5575541 | biostudies-literature
Project description:No biomarker of Parkinson's disease exists that allows clinicians to adjust chronic therapy, either medication or deep brain stimulation, with real-time feedback. Consequently, clinicians rely on time-intensive, empirical, and subjective clinical assessments of motor behaviour and adverse events to adjust therapies. Accumulating evidence suggests that hypokinetic aspects of Parkinson's disease and their improvement with therapy are related to pathological neural activity in the beta band (beta oscillopathy) in the subthalamic nucleus. Additionally, effectiveness of deep brain stimulation may depend on modulation of the dorsolateral sensorimotor region of the subthalamic nucleus, which is the primary site of this beta oscillopathy. Despite the feasibility of utilizing this information to provide integrated, biomarker-driven precise deep brain stimulation, these measures have not been brought together in awake freely moving individuals. We sought to directly test whether stimulation-related improvements in bradykinesia were contingent on reduction of beta power and burst durations, and/or the volume of the sensorimotor subthalamic nucleus that was modulated. We recorded synchronized local field potentials and kinematic data in 16 subthalamic nuclei of individuals with Parkinson's disease chronically implanted with neurostimulators during a repetitive wrist-flexion extension task, while administering randomized different intensities of high frequency stimulation. Increased intensities of deep brain stimulation improved movement velocity and were associated with an intensity-dependent reduction in beta power and mean burst duration, measured during movement. The degree of reduction in this beta oscillopathy was associated with the improvement in movement velocity. Moreover, the reduction in beta power and beta burst durations was dependent on the theoretical degree of tissue modulated in the sensorimotor region of the subthalamic nucleus. Finally, the degree of attenuation of both beta power and beta burst durations, together with the degree of overlap of stimulation with the sensorimotor subthalamic nucleus significantly explained the stimulation-related improvement in movement velocity. The above results provide direct evidence that subthalamic nucleus deep brain stimulation-related improvements in bradykinesia are related to the reduction in beta oscillopathy within the sensorimotor region. With the advent of sensing neurostimulators, this beta oscillopathy combined with lead location could be used as a marker for real-time feedback to adjust clinical settings or to drive closed-loop deep brain stimulation in freely moving individuals with Parkinson's disease.
| S-EPMC8240742 | biostudies-literature
Project description:Gamma synchronization increases during movement and scales with kinematic parameters. Here, disease-specific characteristics of this synchronization and the dopamine-dependence of its scaling in Parkinson's disease are investigated. In 16 patients undergoing deep brain stimulation surgery, movements of different velocities revealed that subthalamic gamma power peaked in the sensorimotor part of the subthalamic nucleus, correlated positively with maximal velocity and negatively with symptom severity. These effects relied on movement-related bursts of transient synchrony in the gamma band. The gamma burst rate highly correlated with averaged power, increased gradually with larger movements and correlated with symptom severity. In the dopamine-depleted state, gamma power and burst rate significantly decreased, particularly when peak velocity was slower than ON medication. Burst amplitude and duration were unaffected by the medication state. We propose that insufficient recruitment of fast gamma bursts during movement may underlie bradykinesia as one of the cardinal symptoms in Parkinson's disease.
| S-EPMC5819947 | biostudies-literature
Project description:BackgroundCurrent approaches to characterizing deficits in upper limb movements after stroke typically focus either on changes in a functional measure, for example, how well a patient can complete a task, or changes in impairment, for example, isolated measurements of joint range of motion. However, there can be notable dissociations between static measures of impairment versus those of function.ObjectiveWe develop a method to measure upper limb joint angles during performance of a functional task and use measurements to characterize joint impairment in the context of a functional task.MethodsWe developed a sensorized glove that can precisely measure select finger, hand, and arm joints while participants complete a functional reach-to-grasp task involving manipulation of a sensorized object.ResultsWe first characterized the accuracy and precision of the glove's joint angle measurements. We then measured joint angles in neurologically intact participants (n = 4 participants, 8 limbs) to define the expected distribution of joint angle variation during task execution. These distributions were used to normalize finger, hand, and arm joint angles in stroke participants (n = 6) as they performed the task. We present a participant-specific visualization of functional joint angle variance which illustrated that stroke participants with nearly identical clinical scores exhibited unique patterns of joint angle variation.ConclusionsOverall, measuring individual joint angles in the context of a functional task may inform whether changes in functional scores over recovery or rehabilitation are driven by changes in impairment or the development of compensatory strategies, and provide a quantified path toward personalized rehabilitative therapy.
| S-EPMC10330436 | biostudies-literature
Project description:Beta frequency oscillations (15 to 35 Hz) in cortical and basal ganglia circuits become abnormally synchronized in Parkinson's disease (PD). How excessive beta oscillations emerge in these circuits is unclear. We addressed this issue by defining the firing properties of basal ganglia neurons around the emergence of cortical beta bursts (? bursts), transient (50 to 350 ms) increases in the beta amplitude of cortical signals. In PD patients, the phase locking of background spiking activity in the subthalamic nucleus (STN) to frontal electroencephalograms preceded the onset and followed the temporal profile of cortical ? bursts, with conditions of synchronization consistent within and across bursts. Neuronal ensemble recordings in multiple basal ganglia structures of parkinsonian rats revealed that these dynamics were recapitulated in STN, but also in external globus pallidus and striatum. The onset of consistent phase-locking conditions was preceded by abrupt phase slips between cortical and basal ganglia ensemble signals. Single-unit recordings demonstrated that ensemble-level properties of synchronization were not underlain by changes in firing rate but, rather, by the timing of action potentials in relation to cortical oscillation phase. Notably, the preferred angle of phase-locked action potential firing in each basal ganglia structure was shifted during burst initiation, then maintained stable phase relations during the burst. Subthalamic, pallidal, and striatal neurons engaged and disengaged with cortical ? bursts to different extents and timings. The temporal evolution of cortical and basal ganglia synchronization is cell type-selective, which could be key for the generation/ maintenance of excessive beta oscillations in parkinsonism.
| S-EPMC6690030 | biostudies-literature
Project description:ObjectivePhasic bursts of beta band synchronisation have been linked to motor impairment in Parkinson's disease (PD). However, little is known about what terminates bursts.MethodsWe used the Hilbert-Huang transform to investigate beta bursts in the local field potential recorded from the subthalamic nucleus in nine patients with PD on and off levodopa.ResultsThe sharpness of the beta waveform extrema fell as burst amplitude dropped. Conversely, an index of phase slips between waveform extrema, and the power of concurrent theta activity increased as burst amplitude fell. Theta activity was also increased on levodopa when beta bursts were attenuated. These phenomena were associated with reduction in coupling between beta phase and high gamma activity amplitude. We discuss how these findings may suggest that beta burst termination is associated with relative desynchronization of the beta drive, increase in competing theta activity and increased phase slips in the beta activity.ConclusionsWe characterise the dynamical nature of beta bursts, thereby permitting inferences about underlying activities and, in particular, about why bursts terminate.SignificanceUnderstanding the dynamical nature of beta bursts may help point to interventions that can cause their termination and potentially treat motor impairment in PD.
| S-EPMC7115847 | biostudies-literature
Project description:The subthalamic nucleus (STN) receives a dopaminergic innervation from the substantia nigra pars compacta, but the role of this projection remains poorly understood, particularly in primates. To address this issue, we used immuno-electron microscopy to localize D1, D2, and D5 dopamine receptors in the STN of rhesus macaques and studied the electrophysiological effects of activating D1-like or D2-like receptors in normal and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated parkinsonian monkeys. Labeling of D1 and D2 receptors was primarily found presynaptically, on preterminal axons and putative glutamatergic and GABAergic terminals, while D5 receptors were more significantly expressed postsynaptically, on dendritic shafts of STN neurons. The electrical spiking activity of STN neurons, recorded with standard extracellular recording methods, was studied before, during, and after intra-STN administration of the dopamine D1-like receptor agonist SKF82958, the D2-like receptor agonist quinpirole, or artificial cerebrospinal fluid (control injections). In normal animals, administration of SKF82958 significantly reduced the spontaneous firing but increased the rate of intraburst firing and the proportion of pause-burst sequences of firing. Quinpirole only increased the proportion of such pause-burst sequences in STN neurons of normal monkeys. In MPTP-treated monkeys, the D1-like receptor agonist also reduced the firing rate and increased the proportion of pause-burst sequences, while the D2-like receptor agonist did not change any of the chosen descriptors of the firing pattern of STN neurons. Our data suggest that dopamine receptor activation can directly modulate the electrical activity of STN neurons by pre- and postsynaptic mechanisms in both normal and parkinsonian states, predominantly via activation of D1 receptors.
| S-EPMC4064409 | biostudies-literature
Project description:The aim of the present study was to investigate the effect of Tai Chi (TC) and mental imagery (MI) on motor performance. MI is the ability of representing different types of images and it can be improved through constant practice (e.g., of TC). The majority of previous literature has mainly investigated the impact of this mental factor by means of qualitative indexes, whereas studies considering more rigorous measures such as kinematic parameters are rare. In this vein, little is known about how MI can affect reach-to-grasp, one of the most studied models in kinematic research. The present study attempts to fill that gap by investigating the relationship between MI and motor performance in TC, a practice that largely promotes the adoption of mental training. One TC master, four instructors, ten apprentices and fifteen untrained participants were requested to reach toward and grasp an object while mentally representing one out of five different images related to water with an increasing degree of dynamicity and expansion (i.e., still water, flowing water, wave, whirlpool, and opening water flower). Kinematic profiles of movements were recorded by means of six infra-red cameras using a 3-D motion analysis system. We tested whether: (i) focusing on MI during the task would help in optimizing motor efficiency, and (ii) expertise in TC would be reflected in higher flexibility during the task. The results indicate that kinematics is highly sensitive to MI and TC practice. In particular, our main finding suggests a statistically significant general improvement in motor efficiency for the TC group and a beneficial effect for all the participants when focusing on the most expansive image (i.e., opening water flower). Moreover, regression analysis indicates that MI and TC practice make online control more flexible in an experience-based way. These results have important implications for the use of mental imagery and TC in the retraining of motor function in people with physical disabilities.
| S-EPMC7161419 | biostudies-literature
Project description:Various movement parameters of grasping movements, like velocity or type of the grasp, have been successfully decoded from neural activity. However, the question of movement event detection from brain activity, that is, decoding the time at which an event occurred (e.g. movement onset), has been addressed less often. Yet, this may be a topic of key importance, as a brain-machine interface (BMI) that controls a grasping prosthesis could be realized by detecting the time of grasp, together with an optional decoding of which type of grasp to apply. We, therefore, studied the detection of time of grasps from human ECoG recordings during a sequence of natural and continuous reach-to-grasp movements. Using signals recorded from the motor cortex, a detector based on regularized linear discriminant analysis was able to retrieve the time-point of grasp with high reliability and only few false detections. Best performance was achieved using a combination of signal components from time and frequency domains. Sensitivity, measured by the amount of correct detections, and specificity, represented by the amount of false detections, depended strongly on the imposed restrictions on temporal precision of detection and on the delay between event detection and the time the event occurred. Including neural data from after the event into the decoding analysis, slightly increased accuracy, however, reasonable performance could also be obtained when grasping events were detected 125 ms in advance. In summary, our results provide a good basis for using detection of grasping movements from ECoG to control a grasping prosthesis.
| S-EPMC3554656 | biostudies-literature
Project description:The performance of brain-machine interfaces (BMIs) that continuously control upper limb neuroprostheses may benefit from distinguishing periods of posture and movement so as to prevent inappropriate movement of the prosthesis. Few studies, however, have investigated how decoding behavioral states and detecting the transitions between posture and movement could be used autonomously to trigger a kinematic decoder. We recorded simultaneous neuronal ensemble and local field potential (LFP) activity from microelectrode arrays in primary motor cortex (M1) and dorsal (PMd) and ventral (PMv) premotor areas of two male rhesus monkeys performing a center-out reach-and-grasp task, while upper limb kinematics were tracked with a motion capture system with markers on the dorsal aspect of the forearm, hand, and fingers. A state decoder was trained to distinguish four behavioral states (baseline, reaction, movement, hold), while a kinematic decoder was trained to continuously decode hand end point position and 18 joint angles of the wrist and fingers. LFP amplitude most accurately predicted transition into the reaction (62%) and movement (73%) states, while spikes most accurately decoded arm, hand, and finger kinematics during movement. Using an LFP-based state decoder to trigger a spike-based kinematic decoder [r = 0.72, root mean squared error (RMSE) = 0.15] significantly improved decoding of reach-to-grasp movements from baseline to final hold, compared with either a spike-based state decoder combined with a spike-based kinematic decoder (r = 0.70, RMSE = 0.17) or a spike-based kinematic decoder alone (r = 0.67, RMSE = 0.17). Combining LFP-based state decoding with spike-based kinematic decoding may be a valuable step toward the realization of BMI control of a multifingered neuroprosthesis performing dexterous manipulation.
| S-EPMC3680811 | biostudies-other