A lightweight microdrive for single-unit recording in freely moving rats and pigeons

doi:10.1016/S1046-2023(03)00076-8

Methods

Volume 30, Issue 2, June 2003, Pages 152-158

https://doi.org/10.1016/S1046-2023(03)00076-8 Get rights and content

Abstract

A design for an inexpensive and reliable subminiature microdrive for recording single neurons in the freely moving animal is presented. The Scribe microdrive is small and lightweight and has been used successfully to record in freely moving rats and pigeons. It would also be suitable for recording in mice. The device is simple and inexpensive yet allows for stable and precise manipulation of the recording electrodes. As a result it supports stable recordings conducted over long periods. Because the Scribe microdrive is a small-diameter device it is also suitable for multisite, multielectrode applications. Here we discuss the construction of the device and comment on its use in recording from freely moving rats and pigeons.

Introduction

Despite major advances in the development of imaging techniques, the single-unit recording procedure is still the only technique via which brain activity, at the level of its basic processing elements, can be related to behavior with a spatial and temporal resolution that matches that of these underlying elements. In the decades since unit recordings were first performed in behaving animals, a number of devices have been developed to move small-diameter, high-impedance recording electrodes gradually through the brain tissue of interest. These devices (microdrives) have been designed to meet one or more of the following requirements:

1.
Small size and low weight: The use of small drives allows for recording from small animals such as rats, birds, and mice. The use of mice opens up interesting possibilities for exploring the effects of genetic manipulations, such as gene knockouts, on neural activity [1]. Furthermore, if a drive is small, it is possible to implant several electrodes simultaneously into different brain regions. By decreasing the size and weight of the drive we also reduce the possibility that it will be knocked and displaced during the recording process or while the animal is in its home cage.
2.
Precise advancement: For single-unit recording, the drive should be able to be advanced in increments of approximately 10 to 20 μm over a range of at least 1 to 2 mm. Additionally, a drive might also be designed to allow for electrode withdrawal to optimize placement or to allow for multiple penetrations.
3.
Stability over time: Ideally, most unit recordings should be stable over at least 24 h. Even if the researcher is not interested in analyzing activity over long periods, if the drive is stable then the probability that a unit will be lost or that the morphology of the recorded waveform will change as a result of electrode movement during a shorter recording period is decreased. Stability over longer periods also allows a researcher to confidently investigate the biology of processes such as long-term memory or to use “within-cell” experimental manipulations.
4.
Simple installation: More rapid implantation leads to shorter surgeries and reduces trauma to the recipient animal.
5.
Low cost: Unfortunately, many of these requirements tend to preclude low cost, as, for example, small size and precision usually require that the component parts be machined to a fine tolerance.

It is possible to design a stable, simple, and inexpensive microdrive by building a device with two or three support legs, with the electrode attached to a chassis supported by these legs. If the legs are threaded, then it is possible to manipulate the electrode within the brain by turning these drive screws. This type of drive tends, however, to be rather large because of the multiple drive screws. Furthermore, machining of the drive screws is often still required and in some cases recording quality may be compromised because of yaw that is generated in the device as the individual drive screws are turned. In contrast, a microdrive built around a single drive screw is potentially half (or less) of the width of a multiple-screw design. Unfortunately, previous single-screw designs were usually more difficult to build (and hence more expensive, although see [2]) because of the requirement that the rotating motion of the drive screw not be transferred to the electrode. A failure to constrain this rotary motion causes the electrode to twist as it enters the brain, reducing the recording quality. One way that previous single-screw microdrive designs eliminated screw-induced rotation was by having the electrode holder keyed to a stable section of the drive so that the holder is free to move along its major axis only. This approach results, however, in an increase in the complexity of the device. Several previously described drives of this type, for instance, are composed of a relatively large number of separate components, many of which require fairly sophisticated machining (e.g. [3], [4], [5], [6], [7]).

We describe here an alternative approach to the construction of a single-screw microdrive that: (1) uses a novel method to isolate the rotation of the driving screw from the electrode assembly, (2) can be built from components that are readily available and have virtually no cost and yet are already machined to fine tolerances, and (3) is small (22 mm tall from skull to drive screw with screw at highest position), lightweight (0.39 g), and stable. This article enlarges on a previous description of this microdrive [8] and provides more detail relating to its construction and use, in particular, in animals other than rats.

Section snippets

Microdrive and electrode construction methods

The basic principle of the design is to prevent transfer of the rotational torque from the single driving screw to the driven electrode assembly by ensuring that the point of contact between the rotating and nonrotating components is (1) at the axis of rotation and (2) low-friction. This is achieved simply by abutting the drive screw directly against the ball end of the tip of the ubiquitous ballpoint pen. Fig. 1 provides a cut-away photograph of the assembled drive and Fig. 2 illustrates the

Recording performance in behaving rats

We have used the Scribe microdrive to record well-isolated units in both the hippocampus and perirhinal cortex regions of the brain in freely moving animals [9], [10]. Good-quality recordings have been made in drives that have been implanted for up to 7 months and signal:noise ratios of at least 3:1 are readily obtained. Stable recordings of individual units have been made for periods of over 1 month (note that this time does not necessarily reflect the maximum time that a particular unit could

Single-unit recording in the brain of behaving pigeons

Over the past few years one of the authors (M.C.) has initiated a series of studies exploring the neural mechanisms of visual information processing in the avian brain. Pigeons are ideal subjects to use in these sorts of experiments for two reasons. First, pigeons are exceptional at processing visual information and can be trained on many of the same tasks that are used to examine visual information processing in both monkeys and humans [13], [14]. Second, the brain of pigeons, like that of

Recording performance in behaving pigeons

An example of a neuron recorded from the ectostriatum of an awake, behaving pigeon is shown in Fig. 4. In the case of this neuron, the subject was trained on a visual delayed matching-to-sample task, a standard procedure used to tap memory across a variety of different species including humans. The procedure is quite simple. At the end of an intertrial interval (ITI), a sample period (S) is initiated during which time either a red or green sample stimulus is presented on the center projector.

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A hole was drilled into the skull above the Wulst, and the dura was removed. A lightweight microdrive (Bilkey, Russell, & Colombo, 2003) housing the electrodes was lowered into the hole until the tips of the electrodes were positioned directly above the Wulst. The microdrive was secured to the skull using dental acrylic, and the wound was sutured.
The avian Wulst is the pallial (analogous to mammalian cortex) termination point of the thalamofugal pathway, one of two main visual pathways in birds, and is considered to be equivalent to primate striate cortex. We recorded neuronal activity from the Wulst in pigeons during two versions of a delayed matching-to-sample procedure. Two birds were trained on a common outcomes (CO) procedure, in which correct responses following both the skateboarder and the flower stimuli were associated with reward. Two other birds were trained on a differential outcomes (DO) procedure in which correct responses following only the skateboarder stimulus were associated with reward, while correct responses following the flower stimulus were not rewarded. In line with previous studies, under CO conditions, and for both excitatory and inhibitory neurons, delay activity in the Wulst was significantly different from baseline activity following both sample stimuli, which may indicate that Wulst delay activity is a neural correlate of working memory for the sample stimulus. On the other hand, under DO conditions, Wulst delay activity appeared to be a neural correlate of the upcoming reward. We argue that Wulst neurons display flexibility in their encoding in that they can encode both sample and reward information, but may default to one type of coding over the other based on the demands of the task. The current study provides the first evidence that delay activity in the Wulst represents both a neural correlate for sample information as well as reward information.
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Serial-order behaviour is the ability to complete a sequence of responses in order to obtain a reward. Serial-order tasks can be thought of as either externally-ordered (EO) such that the order of responses is predetermined, or internally-ordered (IO) such that the subject determines the order of responses from trial to trial. Ordinal knowledge (representation of first, second, or third etc.) is a key component of successful serial-order behaviour, and is considered a higher-order cognitive function. The nidopallium caudolaterale (NCL) is the avian equivalent to the prefrontal cortex, an area of the primate brain important for serial-order behaviour. The importance of the NCL for serial-order behaviour, however, is still unknown. In the current study, we trained pigeons to complete either three-item EO or IO tasks and recorded single-neuron activity from the NCL to determine whether neurons in the NCL code ordinal knowledge. Our results support the view that the NCL is involved in serial-order behaviour by coding ordinal position, at least with respect to the IO task. The absence of any ordinal coding during the EO task could be explained by the different strategies that birds adopt between the EO and IO tasks.
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All experimental hardware was controlled with custom-written Matlab code (MathWorks, Natick, MA, USA) with the aid of the Biopsychology toolbox [34]. After behavioral training, pigeons were implanted with custom-built microdrives [35–38]. Each microdrive housed seven electrodes made of 25 μm formvar-coated nichrome wires (Science Products GmbH, Hofheim, Germany) and one additional 76 μm heavy-polyimide-coated stainless steel wire serving as reference (Franco Corradi, Milano, Italy), which were connected to microconnectors (Omnetics Connector Corporation, Minneapolis, USA).
Recognizing and categorizing visual stimuli are cognitive functions vital for survival, and an important feature of visual systems in primates as well as in birds. Visual stimuli are processed along the ventral visual pathway. At every stage in the hierarchy, neurons respond selectively to more complex features, transforming the population representation of the stimuli. It is therefore easier to read-out category information in higher visual areas. While explicit category representations have been observed in the primate brain, less is known on equivalent processes in the avian brain. Even though their brain anatomies are radically different, it has been hypothesized that visual object representations are comparable across mammals and birds. In the present study, we investigated category representations in the pigeon visual forebrain using recordings from single cells responding to photographs of real-world objects. Using a linear classifier, we found that the population activity in the visual associative area mesopallium ventrolaterale (MVL) distinguishes between animate and inanimate objects, although this distinction is not required by the task. By contrast, a population of cells in the entopallium, a region that is lower in the hierarchy of visual areas and that is related to the primate extrastriate cortex, lacked this information. A model that pools responses of simple cells, which function as edge detectors, can account for the animate vs. inanimate categorization in the MVL, but performance in the model is based on different features than in MVL. Therefore, processing in MVL cells is very likely more abstract than simple computations on the output of edge detectors.
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This chapter outlines technical approaches to recording neurophysiological data in birds. A wide variety of electrophysiological techniques are used in the avian brain. These range from acute recordings in head-restrained animals to chronic recordings in unrestrained birds and even include recording during flight. The most common technical approach uses small movable microdrives, in some cases motorized, to advance single electrodes or bundles of electrodes. Recently, high-channel-count silicon probes have also been used in conjunction with microdrives. In all these scenarios, neurophysiological recordings in birds pose unique challenges and problems, one of which is the low weight tolerance, especially of smaller birds. This chapter discusses these unique challenges and provides solutions wherever possible.
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A hole was drilled above the targeted area, and the dura was removed. A microdrive [2] housing the electrodes was lowered into the hole until the tips of the electrodes were positioned just directly above either the ENTO or NCL. The microdrive was secured to the skull using dental acrylic and the wound was closed.
We recorded neuronal activity from the nidopallium caudolaterale, the avian equivalent of mammalian prefrontal cortex, and the entopallium, the avian equivalent of the mammalian visual cortex, in four birds trained on a differential outcomes delayed matching-to-sample procedure in which one sample stimulus was followed by reward and the other was not. Despite similar incidence of reward-specific and reward-unspecific delay cell types across the two areas, overall entopallium delay activity occurred following both rewarded and non-rewarded stimuli, whereas nidopallium caudolaterale delay activity tended to occur following the rewarded stimulus but not the non-rewarded stimulus. These findings are consistent with the view that delay activity in entopallium represents a code of the sample stimulus whereas delay activity in nidopallium caudolaterale represents a code of the possibility of an upcoming reward. However, based on the types of delay cells encountered, cells in NCL also code the sample stimulus and cells in ENTO are influenced by reward. We conclude that both areas support the retention of information, but that the activity in each area is differentially modulated by factors such as reward and attentional mechanisms.

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A lightweight microdrive for single-unit recording in freely moving rats and pigeons

Abstract

Introduction

Section snippets

Microdrive and electrode construction methods

Recording performance in behaving rats

Single-unit recording in the brain of behaving pigeons

Recording performance in behaving pigeons

Trends Neurosci.

Brain Res. Bull.

Electroencephalogr. Clin. Neurophysiol.

J. Neurosci. Methods

Brain Res. Bull.

J. Neurosci. Methods

J. Neurosci. Methods

J. Neurosci. Methods

Neuron

Neurosci. Biobehav. Rev.

Brain Res.

Brain Res.

Vision Res.