Wireless multi-channel single unit recording in freely moving and vocalizing primates

Abstract

The ability to record well-isolated action potentials from individual neurons in naturally behaving animals is crucial for understanding neural mechanisms underlying natural behaviors. Traditional neurophysiology techniques, however, require the animal to be restrained which often restricts natural behavior. An example is the common marmoset (Callithrix jacchus), a highly vocal New World primate species, used in our laboratory to study the neural correlates of vocal production and sensory feedback. When restrained by traditional neurophysiological techniques marmoset vocal behavior is severely inhibited. Tethered recording systems, while proven effective in rodents pose limitations in arboreal animals such as the marmoset that typically roam in a three-dimensional environment. To overcome these obstacles, we have developed a wireless neural recording technique that is capable of collecting single-unit data from chronically implanted multi-electrodes in freely moving marmosets. A lightweight, low power and low noise wireless transmitter (headstage) is attached to a multi-electrode array placed in the premotor cortex of the marmoset. The wireless headstage is capable of transmitting 15 channels of neural data with signal-to-noise ratio (SNR) comparable to a tethered system. To minimize radio-frequency (RF) and electro-magnetic interference (EMI), the experiments were conducted within a custom designed RF/EMI and acoustically shielded chamber. The individual electrodes of the multi-electrode array were periodically advanced to densely sample the cortical layers. We recorded single-unit data over a period of several months from the frontal cortex of two marmosets. These recordings demonstrate the feasibility of using our wireless recording method to study single neuron activity in freely roaming primates.

Distinct Neural Activities in Premotor Cortex during Natural Vocal Behaviors in a New World Primate, the Common Marmoset (Callithrix jacchus)

“…The animals used in this study were born and raised in a breeding colony that we have maintained at Johns University School of Medicine since 1996. This study overcame three technical challenges in this line of research: (1) the ability to induce and observe repeatable natural vocal behaviors without subjecting marmosets to behavioral training in tasks involving in nonvocal motor behaviors (e.g., limb movement) and food rewards, which was achieved by developing the antiphonal calling vocal behavior in the laboratory condition (Miller and Wang, 2006;Miller et al, 2009Miller et al, , 2010b; (2) the ability to record chronically single neuron activity over a long period of time and in populations of neurons in the premotor cortex (Eliades andWang, 2008a, 2008b); and (3) the ability to conduct neural recordings in freely roaming and naturally vocalizing marmosets via wireless neural recording techniques (Roy and Wang, 2012). With these technical advancements, it became possible to investigate neural mechanisms underlying natural vocal behaviors in freely moving and vocalizing marmosets.…”

“…This licking behavior was used as a control condition because it generated mouth movement but without vocal production. Licking involves similar musculature (e.g., The custom-built chamber was designed to isolate electromagnetic wave transmission and reflection, attenuate external sounds, and reduce internal sound reflection (Roy and Wang, 2012). In the vocal production condition, an experimental subject was placed in a plastic cage shown on the left side of the chamber.…”

“…Two adult marmosets (35U and 6207A, both female) were implanted with 16-channel multielectrode arrays (Eliades and Wang, 2008a; Warp-16; Neuralynx), including both hemispheres of marmoset 35U and the right hemisphere of marmoset 6207A. Details about the array implantation and the recording techniques have been described previously (Eliades and Wang, 2008a;Roy and Wang, 2012). Briefly, marmosets were implanted with a head cap using standard surgical procedures (Lu et al, 2001).…”

“…Neural signals were transmitted by a wireless head stage (W16; Triangle Biosystems) connected to the electrode array, mounted on top of the marmoset's head, and protected by a polycarbonate cap (Roy and Wang, 2012). The array (ϳ1 g), wireless head stage (ϳ4 g), and protection cap (ϳ7 g) were relatively lightweight and did not interfere with marmosets' vocalizations or movements.…”

“…In the present study, we used chronically implanted multielectrode arrays (Eliades and Wang, 2008a) and a wireless neural recording system (Roy and Wang, 2012) developed in our laboratory to study single neuron activity in the frontal cortex of marmosets while they roamed freely in recording cages and engaged in the antiphonal calling behavior (see Materials and Methods). A substantial number of neurons in premotor cortex were found to have either increased or decreased activities before or during vocal production.…”