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Emergence of a stable cortical map for neuroprosthetic control.

ABSTRACT: Cortical control of neuroprosthetic devices is known to require neuronal adaptations. It remains unclear whether a stable cortical representation for prosthetic function can be stored and recalled in a manner that mimics our natural recall of motor skills. Especially in light of the mixed evidence for a stationary neuron-behavior relationship in cortical motor areas, understanding this relationship during long-term neuroprosthetic control can elucidate principles of neural plasticity as well as improve prosthetic function. Here, we paired stable recordings from ensembles of primary motor cortex neurons in macaque monkeys with a constant decoder that transforms neural activity to prosthetic movements. Proficient control was closely linked to the emergence of a surprisingly stable pattern of ensemble activity, indicating that the motor cortex can consolidate a neural representation for prosthetic control in the presence of a constant decoder. The importance of such a cortical map was evident in that small perturbations to either the size of the neural ensemble or to the decoder could reversibly disrupt function. Moreover, once a cortical map became consolidated, a second map could be learned and stored. Thus, long-term use of a neuroprosthetic device is associated with the formation of a cortical map for prosthetic function that is stable across time, readily recalled, resistant to interference, and resembles a putative memory engram.

SUBMITTER: Ganguly K

PROVIDER: S-EPMC2702684 | biostudies-literature | 2009 Jul

REPOSITORIES: biostudies-literature

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Emergence of a stable cortical map for neuroprosthetic control.

Ganguly Karunesh K Carmena Jose M JM

PLoS biology 20090721 7

Cortical control of neuroprosthetic devices is known to require neuronal adaptations. It remains unclear whether a stable cortical representation for prosthetic function can be stored and recalled in a manner that mimics our natural recall of motor skills. Especially in light of the mixed evidence for a stationary neuron-behavior relationship in cortical motor areas, understanding this relationship during long-term neuroprosthetic control can elucidate principles of neural plasticity as well as ...[more]

PMID: 19621062

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Project description:BackgroundParalysis or amputation of an arm results in the loss of the ability to orient the hand and grasp, manipulate, and carry objects, functions that are essential for activities of daily living. Brain-machine interfaces could provide a solution to restoring many of these lost functions. We therefore tested whether an individual with tetraplegia could rapidly achieve neurological control of a high-performance prosthetic limb using this type of an interface.MethodsWe implanted two 96-channel intracortical microelectrodes in the motor cortex of a 52-year-old individual with tetraplegia. Brain-machine-interface training was done for 13 weeks with the goal of controlling an anthropomorphic prosthetic limb with seven degrees of freedom (three-dimensional translation, three-dimensional orientation, one-dimensional grasping). The participant's ability to control the prosthetic limb was assessed with clinical measures of upper limb function. This study is registered with ClinicalTrials.gov, NCT01364480.FindingsThe participant was able to move the prosthetic limb freely in the three-dimensional workspace on the second day of training. After 13 weeks, robust seven-dimensional movements were performed routinely. Mean success rate on target-based reaching tasks was 91·6% (SD 4·4) versus median chance level 6·2% (95% CI 2·0-15·3). Improvements were seen in completion time (decreased from a mean of 148 s [SD 60] to 112 s [6]) and path efficiency (increased from 0·30 [0·04] to 0·38 [0·02]). The participant was also able to use the prosthetic limb to do skilful and coordinated reach and grasp movements that resulted in clinically significant gains in tests of upper limb function. No adverse events were reported.InterpretationWith continued development of neuroprosthetic limbs, individuals with long-term paralysis could recover the natural and intuitive command signals for hand placement, orientation, and reaching, allowing them to perform activities of daily living.FundingDefense Advanced Research Projects Agency, National Institutes of Health, Department of Veterans Affairs, and UPMC Rehabilitation Institute.

Project description:A neuroprosthesis using a brain-machine interface (BMI) is a promising therapeutic option for severely paralyzed patients, but the ability to control it may vary among individual patients and needs to be evaluated before any invasive procedure is undertaken. We have developed a neuroprosthetic hand that can be controlled by magnetoencephalographic (MEG) signals to noninvasively evaluate subjects' ability to control a neuroprosthesis.Six nonparalyzed subjects performed grasping or opening movements of their right hand while the slow components of the MEG signals (SMFs) were recorded in an open-loop condition. The SMFs were used to train two decoders to infer the timing and types of movement by support vector machine and Gaussian process regression. The SMFs were also used to calculate estimated slow cortical potentials (eSCPs) to identify the origin of motor information. Finally, using the trained decoders, the subjects controlled a neuroprosthetic hand in a closed-loop condition.The SMFs in the open-loop condition revealed movement-related cortical field characteristics and successfully inferred the movement type with an accuracy of 75.0 ± 12.9% (mean ± SD). In particular, the eSCPs in the sensorimotor cortex contralateral to the moved hand varied significantly enough among the movement types to be decoded with an accuracy of 76.5 ± 10.6%, which was significantly higher than the accuracy associated with eSCPs in the ipsilateral sensorimotor cortex (58.1 ± 13.7%; p = 0.0072, paired two-tailed Student's t-test). Moreover, another decoder using SMFs successfully inferred when the accuracy was the greatest. Combining these two decoders allowed the neuroprosthetic hand to be controlled in a closed-loop condition.Use of real-time MEG signals was shown to successfully control the neuroprosthetic hand. The developed system may be useful for evaluating movement-related slow cortical potentials of severely paralyzed patients to predict the efficacy of invasive BMI.

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Emergence of a stable cortical map for neuroprosthetic control.

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Emergence of a stable cortical map for neuroprosthetic control.

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