A bundled microwire array for long-term chronic single-unit recording in deep brain regions of behaving rats

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Abstract

Chronic single-unit recording in subcortical brain regions is increasingly important in neurophysiological studies. However, methods for long-term, stable recording of multiple single-units in deep brain regions and in dura-surrounded ganglion have not yet been established. In the present study, we propose a bundled microwire array design which is capable of long-term recording of the trigeminal ganglion and deep-brain units. This electrode set is easy to construct from common materials and tools found in an electrophysiological laboratory. The salient features of our design include: (1) short and separated tungsten microwires for stable chronic recording; (2) the use of a 30-guage stainless steel guide tube for facilitating penetration and aiming for deep targets as well as electrical grounding; (3) the inclusion of a reference of the same microwire material inside the bundle to enhance common mode rejection of far field noises; and (4) an adjustable connector. In our case, we used a 90° backward bending connector so that implanted rats could perform the same hole-seeking behavior and their faces and the whiskers could be stimulated in the behaving state. It was demonstrated that this multi-channel electrode caused minimal tissue damage at the recording site and we were able to obtain good, stable single-unit recordings from the trigeminal ganglion and ventroposterior medial thalamus areas of freely moving rats for up to 80 days. This methodology is useful for the studies that require long term and high quality unit recording in the deep brain or in the trigeminal system.

Highlights

► A bundled microwire array for chronic recording in the deep brain of behaving rats. ► The recording stability was assessed using spike shape and receptive field. ► Stable trigeminal ganglion and thalamic single-units were recorded up to 80 days.

Introduction

Monitoring the change of activity of the same neuron for an extended period of time is needed for probing many physiological and pathological questions. For example, Herry et al. (2008) recorded the same amygdala neurons for 11 days in series of behavior tasks to test the role of single amygdaloid neuron in context-specific conditioning and extinction. In the field of long-term memory and chronic diseases, an even longer monitoring time is required.

Many types of electrodes, such as movable electrodes (Eliades and Wang, 2008, Haiss et al., 2010, Jackson and Fetz, 2007, Wilson et al., 2003, Yamamoto and Wilson, 2008, Yang et al., 2010), tetrodes (Tolias et al., 2007), microarrays (Nicolelis et al., 2003), microelectrode bundles (Herry et al., 2008, Kubie, 1984, Nicolelis et al., 1997, Szymusiak et al., 1998), and silicone based probes (Suner et al., 2005, Vetter et al., 2004), have been successfully used to obtain good unit recordings chronically in rodents and primates. In the primate cortex, good quality neuronal recording could be extended to 1.5 years using microarray electrodes (Nicolelis et al., 2003) and silicone based probes (Suner et al., 2005). However, high density array electrodes have limitedly used in deeper brain regions due to their tendency of causing severe brain damages. In addition, it is very difficult for the conventional linear microwire arrays to reach deep brain targets accurately and thus is of little practical use.

Bundled microwires, either singularly or in stereode/tetrode configurations, are better choices for making recordings in the nuclei of the deeper brain, and these were successfully used to record the nuclei in many regions, such as the amygdala (Chang et al., 2005, Herry et al., 2008), hypothalamus (Szymusiak et al., 1998), hippocampus (Kubie, 1984, Thompson and Best, 1990), and lateral thalamus (Nicolelis et al., 1997). It has been demonstrated in rabbits and primates that the temporal recording stability of bundle electrodes in visual cortex (Porada et al., 2000) and hippocampus (Thompson and Best, 1990) was over a year. However, one difficulty is the recording of trigeminal ganglion (TG) units. TG is located deep under the brain (∼9 mm from the brain surface in a rat) while being surrounded by thick dura. Therefore, long thin microwires (∼1 cm long), even when bundled together, cannot have sufficient rigidity to penetrate the layers of dura to reach it. Several studies successfully recorded the single-unit activity of TG using single-channel metal electrode with a wider shank (125 or 250 μm, to maintain the rigidity) and a sharp tip (to penetrate more easily) (Bermejo et al., 2004, Khatri et al., 2009, Leiser and Moxon, 2007). The drawback of the above-mentioned method is using the wider shank as well as the limited channel number; accordingly only one or two electrodes can be implanted.

Ideally, it is preferable to have more channels while minimizing tissue damage within a certain brain region. We noted that a tungsten microwire maintains strong rigidity when it is shorter than 1.5 mm. In addition, at this length, if the adjacent microwires are separated by a minimal inter-electrode distance of 200 μm, they can resist the adhesion force of water to remain separated in the implantation process. Based on the above characteristics, we developed a multi-channel electrode set for multiple single-unit recording chronically in the deep brain region.

Section snippets

Electrode construction

A glass slide with a piece of two-sided adhesive tape stuck on it was used as the fabrication jig. A 12-mm stainless steel needle with a sharp tip was cut to serve as a guide tube (30- and 29-guage for TG and thalamic recording respectively). Three or four circular notches were made with an electronic cutter at the blunt end, and a 15-mm copper wire (with a diameter of about 150 μm) was tightly wound two or three times on the notches and soldered onto the needle to serve as the ground wire. The

Results

Both TG and thalamic single-unit recordings were successfully obtained from 6 rats. The recorded noises were effectively attenuated by the needle-grounding with local reference method as shown in Fig. 2. These included smaller peak-to-peak background noise, and fewer and smaller far-field noise from animal movements.

Behavioral evaluation of the rats showed that escape thresholds of the ipsilateral and contralateral sides of the whisker pad significantly dropped to 22 ± 8.7 and 20.2 ± 8.8 g

Discussion

Chronically tracking neuronal signals in the same electrode over a period of 1.5 years has been reported using silicone-base microelectrode in primate motor cortex (Suner et al., 2005). In rodents, high quality cortical single-units could be recorded for over 127 days (Vetter et al., 2004). It is unclear, however, whether the same single-units were followed. Recently, the prevailing technique for chronic recording in the awake primates and rodents is the movable electrode (microarray or

Acknowledgement

This study was supported by a grant (NSC98-2313-B-197-003-MY3) from the National Science Council, Taiwan.

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