A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys

Abstract

Background: We have developed a novel head-holding device for behaving non-human primates that affords stability suitable for reliable chronic electrophysiological recording experiments. The device is completely non-invasive, and thus avoids the risk of infection and other complications that can occur with the use of conventional, surgically implanted head-fixation devices.

New method: The device consists of a novel non-invasive head mold and bar clamp holder, and is customized to the shape of each monkey's head. The head-holding device that we introduce, combined with our recording system and reflection-based eye-tracking system, allows for chronic behavioral experiments and single-electrode or multi-electrode recording, as well as manipulation of brain activity.

Results and comparison with existing methods: With electrodes implanted chronically in multiple brain regions, we could record neural activity from cortical and subcortical structures with stability equal to that recorded with conventional head-post fixation. Consistent with the non-invasive nature of the device, we could record neural signals for more than two years with a single implant. Importantly, the monkeys were able to hold stable eye fixation positions while held by this device, demonstrating the possibility of analyzing eye movement data with only the gentle restraint imposed by the non-invasive head-holding device.

Conclusions: We show that the head-holding device introduced here can be extended to the head holding of smaller animals, and note that it could readily be adapted for magnetic resonance brain imaging over extended periods of time.

Keywords: Chronic recording; Electrophysiology; Eye-tracking; Head holding; Primate.

Fig. 1

Design of the head-holding device. (A) Individual components of the device: adjustable 21-cm-long bar clamp (1), extender (2), attachment bracket (3) and extender holder (4). (B) Head mold made with flexible plastic. (C–F) Front (C), rear (D), left side (E) and right side (F) views of the head-holding device attached to a primate chair. (G) Head-holding device designed for squirrel monkey.

Fig. 2

Negligible effect of head movements on stability of eye tracking. (A) Example of horizontal (red) and vertical (blue) eye-position traces during the active task. (B) Angular velocity of head movement monitored during the same trial as Fig. 2A. Magenta, cyan, and green lines indicate, respectively, roll, pitch, and yaw movements. Head movements were minimal except during reward-licking period.

Fig. 3

Eye position and head movement traces in the active and passive tasks. (A and B) Horizontal (top row) and vertical (second row) eye position, relative to the fixation cue position, and roll (third row), pitch (fourth row) and yaw (bottom row) angular velocity of head movements recorded during rightward saccades (A) and leftward saccades (B) made during performance of the active task. Zero on x-axis indicates saccade onset time. (C and D) Traces showing eye position and head movements during fixations for the 300 ms starting at 350 ms after fixation cue onset (C), and during fixations for 200 ms before the reward delivery (D) by a monkey performing the passive task. Traces from multiple trials are overlaid.

Fig. 4

Cue-related spike activity recorded during use of the head-holding device. (A and B) Raster plots (above) and spike histograms (below) of spike activity recorded during cue (left) and reward (right) periods in the dorsolateral prefrontal cortex (A) and caudate nucleus (B) in a monkey performing the approach-approach task. Activity was recorded with the multi-electrode recording method. (C) Spike activity recorded from the substantia nigra pars compacta with conventional single-electrode recording methods during performance of the passive task. Spike histograms are aligned to cue onset (left) and reward delivery (right). (D) Eye position trace from the same recording session as shown in Fig. 4C. Horizontal (left) and vertical (right) eye positions, relative to the fixation cue position, are shown for the ±800 ms period around the onset of the target cue. Shading indicates the range within which the monkey was required to maintain eye position (8° square window).