Coupling the neural and physical dynamics in rhythmic movements

A pair of coupled oscillators simulating a central pattern generator (CPG) interacting with a pendular limb were numerically integrated. The CPG was represented as a van der Pol oscillator and the pendular limb was modeled as a linearized, hybrid spring-pendulum system. The CPG oscillator drove the pendular limb while the pendular limb modulated the frequency of the CPG. Three results were observed. First, sensory feedback influenced the oscillation frequency of the coupled system. The oscillation frequency was lower in the absence of sensory feedback. Moreover, if the muscle gain was decreased, thereby decreasing the oscillation amplitude of the pendular limb and indirectly lowering the effect of sensory feedback, the oscillation frequency decreased monotonically. This is consistent with experimental data (Williamson and Roberts 1986). Second, the CPG output usually led the angular displacement of the pendular limb by a phase of 90° regardless of the length of the limb. Third, the frequency of the coupled system tuned itself to the resonant frequency of the pendular limb. Also, the frequency of the coupled system was highly resistant to changes in the endogenous frequency of the CPG. The results of these simulations support the view that motor behavior emerges from the interaction of the neural dynamics of the nervous system and the physical dynamics of the periphery

Exploiting Multiple Sensory Modalities in Brain-Machine Interfaces

Recent improvements in cortically-controlled brain-machine interfaces (BMIs) have raised hopes that such technologies may improve the quality of life of severely motor-disabled patients. However, current generation BMIs do not perform up to their potential due to the neglect of the full range of sensory feedback in their strategies for training and control. Here we confirm that neurons in the primary motor cortex (MI) encode sensory information and demonstrate a significant heterogeneity in their responses with respect to the type of sensory modality available to the subject about a reaching task. We further show using mutual information and directional tuning analyses that the presence of multi-sensory feedback (i.e. vision and proprioception) during replay of movements evokes neural responses in MI that are almost indistinguishable from those responses measured during overt movement. Finally, we suggest how these playback-evoked responses may be used to improve BMI performance

Neuronal interactions improve cortical population coding of movement direction

Journal ArticleInteractions among groups of neurons in primary motor cortex (MI) may convey information about motor behavior. We investigated the information carried by interactions in MI of macaque monkeys using a novel multielectrode array to record simultaneously from 12-16 neurons during an arm-reaching task. Pairs of simultaneously recorded cells revealed significant correlations in their trial-to-trial firing rate variation when estimated over broad (600 msec) time intervals. This covariation was only weakly related to the preferred directions of the individual MI neurons estimated from the firing rate and did not vary significantly with interelectrode distance. Most significantly, in a portion of cell pairs, correlation strength varied with the direction of the arm movement. We evaluated to what extent correlated activity provided additional information about movement direction beyond that available in single neuron firing rate. A multivariate statistical model successfully classified direction from single trials of neural data. However, classification was consistently better when correlations were incorporated into the model as compared to one in which neurons were treated as independent encoders. Information-theoretic analysis demonstrated that interactions caused by correlated activity carry additional information about movement direction beyond that based on the firing rates of independently acting neurons. These results also show that cortical representations incorporating higher order features of population activity would be richer than codes based solely on firing rate, if such information can exploited by the nervous system

Temporal Evolution of Both Premotor and Motor Cortical Tuning Properties Reflect Changes in Limb Biomechanics

A prevailing theory in the cortical control of limb movement posits that premotor cortex initiates a high-level motor plan that is transformed by the primary motor cortex (MI) into a low-level motor command to be executed. This theory implies that the premotor cortex is shielded from the motor periphery and therefore its activity should not represent the low-level features of movement. Contrary to this theory, we show that both dorsal (PMd) and ventral premotor (PMv) cortices exhibit population-level tuning properties that reflect the biomechanical properties of the periphery similar to those observed in M1. We recorded single-unit activity from M1, PMd, and PMv and characterized their tuning properties while six rhesus macaques performed a reaching task in the horizontal plane. Each area exhibited a bimodal distribution of preferred directions during execution consistent with the known biomechanical anisotropies of the muscles and limb segments. Moreover, these distributions varied in orientation or shape from planning to execution. A network model shows that such population dynamics are linked to a change in biomechanics of the limb as the monkey begins to move, specifically to the state-dependent properties of muscles. We suggest that, like M1, neural populations in PMd and PMv are more directly linked with the motor periphery than previously thought

Improving Brain–Machine Interface Performance by Decoding Intended Future Movements

Objective. A brain–machine interface (BMI) records neural signals in real time from a subject\u27s brain, interprets them as motor commands, and reroutes them to a device such as a robotic arm, so as to restore lost motor function. Our objective here is to improve BMI performance by minimizing the deleterious effects of delay in the BMI control loop. We mitigate the effects of delay by decoding the subject\u27s intended movements a short time lead in the future. Approach. We use the decoded, intended future movements of the subject as the control signal that drives the movement of our BMI. This should allow the user\u27s intended trajectory to be implemented more quickly by the BMI, reducing the amount of delay in the system. In our experiment, a monkey (Macaca mulatta) uses a future prediction BMI to control a simulated arm to hit targets on a screen. Main Results. Results from experiments with BMIs possessing different system delays (100, 200 and 300 ms) show that the monkey can make significantly straighter, faster and smoother movements when the decoder predicts the user\u27s future intent. We also characterize how BMI performance changes as a function of delay, and explore offline how the accuracy of future prediction decoders varies at different time leads. Significance. This study is the first to characterize the effects of control delays in a BMI and to show that decoding the user\u27s future intent can compensate for the negative effect of control delay on BMI performance

Incorporating Feedback from Multiple Sensory Modalities Enhances Brain–Machine Interface Control

The brain typically uses a rich supply of feedback from multiple sensory modalities to control movement in healthy individuals. In many individuals, these afferent pathways, as well as their efferent counterparts, are compromised by disease or injury resulting in significant impairments and reduced quality of life. Brain–machine interfaces (BMIs) offer the promise of recovered functionality to these individuals by allowing them to control a device using their thoughts. Most current BMI implementations use visual feedback for closed-loop control; however, it has been suggested that the inclusion of additional feedback modalities may lead to improvements in control. We demonstrate for the first time that kinesthetic feedback can be used together with vision to significantly improve control of a cursor driven by neural activity of the primary motor cortex (MI). Using an exoskeletal robot, the monkey\u27s arm was moved to passively follow a cortically controlled visual cursor, thereby providing the monkey with kinesthetic information about the motion of the cursor. When visual and proprioceptive feedback were congruent, both the time to successfully reach a target decreased and the cursor paths became straighter, compared with incongruent feedback conditions. This enhanced performance was accompanied by a significant increase in the amount of movement-related information contained in the spiking activity of neurons in MI. These findings suggest that BMI control can be significantly improved in paralyzed patients with residual kinesthetic sense and provide the groundwork for augmenting cortically controlled BMIs with multiple forms of natural or surrogate sensory feedback

Spatio-Temporal Patterning in Primary Motor Cortex at Movement Onset

Voluntary movement initiation involves the engagement of large populations of motor cortical neurons around movement onset. Despite knowledge of the temporal dynamics that lead to movement, the spatial structure of these dynamics across the cortical surface remains unknown. In data from 4 rhesus macaques, we show that the timing of attenuation of beta frequency local field potential oscillations, a correlate of locally activated cortex, forms a spatial gradient across primary motor cortex (MI). We show that these spatio-temporal dynamics are recapitulated in the engagement order of ensembles of MI neurons. We demonstrate that these patterns are unique to movement onset and suggest that movement initiation requires a precise spatio-temporal sequential activation of neurons in MI

Comparing Offline Decoding Performance in Physiologically Defined Neuronal Classes

Objective: Recently, several studies have documented the presence of a bimodal distribution of spike waveform widths in primary motor cortex. Although narrow and wide spiking neurons, corresponding to the two modes of the distribution, exhibit different response properties, it remains unknown if these differences give rise to differential decoding performance between these two classes of cells. Approach: We used a Gaussian mixture model to classify neurons into narrow and wide physiological classes. Using similar-size, random samples of neurons from these two physiological classes, we trained offline decoding models to predict a variety of movement features. We compared offline decoding performance between these two physiologically defined populations of cells. Main results: We found that narrow spiking neural ensembles decode motor parameters better than wide spiking neural ensembles including kinematics, kinetics, and muscle activity. Significance: These findings suggest that the utility of neural ensembles in brain machine interfaces may be predicted from their spike waveform widths