The Function of Oscillations in the Hippocampal Formation

Some of the strongest experimental and computational links between oscillations and cognition concern the oscillations in the hippocampal formation supporting spatial and mnemonic processing. We review experimental and theoretical work concerning well-est

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Colin Lever, Raphael Kaplan, and Neil Burgess

Abstract

Some of the strongest experimental and computational links between oscillations and cognition concern the oscillations in the hippocampal formation supporting spatial and mnemonic processing. We review experimental and theoretical work concerning well-established hippocampal oscillations such as theta, gamma, and high-frequency ripples and how they relate to spatial, mnemonic, and anxietyrelated representation and behaviour. We specifically consider the following computational roles for oscillations: organising processing into discrete chunks, as seen in encoding versus retrieval scheduling; ordinal and metric coding by oscillatory phase; temporal integration by oscillatory phase; and interregional communication. The literature on oscillations has typically been concerned with changes in band-specific power. Here, focusing on the theta oscillation, we summarise how key variables are linked not only to power but also to frequency and to coherence. We conclude that the hippocampal formation provides an invaluable model system for understanding the functional roles of neuronal oscillations and the interaction between oscillations.

C. Lever (*) Department of Psychology, University of Durham, Durham DH1 3LE, UK e-mail: [email protected] R. Kaplan Laboratory of Brain and Cognition, National Institute of Mental Health, Bethseda, MD, USA UCL Institute of Cognitive Neuroscience, London WC1N 3AR, UK N. Burgess (*) UCL Institute of Cognitive Neuroscience, London WC1N 3AR, UK UCL Institute of Neurology, London WC1N 3BG, UK e-mail: [email protected] D. Derdikman and J.J. Knierim (eds.), Space, Time and Memory in the Hippocampal Formation, DOI 10.1007/978-3-7091-1292-2_12, # Springer-Verlag Wien 2014

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12.1

C. Lever et al.

Different Types of Hippocampal Oscillations

12.1.1 Characteristic Oscillations in the Rodent Hippocampus It is perhaps worth stating at the outset that the characteristic oscillatory bands historically defined by human scalp EEG are of only limited relevance to those identified by invasive electrophysiological studies of the rodent hippocampus. At the lower-frequency end, researchers of the rodent hippocampus do not consider there to be a distinct ‘alpha’ (8–12 Hz) oscillation. Rather, it seems that the theta oscillation extends into ‘alpha’ territory, and theta is typically assigned a range of around 4–12 Hz. Indeed, the upper limit of rodent hippocampal theta seems higher than that typically found in intracranial and magnetoencephalographic (MEG) studies of the human hippocampal formation, an issue we briefly discuss in Sect. 12.1.3. At the higher-frequency end, there is a lot of important hippocampal activity beyond 100 Hz: most notably, the high band (90–150 Hz) of gamma oscillations (30–150 Hz; Bragin et al. 1995; Csicsvari et al. 2003; Scheffer-Teixeira et al. 2011; Belluscio et al. 2012) and ripple oscillations (140–200 Hz, O’Keefe and Nadel 1978, pp. 150–153; Bragin et al. 1999;). For excellent general reviews of hippoc