Long-term stability of neural signals from microwire arrays implanted in common marmoset motor cortex and striatum

Abstract

Current neuroprosthetics rely on stable, high quality recordings from chronically implanted microelectrode arrays (MEAs) in neural tissue. While chronic electrophysiological recordings and electrode failure modes have been reported from rodent and larger non-human primate (NHP) models, chronic recordings from the marmoset model have not been previously described. The common marmoset is a New World primate that is easier to breed and handle compared to larger NHPs and has a similarly organized brain, making it a potentially useful smaller NHP model for neuroscience studies. This study reports recording stability and signal quality of MEAs chronically implanted in behaving marmosets. Six adult male marmosets, trained for reaching tasks, were implanted with either a 16-channel tungsten microwire array (five animals) or a Pt-Ir floating MEA (one animal) in the hand-arm region of the primary motor cortex (M1) and another MEA in the striatum targeting the nucleus accumbens (NAcc). Signal stability and quality was quantified as a function of array yield (active electrodes that recorded action potentials), neuronal yield (isolated single units during a recording session), and signal-to-noise ratio (SNR). Out of 11 implanted MEAs, nine provided functional recordings for at least three months, with two arrays functional for 10 months. In general, implants had high yield, which remained stable for up to several months. However, mechanical failure attributed to MEA connector was the most common failure mode. In the longest implants, signal degradation occurred, which was characterized by gradual decline in array yield, reduced number of isolated single units, and changes in waveform shape of action potentials. This work demonstrates the feasibility of longterm recordings from MEAs implanted in cortical and deep brain structures in the marmoset model. The ability to chronically record cortical signals for neural prosthetics applications in the common marmoset extends the potential of this model in neural interface research.

A Critical Review of Microelectrode Arrays and Strategies for Improving Neural Interfaces

“…It was found that over a course of 12 weeks, there was an increase in recording failure among the MEAs. Similar phenomena were observed in a study by Debnath et al, where MEAs were implanted into marmoset brains and monitored for signal stability and quality over the course of several months. Over time, many of the MEAs lost signal stability, with only 2 of 11 MEAs showing long‐term stability.…”

“…As a result, without good cell adhesion, MEAs are free to move around in the brain, causing additional strain on the surrounding tissue 41b. Not only does this cause damage to the brain, but it also compromises MEA function over time . Adding to this problem is the ensuing FBR following MEA insertion.…”

A hardware/software system for electrophysiology “supersessions” in marmosets

“…Although a complete comparison between these types of array is beyond the scope of this proof-of-concept tool introduction, we believe it is likely that the variations in performance observed with ‘Utah’ arrays in macaques were larger than for the 3D arrays we used. In fact, in marmosets, arrays with similar sizes as the ones used in this study (but with fewer electrode contacts) have been reliably implanted and often measured spiking activity for months ( Debnath et al, 2018 ).…”

Toward Standardization of Electrophysiology and Computational Tissue Strain in Rodent Intracortical Microelectrode Models

“…Utilization of primates in IME studies have shown the potential clinical applications of the electrodes, but unfortunately suffer from the same decline in recording performance (Chestek et al, 2011;Barrese et al, 2013Barrese et al, , 2016. Recent work introducing a marmoset model also displayed similar signal degradation found in traditional animal models (Debnath et al, 2018). Rodent models yield similar electrode reliability results compared to the larger animal alternatives.…”