Miniature multichannel preamplifier for extracellular recordings of single unit activity in freely moving and swimming small animals

Abstract

The design of a miniature multichannel preamplifier for extracellular recordings of single unit activity in freely moving and swimming small animals is presented. The advantages of this design include perfect protection of the critical components and electric contacts from water. Thus, neuronal activity and EEG may be recorded differentially in any kinds of behavioral tasks including swimming in Morris water maze. Recordings are stable even if an animal is diving and swimming under the water surface. The reusable dismountable base can adopt different types of chronically implanted fine wire electrodes and movable arrays. Electrodes may be implanted to any desired depth. The assembly weight is less than 240 mg. Thus, the construction is light enough even for mice. This work is the first successful attempt for multichannel recording of neuronal activity in mice performing spatial task in Morris water maze.

Introduction

Genetically modified animals are promising models of different kinds of behavioral pathology. Morris water maze task (Morris, 1981, Morris, 1984) has been recognized as an effective test for measuring genetic variations of spatial memory in mice (Nakazawa et al., 2002, Nakazawa et al., 2004). Much of our understanding of the brain function has come from neuronal recordings, but recording neuronal activity in swimming animals causes a lot of technical challenges. The first successful attempt to record neuronal activity in mice performing spatial task in Morris water maze was published in 2007 (Korshunov and Averkin, 2007). Using high-impedance sharp electrodes we managed to overcome many technical difficulties. Nevertheless, the disadvantage of this recording technique is the relatively short (h) time of recording. If the experiments require very long times (days and weeks) of stable recordings, chronically implanted fine wires are more suitable. Single wire electrodes are successfully used for recordings in the cortex, thalamus, and other brain structures where the neurons are not densely packed. Nevertheless, this technique also has some disadvantages. Analysis of several papers (Rotenberg et al., 1996, Oka and Imanishi, 2000, Rennaker et al., 2005) shows that only 30–40% (in the best case) of chronically implanted single wires can record cells. Thus, in order to obtain any recordings with this method, it is necessary to implant several wires. Also, single wire electrodes are less effective in brain structures with high cell density because these electrodes have low selectivity and record the activity of a large number of cells. In order to increase the selectivity, several wires are fixed together to provide multichannel recording of the same group of cells. Off-line analysis of recordings on the basis of temporal coherence of spikes across channels is used for single unit sorting (McNaughton et al., 1983). Thus in both cases a multichannel preamplifier is required. Recordings in swimming tasks cause additional technical challenges. The construction should be waterproof and as light as possible. If the recording device fixed onto the skull is heavy, a swimming animal wastes too much energy to hold the head above the water surface.

The first method for multichannel recording of neuronal activity in swimming task was applied in rats (Hollup et al., 2001a, Hollup et al., 2001b, Fyhn et al., 2002). The headstage connections were shielded from the water using Vaseline. Nevertheless, this approach does not seem to be effective enough, because experimental animals can dive during swimming (see reference Korshunov and Averkin, 2007); in such cases the contacts can be scarcely protected from water by this technique. Also all existing multi-electrode arrays and multichannel preamplifiers are too large and heavy for swimming mice.

A design for a miniature, waterproof, multichannel preamplifier for recording neuronal activity in freely moving and swimming small animals is described. The construction provides stable recordings of neuronal activity even if the animal is diving and swimming under the water surface.