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-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 303 12.1 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 hippocampal oscillations, see Buzsaki (2006) and O’Keefe (2007). The most prominent distinction in the hippocampal EEG of awake behaving rodents is that between ‘large irregular activity’ (LIA), typically present during stationary behaviours such as eating and grooming, and theta, which is very prominent during behaviours which involve spatial translation of the head (Vanderwolf 1969; O’Keefe and Nadel 1978) or arousal and anxiety (e.g. Green and Arduini 1954; Sainsbury 1998; Seidenbecher et al. 2003). In the next section, we discuss the idea of two types or components of theta. The typical observation is that LIA and theta are exclusive and dominant hippocampal EEG states. That is to say, either LIA occurs or theta occurs, and higher-frequency oscillations accompany LIA or theta. ‘Small irregular activity’ has also been described (Vanderwolf 1969; Jarosiewicz et al. 2002; Jarosiewicz and Skaggs 2004a, b), which may be an intermediate state between LIA and theta, occurring during sleep and during transitions to alertness. During sleep, the characteristic EEG states are LIA, SIA, theta during REM sleep, and a more recently described slow oscillation which may be linked to neocortical input (Wolansky et al. 2006). Oscillations intermediate between theta and gamma have generally received comparatively little attention. As noted above, a hippocampal ‘alpha’ is not really recognised. An oscillation termed ‘flutter’ has been reported, occurring at around 10–12 Hz, which does not show phase reversal across the CA1 pyramidal layer, and is most prominent when an environment is familiar rather than novel (Nerad and Bilkey 2005). Berke et al. (2008) reported transient beta oscillations in CA3 and CA1 fields in the 23–30 Hz (‘beta2’) range which were highly modulated by environmental novelty. These beta oscillations were most prominent on the second and third laps of continuous linear tracks and were greatly attenuated when an environment was familiar. Grossberg (2009) has interpreted this oscillation within the framework of adaptive resonance theory and has suggested that it reflects a 304 C. Lever et al.