Abstract
In 1999 we reported an important demonstration of a working brain-machine interface (BMI), in which recordings from multiple, single neurons in sensorimotor cortical areas of rats were used to directly control a robotic arm to retrieve a water reward. Subsequent studies in monkeys, using a similar approach, demonstrated that primates can use a BMI device to control a cursor on a computer screen and a robotic arm. Recent studies in humans with spinal cord injuries have shown that recordings from multiple, single neurons can be used by the patient to control the cursor on a computer screen. The promise is that one day it will be possible to use these control signals from neurons to re-activate the patient’s own limbs. However, the ability to record from large populations of single neurons for long periods of time has been hampered because either the electrode itself fails or the immunological response in the tissue surrounding the microelectrode produces a glial scar, preventing single-neuron recording. While we have largely solved the problem of mechanical or electrical failure of the electrode itself, much less is known about the long term immunological response to implantation of a microelectrode, its effect on neuronal recordings and, of greatest importance, how it can be reduced to allow long term single neuron recording. This article reviews materials approaches to resolving the glial scar to improve the longevity of recordings. The work to date suggests that approaches utilizing bioactive interventions that attempt to alter the glial response and attract neurons to the recording site are likely to be the most successful. Importantly, measures of the glial scar alone are not sufficient to assess the effect of interventions. It is imperative that recordings of single neurons accompany any study of glial activation because, at this time, we do not know the precise relationship between glial activation and loss of neuronal recordings. Moreover, new approaches to immobilize bioactive molecules on microelectrode surfaces while maintaining their functionality may open new avenues for very long term single neuron recording. Finally, it is important to have quantitative measures of glial upregulation and neuronal activity in order to assess the relationship between the two. These types of studies will help rationalize the study of interventions to improve the longevity of recordings from microelectrodes.
Highlights
In the past few decades, recording microelectrodes have been utilized to simultaneously acquire information from multiple, single neurons that encode for the intention to move in awake, freely moving animals
If the device used to create the stab wound is left in place, a glial scar can form around the device, effectively walling it off from the healthy neural tissue [26].the initial damage done by microelectrode insertion, coupled with the continuous existence of the microelectrode, creates an environment that does not allow healthy neurons to remain close enough to the electrode to be recorded
Given that some upregulation of glia are important to remove cells damaged from electrode insertion, it is likely that any intervention would have to be an active process, allowing for some upregulation followed by a signal to down-regulate the response and maintain healthy neuron-electrode interactions
Summary
In the past few decades, recording microelectrodes have been utilized to simultaneously acquire information from multiple, single neurons that encode for the intention to move in awake, freely moving animals. Two major reasons have been noted for the failure of such implants: (i) the mechanical failure of the implant itself, typically due to failure of the cable from the electrode to the signal conditioning device or loss of polymeric insulation of the microelectrode due to the corrosive extracellular environment and (ii) the formation of a glial scar surrounding the microelectrode rendering the implant useless because of its inability to record action potentials from single neurons [5] While the former has been largely resolved in recent years, the latter continues to be a major impediment for the long-term in-vivo functionality of neural implants [6,7]. When the value of the NPC exceeds the threshold, a seizure is predicted
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