Chapter 3 - Toward a whole-body neuroprosthetic

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Abstract

Brain–machine interfaces (BMIs) hold promise for the restoration of body mobility in patients suffering from devastating motor deficits caused by brain injury, neurological diseases, and limb loss. Considerable progress has been achieved in BMIs that enact arm movements, and initial work has been done on BMIs for lower limb and trunk control. These developments put Duke University Center for Neuroengineering in the position to develop the first BMI for whole-body control. This whole-body BMI will incorporate very large-scale brain recordings, advanced decoding algorithms, artificial sensory feedback based on electrical stimulation of somatosensory areas, virtual environment representations, and a whole-body exoskeleton. This system will be first tested in nonhuman primates and then transferred to clinical trials in humans.

Introduction

Brain–machine interfaces (BMIs) (Andersen et al., 2004, Birbaumer and Cohen, 2007, Fetz, 2007, Lebedev and Nicolelis, 2006, Nicolelis, 2001, Nicolelis and Lebedev, 2009, Schwartz et al., 2006, Wessberg et al., 2000) offer a translational solution to the problem of restoring mobility to millions of people who suffer from paralysis caused by neurological injuries, neurodegenerative diseases, or limb loss (Paddock, 2009). Only limited treatment options are available to these patients, and often their condition cannot be improved or ameliorated (Dobkin and Havton, 2004, Fouad and Pearson, 2004). BMIs hold promise to revolutionize the treatment of paralysis, as they strive to repair the damaged neural circuitry by bypassing the site of the lesion and establishing direct neural control of artificial tools by the activity of intact brain areas, such as the primary motor cortex (M1), which in many cases remain capable of generating motor commands despite being disconnected from the body effectors (Mattia et al., 2009). BMI research has expanded rapidly during the past decade (Lebedev and Nicolelis, 2006, Nicolelis and Lebedev, 2009), generating high expectations for potential clinical applications. Proof-of-concept BMIs have been tested in rodents (Chapin et al., 1999), nonhuman primates (Carmena et al., 2003, Moritz et al., 2008, Taylor et al., 2002, Velliste et al., 2008, Wessberg et al., 2000), and human subjects (Allison et al., 2007, Birbaumer and Cohen, 2007, Hochberg et al., 2006, Kennedy and Bakay, 1998, Patil et al., 2004, Pfurtscheller and Neuper, 2006). BMI systems developed at the Duke University Center for Neuroengineering (DUCN) during the past 12 years have made it possible to control many motor functions by neuronal ensemble activity recorded with chronic implants, ranging from arm reaching and grasping movements (Carmena et al., 2003, Lebedev et al., 2005, Wessberg et al., 2000) to bipedal locomotion (Cheng, Hyon, et al., 2007, Fitzsimmons et al., 2009). Moreover, recently we have demonstrated for the first time brain–machine–brain interfaces (BMBIs) that incorporate somatosensory feedback loops that transmit information from the actuator to the brain (O'Doherty et al., 2009, O'Doherty et al., 2010). These developments have put us in the position to develop the first whole-body neuroprosthetic for severely paralyzed patients.

Section snippets

Whole-body neuroprosthetic

Previous BMI studies focused predominantly on behavioral tasks in which an artificial actuator enacted upper extremity movements, such as reaching and grasping. Except for a few studies (Fitzsimmons et al., 2009, Pfurtscheller et al., 2006, Prilutsky et al., 2005), virtually no attempts have been made to translate BMI technology to tasks enacting motor functionality of lower extremities and the trunk. Yet, deficits or the complete loss of the ability to walk presents a considerable problem for

BMI components

The basic components of a BMI system are exemplified by the now classical paradigm that enacts direct control of robotic arm reaching movements based on the combined cortical activity of hundreds of cortical neurons (Carmena et al., 2003, Lebedev and Nicolelis, 2006, Lebedev et al., 2005, Nicolelis and Lebedev, 2009, Wessberg et al., 2000). In this BMI paradigm, the electrical activity of large populations of motor cortical neurons is recorded by chronically implanted multielectrode arrays and

Large-scale neuronal recordings

The major prerequisite for the performance of a neuroprosthetic device to be versatile, accurate, and stable, and to allow simultaneous motor control of both lower and upper extremities, is that multiple brain areas should be implanted and large-scale neuronal activity sampled from those areas simultaneously during operation of a whole-body BMI (Nicolelis and Lebedev, 2009, Nicolelis et al., 2003). During the past two decades, advanced electrophysiological methods have allowed recording from

BMI decoders

The success of any BMI system depends to a significant degree on the choice of BMI decoders that extract motor parameters from the sample of neuronal electrical activity recorded in real time. In our current studies, online processing of large-scale brain activity is achieved through an integrated BMI suite that incorporates the recording and stimulation hardware, as well as a computer cluster employed for all real-time processing of the massive stream of neurophysiological data generated in

Bimanual control

A whole-body neuroprosthetic will have to enable independent control of two prosthetic arms. Such BMI control has not been achieved before. The majority of BMIs developed so far involved only a single actuator (computer cursor or a robotic arm) that enacted arm reaching movements under the control of the subject's brain activity. We are currently exploring the use of BMIs for bimanual actuator control. As in other applications, the starting point in developing a bimanual BMI is to understand

Bipedal locomotion

Our laboratory pioneered BMIs that reproduce kinematics of leg movements during bipedal locomotion (Fitzsimmons et al., 2009). Previously, both BMI research and neurophysiological studies in awake, behaving monkeys focused predominantly on the behavioral tasks that involved arm movements and arm representation in the brain. Neurophysiology of lower extremity control has been virtually neglected in nonhuman primates. Yet, a complete loss of the ability to walk is commonly caused by spinal cord

Posture and balance

Whole-body neuroprosthetics will not only have to produce stereotypical stepping but also adapt to postural control. As an advancement toward this goal, we have developed a proof-of-concept BMI for postural control (Tate et al., 2009). In these experiments, monkeys first learned to maintain an upright posture on a platform. Then, the platform moved abruptly, generating a postural perturbation. The platform was driven either periodically, allowing the animal to anticipate the upcoming

Functional electrical stimulation

FES that activates the subject's own muscles may be implemented in future whole-body neuroprosthetics. FES devices have been already introduced to clinical practice as therapies for leg paralysis (Barbeau et al., 2002, Dobkin, 2007, Peckham et al., 1988, Thrasher and Popovic, 2008) along with robotic orthoses (Colombo et al., 2000, Dollar and Herr, 2008, Ferris et al., 2007). The first publications on a FES device for helping to achieve an upright posture date back to the 1960s (Kantrowitz, 1960

Sensorized neuroprosthetic

Recently, we have reported our findings on the first BMBI. Such a paradigm expands on traditional BMIs by adding an artificial somatosensory feedback channel that can deliver artificially created tactile signals, generated by either real sensors placed in a robotic hand or virtual ones added to an avatar arm, directly to the somatosensory cortex, via ICMS. In our first study on this subject (Fitzsimmons et al., 2007), we investigated whether multichannel ICMS of S1 could be discriminated by owl

A whole-body exoskeleton

In our research program, the definitive demonstration of a whole-body neuroprosthetic will involve a subject that is able to use his/her VLSBA to control movements of an exoskeleton that encases the entire body. Currently, we have all components needed for this demonstration. We have demonstrated BMIs for arm reaching and leg locomotion in separate experiments. We have also implanted leg and arm representations of the sensorimotor cortex in both hemispheres (Winans et al., 2010). The

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