Trends in Neurosciences
Volume 29, Issue 9, September 2006, Pages 536-546
Journal home page for Trends in Neurosciences

Review
Brain–machine interfaces: past, present and future

https://doi.org/10.1016/j.tins.2006.07.004Get rights and content

Since the original demonstration that electrical activity generated by ensembles of cortical neurons can be employed directly to control a robotic manipulator, research on brain–machine interfaces (BMIs) has experienced an impressive growth. Today BMIs designed for both experimental and clinical studies can translate raw neuronal signals into motor commands that reproduce arm reaching and hand grasping movements in artificial actuators. Clearly, these developments hold promise for the restoration of limb mobility in paralyzed subjects. However, as we review here, before this goal can be reached several bottlenecks have to be passed. These include designing a fully implantable biocompatible recording device, further developing real-time computational algorithms, introducing a method for providing the brain with sensory feedback from the actuators, and designing and building artificial prostheses that can be controlled directly by brain-derived signals. By reaching these milestones, future BMIs will be able to drive and control revolutionary prostheses that feel and act like the human arm.

Introduction

Less than a decade ago, hardly anyone could have predicted that attempts to build direct functional interfaces between brains and artificial devices, such as computers and robotic limbs, would have succeeded so readily, and in the process would have led to the establishment of a new area at the frontier of systems neuroscience. Born as a highly multidisciplinary field, basic research on brain–machine interfaces (BMIs) has moved at a stunning pace since the first experimental demonstration in1999 that ensembles of cortical neurons could directly control a robotic manipulator [1]. Since then, a continuous stream of research papers has kindled an enormous interest in BMIs among the scientific community and the lay public. This interest stems from the considerable potential of this technology for restoration of motor behaviors in severely handicapped patients.

Indeed, BMIs have been primarily conceived as a potential new therapy to restore motor control in severely disabled patients, particularly those suffering from devastating conditions such as amyotrophic lateral sclerosis (ALS), spinal cord injury, stroke and cerebral palsy. As this technology advances and the risks of invasive brain recordings decrease, BMIs might also hold promise for amputees. In addition to the systems controlling upper-limb prostheses, BMIs dedicated to the restoration of locomotion and speech are likely to emerge.

However, such stellar progress also breeds unrealistic expectations that such a future is just around the corner. Thus, the understandable eagerness in attaining the lofty goal of helping severely disabled patients has to be carefully calibrated by an objective analysis of the current state and future directions of the field. Such analysis indicates that, despite the optimism raised by a barrage of new accomplishments, there are still many issues that preclude straightforward translation of experimental BMIs into clinical applications. Indeed, most of the invasive BMIs have been tested only in experimental animals. Thus, despite recent enthusiasm to move emergent, and in some cases not thoroughly tested, BMI-related technology into clinical trials, much experimentation remains to be done before BMIs can become a safe and efficient rehabilitation tool.

Here, we highlight some of the fundamental obstacles faced by BMI research and propose a series of milestones that can transform recent experimental advances into viable clinical applications in the next 10–20 years. The roadmap detailed here takes into account the recent history of the field, the factors that influenced its growth, and a critical analysis of the published work.

Section snippets

Non-invasive BMIs

Figure 1 depicts a classification of the BMIs (or brain–computer interfaces, BCIs) developed during the past decade. The first feature that distinguishes BMIs is whether they utilize invasive (i.e. intra-cranial) or non-invasive methods of electrophysiological recordings. Non-invasive systems primarily exploit electroencephalograms (EEGs) to control computer cursors or other devices. This approach has proved useful for helping paralyzed or ‘locked in’ patients develop ways of communication with

Invasive BMIs

Invasive BMI approaches are based on recordings from ensembles of single brain cells (also known as single units) or on the activity of multiple neurons (also known as multi-units). These approaches have their roots in the pioneering studies conducted by Fetz and colleagues in the 1960s and 1970s 40, 41, 42, 43, 44, 45. In these experiments, monkeys learned to control the activity of their cortical neurons voluntarily, aided by biofeedback indicating the firing rate of single neurons. A few

Principles of BMI operation

Invasive BMIs rely on the physiological properties of individual cortical and subcortical neurons (or pools of neurons) that modulate their activity in association with movements. First documented four decades ago by Evarts 66, 67, 68, such modulations are highly variable, from neuron to neuron and from trial to trial 69, 70, 71, 72. Thus, as much as neighboring neurons might display highly distinct firing modulation patterns during the execution of a particular movement, single-neuron firing

A proposed roadmap for the future of BMI research

To achieve the ambitious goal of creating a clinically useful invasive BMI for restoring upper-limb mobility, one has to pass the following key bottlenecks:

  • Obtaining stable, very long-term recordings (i.e. over years) of large populations of neurons (i.e. hundreds to thousands) from multiple brain areas. This task encourages development of a new generation of biocompatible 3D electrode matrices that yield thousands of channels of recordings while producing little tissue damage at implantation

Developing algorithms for translating neuronal activity into command signals for artificial actuators

Currently, neuroscientists are far from obtaining a clear understanding of how motor and cognitive information is processed by the populations of neurons that form large brain circuits. Rate encoding, temporal encoding and population encoding principles have been suggested, and various experimental paradigms, including BMIs, have been developed to test the validity of these concepts. However, precise knowledge of computations performed by brain circuits is not crucial for the construction of

Making use of brain plasticity to incorporate prosthetic devices into the body representation

Controlling an artificial actuator through a BMI can be thought of as a process somewhat similar to the operation required by subjects to operate tools – a capacity that is inherent only in higher primates such as chimpanzees and humans [139]. Almost 100 years ago [140], Head and Holmes suggested that the ‘body schema’– that is, the internal brain representations of one's body – could extend itself to include a wielded tool. This idea was validated by the experimental demonstration that

Making the prosthetic feel like the subject's own limb using microstimulation of cortical sensory areas

Peripheral tactile and proprioceptive signals contribute to the normal operation of one's limbs and the perception that they are part of the body 142, 143. For a neuroprosthesis to behave and feel as a natural appendage of the subject's body, it will have to be instrumented with various sensors that can provide multiple channels of ‘sensory’ information back to the subject's brain. In most current BMI designs, animal subjects receive sensory information from the actuator through visual feedback

Concluding remarks

Our vision of neuroprosthetic developments that might emerge in the next 10–20 years includes a fully implantable recording system that wirelessly transmits multiple streams of electrical signals, derived from thousands of neurons, to a BMI capable of decoding spatial and temporal characteristics of movements and intermittent periods of immobility, in addition to cognitive characteristics of the intended actions (Figure 3). This BMI would utilize a combination of high-order motor commands,

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