Dataset Information

Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices.

ABSTRACT: 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.

SUBMITTER: Bansal AK

PROVIDER: S-EPMC3075284 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices.

Bansal Arjun K AK Vargas-Irwin Carlos E CE Truccolo Wilson W Donoghue John P JP

Journal of neurophysiology 20110127 4

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 contex ...[more]

PMID: 21273313

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Project description: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.

Project description:Interactions between the ventral premotor (PMv) and the primary motor cortex (M1) are crucial for transforming an object's geometrical properties, such as its size and shape, into a motor command suitable for grasp of the object. Recently, we showed that PMv interacts with M1 in a specific fashion, depending on the hand posture. However, the functional connectivity between PMv and M1 during the preparation of an actual grasp is still unknown. To address this issue, PMv-M1 interactions were tested while subjects were preparing to grasp different visible objects requiring either a precision grip or a whole hand grasp. A conditioning-test transcranial magnetic stimulation (TMS) paradigm was used: a test stimulus was applied over M1 either in isolation or after a conditioning stimulus delivered, at different delays, over the ipsilateral PMv. Motor evoked potentials (MEPs) were recorded in the first dorsal interosseus and abductor digiti minimi muscles, which show highly differentiated activity according to grasp. While subjects prepared to grasp, delivering a conditioning PMv pulse 6 or 8msec before a test pulse over M1 strikingly facilitated MEPs in the specific muscles that were used in the upcoming grasp. This degree of facilitation correlated with the amount of muscle activity used later in the trial to grasp the objects. The present results demonstrate that, during grasp preparation, the PMv-M1 interactions are muscle-specific. PMv appears to process the object geometrical properties relevant for the upcoming grasp, and transmits this information to M1, which in turn generates a motor command appropriate for the grasp. We also reveal that the grasp-specific facilitation resulting from PMv-M1 interactions is differently related to the upcoming grasp muscle activity than is that from paired-pulse stimulation over M1, suggesting that these two TMS paradigms assess the excitability of cortico-cortical pathways devoted to the control of grasp at two different levels.

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.

Dataset Information

Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices.

Publications

Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices.

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