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Motor Neuroprostheses

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ABSTRACT

Neuroprostheses (NPs) are electrical stimulators that activate nerves, either to provide sensory input to the central nervous system (sensory NPs), or to activate muscles (motor NPs: MNPs). The first MNPs were belts with inbuilt batteries and electrodes developed in the 1850s to exercise the abdominal muscles. They became enormously popular among the general public, but as a result of exaggerated therapeutic claims they were soon discredited by the medical community. In the 1950s, MNPs reemerged for the serious purpose of activating paralyzed muscles. Neuromuscular electrical stimulation (NMES), when applied in a preset sequence, is called therapeutic electrical stimulation (TES). NMES timed so that it enhances muscle contraction in intended voluntary movements is called functional electrical stimulation (FES) or functional neuromuscular stimulation (FNS). It has been 50 years since the first FES device, a foot‐drop stimulator, was described and 40 years since the first implantable version was tested in humans. A commercial foot‐drop stimulator became available in the 1970s, but for various reasons, it failed to achieve widespread use. With advances in technology, such devices are now more convenient and reliable. Enhancing upper limb function is a more difficult task, but grasp‐release stimulators have been shown to provide significant benefits. This chapter deals with the technical aspects of NMES, the therapeutic and functional benefits of TES and FES, delayed‐onset and carryover effects attributable to “neuromodulation” and the barriers and opportunities in this rapidly developing field. © 2019 American Physiological Society. Compr Physiol 9:127‐148, 2019.

Figure 1. Figure 1. Basic designs of neural prostheses. (A) A surface stimulator (external pulse generator: EPG) delivers current pulses through the skin via a pair of surface electrodes. In some cases, a wireless controller controls the EPG. (B) An EPG delivers current pulses via one or more conductors, typically insulated wires that pass through the skin and terminate close to or on the nerve. The return current flows through the tissues to a surface (reference) electrode. (C) An EPG delivers current pulses through the skin via a pair of surface electrodes and some of the current is intercepted and “picked up” by a fully implanted lead, which delivers this current to the nerve. (D) An implanted pulse generator (IPG) receives energy and commands wirelessly through the skin and delivers current pulses to the nerve via an electrode. The return current flows through the tissues to a reference electrode on the body of the IPG. (E) An implanted pulse generator (IPG) receives energy and commands wirelessly through the skin and delivers current pulses to the nerve via a pair of electrodes. (F) An injectable microstimulator receives energy and commands wirelessly through the skin and delivers current pulses to the nerve through two conductive terminals on the body of the stimulator.
Figure 2. Figure 2. Four surface foot‐drop stimulators that activate the common peroneal nerve to lift the foot in the swing phase of the locomotor step cycle. (A) The Functional Electrical Peroneal Orthosis (FEPO), commercialized in Europe in the 1970s. (B) The Bioness L300. (C) The Innovative Neurotronics Walkaide. (D) The Bioness L300Go. The FEPO and L300 had underheel switches wirelessly linked to an EPG in a cuff attached below the knee. When the underheel force dropped at the onset of the swing phase, a signal from the switch assembly triggered the EPG to stimulate the nerve via electrodes in the cuff. The Walkaide and Bioness L300Go have a tilt sensor built into the cuff, which is used to trigger stimulation, replacing the underheel switch and allowing users to walk barefoot.
Figure 3. Figure 3. Four surface stimulators that activate muscles in the forearm and hand. (A) The Medtronic Respond physiotherapy stimulator activating the wrist and finger extensors. Preset trains of stimulus pulses were triggered by activating a hand‐held push‐button. Numerous therapeutic stimulators based on this design are commercially available. (B) The EMG‐triggered Neuromove. Weak voluntary contractions are detected via a pair of surface electrodes and this triggers a preset period of stimulation through a pair of electrodes placed orthogonally to the electromyogram electrodes. (C) The Bioness H200. This device comprises a flexible splint with inbuilt electrodes. Trains of stimuli eliciting hand opening and grasp are triggered via a radiofrequency push‐button controller. (D) The Rehabtronics ReGrasp comprises a wristlet garment with inbuilt stimulator/receiver and electrodes. A wireless earpiece detects voluntary head movements and transmits control signals to the wristlet, by which means the user can trigger hand opening or grasp.
Figure 4. Figure 4. Proximal and distal muscle activation in which signals from a microelectrode array implanted in the motor cortex of a tetraplegic man were used to control stimulation through electrodes inserted percutaneously into his upper limb. This enabled him voluntarily to reach out with his weight‐supported arm to drink a mug of coffee and feed himself. Reproduced with permission from ().
Figure 5. Figure 5. Sacral spinal cord targets (segments S2‐S4) for electrical stimulation to improve bladder function. SNS, sacral nerve stimulation; SARS, sacral anterior root stimulation; ISMS, intraspinal microstimulation; PNS, pudendal nerve stimulation; PTNS, percutaneous tibial nerve stimulation; TENS, transcutaneous electrical nerve stimulation; HFNB, high‐frequency stimulation eliciting nerve block (HFNB); SPN, sacral parasympathetic nucleus (activates bladder contractions); ON, Onuf's nucleus; CSN, cranial sensory neuron; DNP, dorsal nerve of the penis (DNP). Reproduced with permission from ().


Figure 1. Basic designs of neural prostheses. (A) A surface stimulator (external pulse generator: EPG) delivers current pulses through the skin via a pair of surface electrodes. In some cases, a wireless controller controls the EPG. (B) An EPG delivers current pulses via one or more conductors, typically insulated wires that pass through the skin and terminate close to or on the nerve. The return current flows through the tissues to a surface (reference) electrode. (C) An EPG delivers current pulses through the skin via a pair of surface electrodes and some of the current is intercepted and “picked up” by a fully implanted lead, which delivers this current to the nerve. (D) An implanted pulse generator (IPG) receives energy and commands wirelessly through the skin and delivers current pulses to the nerve via an electrode. The return current flows through the tissues to a reference electrode on the body of the IPG. (E) An implanted pulse generator (IPG) receives energy and commands wirelessly through the skin and delivers current pulses to the nerve via a pair of electrodes. (F) An injectable microstimulator receives energy and commands wirelessly through the skin and delivers current pulses to the nerve through two conductive terminals on the body of the stimulator.


Figure 2. Four surface foot‐drop stimulators that activate the common peroneal nerve to lift the foot in the swing phase of the locomotor step cycle. (A) The Functional Electrical Peroneal Orthosis (FEPO), commercialized in Europe in the 1970s. (B) The Bioness L300. (C) The Innovative Neurotronics Walkaide. (D) The Bioness L300Go. The FEPO and L300 had underheel switches wirelessly linked to an EPG in a cuff attached below the knee. When the underheel force dropped at the onset of the swing phase, a signal from the switch assembly triggered the EPG to stimulate the nerve via electrodes in the cuff. The Walkaide and Bioness L300Go have a tilt sensor built into the cuff, which is used to trigger stimulation, replacing the underheel switch and allowing users to walk barefoot.


Figure 3. Four surface stimulators that activate muscles in the forearm and hand. (A) The Medtronic Respond physiotherapy stimulator activating the wrist and finger extensors. Preset trains of stimulus pulses were triggered by activating a hand‐held push‐button. Numerous therapeutic stimulators based on this design are commercially available. (B) The EMG‐triggered Neuromove. Weak voluntary contractions are detected via a pair of surface electrodes and this triggers a preset period of stimulation through a pair of electrodes placed orthogonally to the electromyogram electrodes. (C) The Bioness H200. This device comprises a flexible splint with inbuilt electrodes. Trains of stimuli eliciting hand opening and grasp are triggered via a radiofrequency push‐button controller. (D) The Rehabtronics ReGrasp comprises a wristlet garment with inbuilt stimulator/receiver and electrodes. A wireless earpiece detects voluntary head movements and transmits control signals to the wristlet, by which means the user can trigger hand opening or grasp.


Figure 4. Proximal and distal muscle activation in which signals from a microelectrode array implanted in the motor cortex of a tetraplegic man were used to control stimulation through electrodes inserted percutaneously into his upper limb. This enabled him voluntarily to reach out with his weight‐supported arm to drink a mug of coffee and feed himself. Reproduced with permission from ().


Figure 5. Sacral spinal cord targets (segments S2‐S4) for electrical stimulation to improve bladder function. SNS, sacral nerve stimulation; SARS, sacral anterior root stimulation; ISMS, intraspinal microstimulation; PNS, pudendal nerve stimulation; PTNS, percutaneous tibial nerve stimulation; TENS, transcutaneous electrical nerve stimulation; HFNB, high‐frequency stimulation eliciting nerve block (HFNB); SPN, sacral parasympathetic nucleus (activates bladder contractions); ON, Onuf's nucleus; CSN, cranial sensory neuron; DNP, dorsal nerve of the penis (DNP). Reproduced with permission from ().
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Teaching Material

A. Prochazka. Motor Neuroprostheses. Compr Physiol 9: 2019, 127-148.

Didactic Synopsis

Major Teaching Points:

  1. Brief history of electrical stimulation of the nervous system. Electrical stimulation of human peripheral nerves with the use of electrostatic machines for clinical purposes began in the 17th century but only began to be properly understood and applied in the 20th century.
  2. Basic mechanisms and methods of electrical stimulation with neural prostheses (NPs). Methods: Trains of current pulses are applied either with stimulators external to the body connected through pad electrodes applied to the skin, or via implanted stimulators and wire electrodes terminating near or on peripheral nerves or within the central nervous system. Mechanisms: control of the recruitment of nerve axons depends on the amount of charge delivered per current pulse.
  3. Tissue interfaces (surface or implanted electrodes), corrosion, tissue reactions. Electrode corrosion and inflammatory reactions of bodily tissues can occur, depending on the type of electrode, the current and duration of pulses delivered and whether the pulses are monophasic or biphasic.
  4. Types of motor NPs. MNPs either deliver fixed sequences of stimulation for exercise and retraining purposes (therapeutic electrical stimulation: TES), or stimulation triggered by biomechanical events or the user's own electromyographic activity to augment muscle contractions in exercise training, or in functional tasks (functional electrical stimulation: FES).
  5. Lower and upper limb MNPs. Various designs of surface and implanted MNPs have been developed and commercialized to stimulate paralyzed muscles. Influential metastudies have concluded that FES may improve walking, balance and range of motion in hemiplegic people and those with spinal cord injury.
  6. Respiratory MNPs, MNPs for bladder control. There is a surprisingly long history of attempts to stimulate the phrenic nerve for respiration, and various nerves innervating or reflexly affecting the bladder and external urethral sphincter to restore control over micturition. Implanted stimulators for respiration and bladder control are available commercially.
  7. Epidural and intraspinal stimulators. Epidural stimulation of the spinal cord via electrode arrays placed on the dorsal dura mater, originally developed to treat chronic pain, is increasingly being used to restore upper and lower limb movements. Intraspinal stimulation targeting motoneuron pools activating limb muscles or spinal cord nuclei controlling micturition is still in the experimental stages.
  8. Carry-over therapeutic effects and mechanisms. Beneficial carry-over effects lasting up to a few hours are commonly observed after sessions of TES or FES. In some NP applications, long-lasting beneficial effects develop slowly, over days or weeks, and may become permanent.
  9. Barriers to MNP technology transfer. TES stimulators have become inexpensive consumer products, and are widely used. FES devices are much more expensive, because they incorporate sensors and control logic, they are designed to be wearable in daily life, and they are subjected to more stringent regulatory testing. Reimbursement of FES devices is a major barrier to their widespread use.

Didactic Legends

The figures—in a freely downloadable PowerPoint format—can be found on the Images tab along with the formal legends published in the article. The following legends to the same figures are written to be useful for teaching.

Figure 1 Teaching points: Basic designs of neural prostheses. (A) A surface stimulator (also known as an external pulse generator: EPG) delivers current pulses through the skin via a pair of surface electrodes. In some cases, a wireless controller controls the EPG. (B) An EPG delivers current pulses via one or more conductors, typically insulated wires that pass through the skin and terminate close to or on the nerve. The return current flows through the tissues to a surface (reference) electrode. (C) An EPG delivers current pulses through the skin via a pair of surface electrodes and some of the current is intercepted and “picked up” by a fully implanted lead, which delivers this current to the nerve. (D) An implanted pulse generator (IPG) receives energy and commands wirelessly through the skin and delivers current pulses to the nerve via an electrode. The return current flows through the tissues to a reference electrode on the body of the IPG. (E) An implanted pulse generator (IPG) receives energy and commands wirelessly through the skin and delivers current pulses to the nerve via a pair of electrodes. (F) An injectable microstimulator receives energy and commands wirelessly through the skin and delivers current pulses to the nerve through two conductive terminals on the body of the stimulator.

Figure 2 Teaching points: The figure shows four surface foot-drop stimulators that activate the common peroneal nerve to lift the foot in the swing phase of the locomotor step cycle. (A) The Functional Electrical Peroneal Orthosis (FEPO), commercialized in Europe in the 1970s. (B) The Bioness L300. (C) The Innovative Neurotronics Walkaide. (D) The Bioness L300Go. The FEPO and L300 had underheel switches wirelessly linked to an EPG in a cuff attached below the knee. When the under-heel force dropped at the onset of the swing phase, a signal from the switch assembly triggered the EPG to stimulate the nerve via electrodes in the cuff. The Walkaide and Bioness L300Go have a tilt sensor built into the cuff, which is used to trigger stimulation, replacing the under-heel switch and allowing users to walk barefoot.

Figure 3 Teaching points: The figure shows four surface stimulators that activate muscles in the forearm and hand. (A) The Medtronic Respond physiotherapy stimulator activating the wrist and finger extensors. Preset trains of stimulus pulses were triggered by activating a hand-held push-button. Numerous therapeutic stimulators based on this design are commercially available. (B) The Neuromove. In this device, weak voluntary contractions are detected via an electromyogram amplifier connected to a pair of surface electromyogram electrodes and this triggers a pre-set period of stimulation through a pair of electrodes placed orthogonally to the electromyogram electrodes. (C) The Bioness H200. This device comprises a flexible splint with inbuilt electrodes. Trains of stimuli eliciting hand opening and grasp are triggered via a wireless push-button controller. (D) The Rehabtronics ReGrasp comprises a wristlet garment with inbuilt stimulator/receiver and electrodes. A wireless earpiece detects voluntary head movements and transmits control signals to the wristlet, by which means the user can trigger hand opening or grasp.

Figure 4 Teaching points: The figure shows a system in which brain signals recorded from a microelectrode array implanted in the motor cortex of a tetraplegic man were used to control stimulation through electrodes implanted through the skin into muscles in his arm. This enabled him voluntarily to reach out with his weight-supported arm to drink a mug of coffee and feed himself.

Figure 5 Teaching points: The figure shows a variety of sites in the sacral spinal cord and peripheral nerves which have been stimulated electrically to improve bladder function. SNS, sacral nerve stimulation; SARS, sacral anterior root stimulation; ISMS, intraspinal microstimulation; PNS, pudendal nerve stimulation; PTNS, percutaneous tibial nerve stimulation; TENS, transcutaneous electrical nerve stimulation; HFNB, high-frequency stimulation eliciting nerve block (HFNB). The following abbreviations refer to anatomical areas in the central and peripheral nervous system: SPN, sacral parasympathetic nucleus (activates bladder contractions); ON, Onuf's nucleus; CSN, cranial sensory neuron; DNP, dorsal nerve of the penis (DNP).

 


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How to Cite

Arthur Prochazka. Motor Neuroprostheses. Compr Physiol 2018, 9: 127-148. doi: 10.1002/cphy.c180006