Dataset Information

Encoding of Both Reaching and Grasping Kinematics in Dorsal and Ventral Premotor Cortices.

ABSTRACT: Classically, it has been hypothesized that reach-to-grasp movements arise from two discrete parietofrontal cortical networks. As part of these networks, the dorsal premotor cortex (PMd) has been implicated in the control of reaching movements of the arm, whereas the ventral premotor cortex (PMv) has been associated with the control of grasping movements of the hand. Recent studies have shown that such a strict delineation of function along anatomical boundaries is unlikely, partly because reaching to different locations can alter distal hand kinematics and grasping different objects can affect kinematics of the proximal arm. Here, we used chronically implanted multielectrode arrays to record unit-spiking activity in both PMd and PMv simultaneously while rhesus macaques engaged in a reach-to-grasp task. Generalized linear models were used to predict the spiking activity of cells in both areas as a function of different kinematic parameters, as well as spike history. To account for the influence of reaching on hand kinematics and vice versa, we applied demixed principal components analysis to define kinematics synergies that maximized variance across either different object locations or grip types. We found that single cells in both PMd and PMv encode the kinematics of both reaching and grasping synergies, suggesting that this classical division of reach and grasp in PMd and PMv, respectively, does not accurately reflect the encoding preferences of cells in those areas.SIGNIFICANCE STATEMENT For reach-to-grasp movements, the dorsal premotor cortex (PMd) has been implicated in the control of reaching movements of the arm, whereas the ventral premotor cortex (PMv) has been associated with the control of grasping movements of the hand. We recorded unit-spiking activity in PMd and PMv simultaneously while macaques performed a reach-to-grasp task. We modeled the spiking activity of neurons as a function of kinematic parameters and spike history. We applied demixed principal components analysis to define kinematics synergies. We found that single units in both PMd and PMv encode the kinematics of both reaching and grasping synergies, suggesting that the division of reach and grasp in PMd and PMv, respectively, cannot be made based on their encoding properties.

SUBMITTER: Takahashi K

PROVIDER: S-EPMC5320606 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Publications

Encoding of Both Reaching and Grasping Kinematics in Dorsal and Ventral Premotor Cortices.

Takahashi Kazutaka K Best Matthew D MD Huh Noah N Brown Kevin A KA Tobaa Adil A AA Hatsopoulos Nicholas G NG

The Journal of neuroscience : the official journal of the Society for Neuroscience 20170111 7

Classically, it has been hypothesized that reach-to-grasp movements arise from two discrete parietofrontal cortical networks. As part of these networks, the dorsal premotor cortex (PMd) has been implicated in the control of reaching movements of the arm, whereas the ventral premotor cortex (PMv) has been associated with the control of grasping movements of the hand. Recent studies have shown that such a strict delineation of function along anatomical boundaries is unlikely, partly because reachi ...[more]

PMID: 28077725

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Project description:A prominent feature of motor cortex field potentials during movement is a distinctive low-frequency local field potential (lf-LFP) (<4 Hz), referred to as the movement event-related potential (mEP). The lf-LFP appears to be a global signal related to regional synaptic input, but its relationship to nearby output signaled by single unit spiking activity (SUA) or to movement remains to be established. Previous studies comparing information in primary motor cortex (MI) lf-LFPs and SUA in the context of planar reaching tasks concluded that lf-LFPs have more information than spikes about movement. However, the relative performance of these signals was based on a small number of simultaneously recorded channels and units, or for data averaged across sessions, which could miss information of larger-scale spiking populations. Here, we simultaneously recorded LFPs and SUA from two 96-microelectrode arrays implanted in two major motor cortical areas, MI and ventral premotor (PMv), while monkeys freely reached for and grasped objects swinging in front of them. We compared arm end point and grip aperture kinematics' decoding accuracy for lf-LFP and SUA ensembles. The results show that lf-LFPs provide enough information to reconstruct kinematics in both areas with little difference in decoding performance between MI and PMv. Individual lf-LFP channels often provided more accurate decoding of single kinematic variables than any one single unit. However, the decoding performance of the best single unit among the large population usually exceeded that of the best single lf-LFP channel. Furthermore, ensembles of SUA outperformed the pool of lf-LFP channels, in disagreement with the previously reported superiority of lf-LFP decoding. Decoding results suggest that information in lf-LFPs recorded from intracortical arrays may allow the reconstruction of reach and grasp for real-time neuroprosthetic applications, thus potentially supplementing the ability to decode these same features from spiking populations.

Project description:BACKGROUND:Active upper-limb prostheses are used to restore important hand functionalities, such as grasping. In conventional approaches, a pattern recognition system is trained over a number of static grasping gestures. However, training a classifier in a static position results in lower classification accuracy when performing dynamic motions, such as reach-to-grasp. We propose an electromyography-based learning approach that decodes the grasping intention during the reaching motion, leading to a faster and more natural response of the prosthesis. METHODS AND RESULTS:Eight able-bodied subjects and four individuals with transradial amputation gave informed consent and participated in our study. All the subjects performed reach-to-grasp motions for five grasp types, while the elecromyographic (EMG) activity and the extension of the arm were recorded. We separated the reach-to-grasp motion into three phases, with respect to the extension of the arm. A multivariate analysis of variance (MANOVA) on the muscular activity revealed significant differences among the motion phases. Additionally, we examined the classification performance on these phases. We compared the performance of three different pattern recognition methods; Linear Discriminant Analysis (LDA), Support Vector Machines (SVM) with linear and non-linear kernels, and an Echo State Network (ESN) approach. Our off-line analysis shows that it is possible to have high classification performance above 80% before the end of the motion when with three-grasp types. An on-line evaluation with an upper-limb prosthesis shows that the inclusion of the reaching motion in the training of the classifier importantly improves classification accuracy and enables the detection of grasp intention early in the reaching motion. CONCLUSIONS:This method offers a more natural and intuitive control of prosthetic devices, as it will enable controlling grasp closure in synergy with the reaching motion. This work contributes to the decrease of delays between the user's intention and the device response and improves the coordination of the device with the motion of the arm.

Dataset Information

Encoding of Both Reaching and Grasping Kinematics in Dorsal and Ventral Premotor Cortices.

Publications

Encoding of Both Reaching and Grasping Kinematics in Dorsal and Ventral Premotor Cortices.

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