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Primary motor cortex underlies multi-joint integration for fast feedback control.

ABSTRACT: A basic difficulty for the nervous system is integrating locally ambiguous sensory information to form accurate perceptions about the outside world. This local-to-global problem is also fundamental to motor control of the arm, because complex mechanical interactions between shoulder and elbow allow a particular amount of motion at one joint to arise from an infinite combination of shoulder and elbow torques. Here we show, in humans and rhesus monkeys, that a transcortical pathway through primary motor cortex (M1) resolves this ambiguity during fast feedback control. We demonstrate that single M1 neurons of behaving monkeys can integrate shoulder and elbow motion information into motor commands that appropriately counter the underlying torque within about 50 milliseconds of a mechanical perturbation. Moreover, we reveal a causal link between M1 processing and multi-joint integration in humans by showing that shoulder muscle responses occurring ?50 milliseconds after pure elbow displacement can be potentiated by transcranial magnetic stimulation. Taken together, our results show that transcortical processing through M1 permits feedback responses to express a level of sophistication that rivals voluntary control; this provides neurophysiological support for influential theories positing that voluntary movement is generated by the intelligent manipulation of sensory feedback.

SUBMITTER: Pruszynski JA

PROVIDER: S-EPMC4974074 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Primary motor cortex underlies multi-joint integration for fast feedback control.

Pruszynski J Andrew JA Kurtzer Isaac I Nashed Joseph Y JY Omrani Mohsen M Brouwer Brenda B Scott Stephen H SH

Nature 20110928 7369

A basic difficulty for the nervous system is integrating locally ambiguous sensory information to form accurate perceptions about the outside world. This local-to-global problem is also fundamental to motor control of the arm, because complex mechanical interactions between shoulder and elbow allow a particular amount of motion at one joint to arise from an infinite combination of shoulder and elbow torques. Here we show, in humans and rhesus monkeys, that a transcortical pathway through primary ...[more]

PMID: 21964335

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Project description:The brain must coordinate with redundant bodies to perform motion tasks. The aim of the present study is to propose a novel control model that predicts the characteristics of human joint coordination at a behavioral level. To evaluate the joint coordination, an uncontrolled manifold (UCM) analysis that focuses on the trial-to-trial variance of joints has been proposed. The UCM is a nonlinear manifold associated with redundant kinematics. In this study, we directly applied the notion of the UCM to our proposed control model called the "UCM reference feedback control." To simplify the problem, the present study considered how the redundant joints were controlled to regulate a given target hand position. We considered a conventional method that pre-determined a unique target joint trajectory by inverse kinematics or any other optimization method. In contrast, our proposed control method generates a UCM as a control target at each time step. The target UCM is a subspace of joint angles whose variability does not affect the hand position. The joint combination in the target UCM is then selected so as to minimize the cost function, which consisted of the joint torque and torque change. To examine whether the proposed method could reproduce human-like joint coordination, we conducted simulation and measurement experiments. In the simulation experiments, a three-link arm with a shoulder, elbow, and wrist regulates a one-dimensional target of a hand through proposed method. In the measurement experiments, subjects performed a one-dimensional target-tracking task. The kinematics, dynamics, and joint coordination were quantitatively compared with the simulation data of the proposed method. As a result, the UCM reference feedback control could quantitatively reproduce the difference of the mean value for the end hand position between the initial postures, the peaks of the bell-shape tangential hand velocity, the sum of the squared torque, the mean value for the torque change, the variance components, and the index of synergy as well as the human subjects. We concluded that UCM reference feedback control can reproduce human-like joint coordination. The inference for motor control of the human central nervous system based on the proposed method was discussed.

Project description:The integration of sensory inputs in the motor cortex is crucial for dexterous movement. We recently demonstrated that a closed-loop control based on the feedback provided through intraneural multichannel electrodes implanted in the median and ulnar nerves of a participant with upper limb amputation improved manipulation skills and increased prosthesis embodiment. Here we assessed, in the same participant, whether and how selective intraneural sensory stimulation also elicits a measurable cortical activation and affects sensorimotor cortical circuits. After estimating the activation of the primary somatosensory cortex evoked by intraneural stimulation, sensorimotor integration was investigated by testing the inhibition of primary motor cortex (M1) output to transcranial magnetic stimulation, after both intraneural and perineural stimulation. Selective sensory intraneural stimulation evoked a low-amplitude, 16 ms-latency, parietal response in the same area of the earliest component evoked by whole-nerve stimulation, compatible with fast-conducting afferent fibre activation. For the first time, we show that the same intraneural stimulation was also capable of decreasing M1 output, at the same time range of the short-latency afferent inhibition effect of whole-nerve superficial stimulation. The inhibition generated by the stimulation of channels activating only sensory fibres was stronger than that due to intraneural or perineural stimulation of channels activating mixed fibres. We demonstrate in a human subject that the cortical sensorimotor integration inhibiting M1 output previously described after the experimental whole-nerve stimulation is present also with a more ecological selective sensory fibre stimulation. KEY POINTS: Cortical integration of sensory inputs is crucial for dexterous movement. Short-latency somatosensory afferent inhibition of motor cortical output is typically produced by peripheral whole-nerve stimulation. We exploited intraneural multichannel electrodes used to provide sensory feedback for prosthesis control to assess whether and how selective intraneural sensory stimulation affects sensorimotor cortical circuits in humans. Activation of the primary somatosensory cortex (S1) was explored by recording scalp somatosensory evoked potentials. Sensorimotor integration was tested by measuring the inhibitory effect of the afferent stimulation on the output of the primary motor cortex (M1) generated by transcranial magnetic stimulation. We demonstrate in humans that selective intraneural sensory stimulation elicits a measurable activation of S1 and that it inhibits the output of M1 at the same time range of whole-nerve superficial stimulation.

Project description:UNLABELLED:Oscillations in the beta and gamma bands (13-30 Hz; 35-70 Hz) have often been observed in motor cortical outputs that reach the spinal cord, acting on motoneurons and interneurons. However, the frequencies of these oscillations are above the muscle force frequency range. A current view is that the transformation of the motoneuron pool inputs into force is linear. For this reason possible roles for these oscillations are unclear, since if this transformation is linear, the high frequencies in the motoneuron inputs (e.g., 20 Hz from pyramidal tract neurons) would be filtered out by the muscle and have no effect on force control. A biologically inspired mathematical model of the neuromuscular system was used to investigate the impact of high-frequency cortical oscillatory activity on force control. The model simulation results evidenced that a typical motoneuron pool has a nonlinear behavior that enables the decoding of a high-frequency oscillatory input. An input at a single frequency (e.g., beta band) leads to an increase in the steady-state force generated by the muscle. When the input oscillation was amplitude modulated at a given low frequency, the force oscillated at this frequency. In both cases, the mechanism relies on the recruitment and derecruitment of motor units in response to the oscillatory descending drive. Therefore, the results from this study suggest a potential role in force control for cortical oscillations at frequencies at or above the beta band, despite the low-pass behavior of the muscles. SIGNIFICANCE STATEMENT:The role of cortical oscillations in motor control has been a long-standing question, one view being that they are an epiphenomenon. Fast oscillations are known to reach the spinal cord, and hence they have been thought to affect muscle behavior. However, experimental limitations have hampered further advances to explain how they could influence muscle force. An approach for such a challenge was adopted in the present research: to study the problem through computer simulations of an advanced biologically compatible mathematical model. Using such a model, we found that the well-known mechanism of recruitment and derecruitment of the spinal cord motoneurons can allow the muscle to respond to cortical oscillations, suggesting that these oscillations are not epiphenomena in motor control.

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Primary motor cortex underlies multi-joint integration for fast feedback control.

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Primary motor cortex underlies multi-joint integration for fast feedback control.

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