Elsevier

NeuroImage

Volume 85, Part 2, 15 January 2014, Pages 656-666
NeuroImage

Review
Theta rhythm and the encoding and retrieval of space and time

https://doi.org/10.1016/j.neuroimage.2013.06.022Get rights and content

Highlights

  • Theta rhythm in hippocampus and entorhinal cortex contributes to memory behavior.

  • Physiological data suggests separate phases of encoding and retrieval during theta.

  • Theta rhythm in entorhinal cells and networks contributes to grid cell periodicity.

  • Models of grid cells utilize theta frequency resonance and attractor dynamics.

  • Theta rhythm contributes to coding space and time in models of episodic memory.

Abstract

Physiological data demonstrates theta frequency oscillations associated with memory function and spatial behavior. Modeling and data from animals provide a perspective on the functional role of theta rhythm, including correlations with behavioral performance and coding by timing of spikes relative to phase of oscillations. Data supports a theorized role of theta rhythm in setting the dynamics for encoding and retrieval within cortical circuits. Recent data also supports models showing how network and cellular theta rhythmicity allows neurons in the entorhinal cortex and hippocampus to code time and space as a possible substrate for encoding events in episodic memory. Here we discuss these models and relate them to current physiological and behavioral data.

Introduction

Theta frequency oscillations appear in electroencephalographic (EEG) recordings from scalp electrodes and depth electrodes in human subjects, but controversy continues over the functional role of theta frequency oscillations (commonly referred to as theta rhythm). Understanding the functional role of theta rhythm will benefit from attention to data on the role of theta rhythm in animals. Here we will review data on theta rhythm in humans and animals and recent theories linking theta rhythm to mechanisms of memory and spatial navigation.

Section snippets

Theta rhythm in humans and animals

In early EEG studies in humans (Niedermeyer, 1999), Hans Berger used the Greek letter alpha to designate 8–12 Hz frequencies observed first in resting participants, then used beta for 12–30 Hz frequencies in more attentive participants. Subsequently, gamma (30 to 100 Hz), and delta (below 4 Hz) were named. The 4 to 7 Hz band was designated theta (Walter and Dovey, 1944) to stand for thalamus (Niedermeyer, 1999) because thalamic lesions in monkeys shifted cortical dynamics from alpha (8–12 Hz) to

Theta rhythm may provide separate phases of encoding and retrieval

The behavioral data indicates a role of theta rhythm in the encoding of new information, but the mechanisms for this role are not known. Modeling shows how specific physiological processes at different phases of theta rhythm could enhance encoding by separating the dynamics of encoding and retrieval on different phases of the theta rhythm (Hasselmo et al., 2002a).

Memory requires separation of information arriving from the external world, to be encoded as new, from the information retrieved from

Theta rhythm and models of the phase coding of space

The extensive data on theta phase precession (Huxter et al., 2003, Huxter et al., 2008, Mehta et al., 2002, Mizuseki et al., 2009, O'Keefe and Recce, 1993, Skaggs et al., 1996) inspired a range of models addressing how the phase of spiking relative to theta rhythm codes the spatial location of an animal (Geisler et al., 2007, Jensen and Lisman, 1996, O'Keefe and Recce, 1993, Tsodyks et al., 1996, Wallenstein and Hasselmo, 1997, Samsonovich and McNaughton, 1997). The first paper on theta phase

Theta rhythm and episodic memory

Theta rhythm may contribute to encoding the where and when of episodic memory. In addition to coding spatial location, neurons in the hippocampus and entorhinal cortex also respond selectively at consistent time points within the trials of a behavioral task (Kraus et al., in press, MacDonald et al., 2011, Pastalkova et al., 2008). These responses have been referred to as “time cells” (MacDonald et al., 2011). The firing of time cells could allow events or items to be associated with a specific

Acknowledgments

Research supported by R01 MH60013, R01 MH61492, Silvio O. Conte Center P50 MH094263 and the Office of Naval Research MURI grant N00014-10-1-0936.

Conflict of interest

The authors have no conflicts of interest.

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