Exploring fast hippocampal network oscillations: Combining multi-electrode recordings with optical imaging and patch-clamp techniques
Mann EO., Paulsen O.
© 2006 Springer Science+Business Media, Inc. All rights reserved. Cortical processing depends on orchestrated activity across distributed neuronal assemblies, and network rhythms may provide a temporal structure relative to which individual neurons within these assemblies can be coordinated. Network oscillations in the gamma-frequency range (∼30 to 100 Hz) have received particular attention because they are prominent in the awake brain, and have been implicated in cognitive processes, such as sensory binding (Singer, 1993), selective attention (Fries et al., 2001), and consciousness (Llinas et al., 1998). Gamma rhythms can be observed in the hippocampus, where they have been implicated in memory processing (Lisman and Idiart, 1995; Jensen and Lisman, 1996), and in vivo multi-electrode techniques have already uncovered some of the mechanisms underlying these hippocampal gamma oscillations in the behaving animal (Bragin et al., 1995; Csicsvari et al., 2003). Adapting such multi-electrode techniques to an in vitro model of hippocampal gamma oscillations would enable a rigorous pharmacological and physiological dissection of the cellular and synaptic mechanisms underlying these rhythms. Furthermore, as hippocampal gamma oscillations represent the coordinated activity of assemblies of neurons, such an in vitro model would provide a convenient screen for potential psychoactive drugs at the network level (Gill et al., 2002; Weiss et al., 2003). Fast network oscillations can be induced in the hippocampal slice in vitro through a variety of paradigms, including patterned afferent stimulation (Whittington et al., 1995; Traub et al., 1996; Whittington et al., 1997), local application of drugs or solutions with altered ionic composition, for example, high potassium (LeBeau et al., 2002; Towers et al., 2002), bath application of kainate (Hajos et al., 2000; Hormuzdi et al., 2001), or drugs that activate metabotropic glutamate receptors (Whittington et al., 1995; Boddeke et al., 1997; Gillies et al., 2002) or muscarinic receptors (Fisahn et al., 1998; Shimono et al., 2000). The frequency of drug-induced oscillations is temperature-dependent. At room temperature, these oscillations are often in the beta-frequency range as defined in vivo (∼10 to 30 Hz), but commonly fall in the gamma-frequency band when recorded at or above 32°C (Ecker et al., 2001; Dickinson et al., 2003), and may therefore provide models for in vivo gamma oscillations. Although planar multi-electrode arrays offer an attractive opportunity to explore the underlying mechanisms and physiological relevance of these network oscillations, the majority of previous studies have been performed in interface-style chambers. Shimono et al. (2000) succeeded in inducing fast network oscillations in hippocampal slices mounted on planar multi-electrode arrays, by lowering the fluid level to create semi-interface conditions and using an atmosphere above the chamber of humidified carbogen gas (95% O 2 /5% CO 2 ). This development has facilitated the detailed study of spatiotemporal patterns of cellular and network events underlying fast hippocampal network oscillations in vitro (Shimono et al., 2000). In this chapter, we discuss how planar multi-electrode arrays can be used to study fast hippocampal network oscillations induced by activation of kainate, muscarinic, and metabotropic glutamate receptors. This includes practical guidelines for recording and analysis, as well as a discussion of current source density analysis, and emphasizes throughout how to optimize the conditions for combining multi-electrode recordings with optical imaging using voltage-sensitive dyes and patch-clamp recordings from single neurons.