Abstract

Hippocampal theta has been related to locomotor speed, attention, anxiety, sensorimotor integration and memory among other emergent phenomena. One difficulty in understanding the function of theta is that the hippocampus (HPC) modulates voluntary behavior at the same time that it processes sensory input. Both functions are correlated with characteristic changes in theta indices. The current review highlights a series of studies examining theta local field potential (LFP) signals across the septotemporal or longitudinal axis of the HPC. While the theta signal is coherent throughout the entirety of the HPC, the amplitude, but not the frequency, of theta varies significantly across its three-dimensional expanse. We suggest that the theta signal offers a rich vein of information about how distributed neuronal ensembles support emergent function. Further, we speculate that emergent function across the long axis varies with respect to spatiotemporal scale. Thus, septal HPC processes details of the proximal spatiotemporal environment while more temporal aspects process larger spaces and wider time-scales. The degree to which emergent functions are supported by the synchronization of theta across the septotemporal axis is an open question. Our working model is that theta synchrony serves to bind ensembles representing varying resolutions of spatiotemporal information at interdependent septotemporal areas of the HPC. Such synchrony and cooperative interactions along the septotemporal axis likely support memory formation and subsequent consolidation and retrieval.

Highlights

  • You remember the last moment of experience, the last few moments and a variable stream of experience that can extend minutes and hours into the past

  • Summary Here, we indicate that HPC theta oscillations can be related to locomotion, sensory and spatial novelty as well as recent experience

  • Data from our lab and others support a role for the septotemporal axis in the processing of spatial and sensory novelty---both exerting fundamentally different effects on theta dynamics

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Summary

Introduction

You remember the last moment of experience, the last few moments and a variable stream of experience that can extend minutes and hours into the past. The septotemporal axis of the HPC can be subdivided into a septal (dorsal), intermediate and temporal (ventral) portions based on variation in entorhinal inputs (Dolorfo and Amaral, 1998a,b), subcortical projections (Risold and Swanson, 1996) and gene expression (Dong et al, 2009; Fanselow and Dong, 2010; see Strange et al, 2014 for review). Neurons within rostrocaudal bands more medially innervate progressively more temporal aspects of the HPC (Steward and Scoville, 1976; Wyss, 1981; Ruth et al, 1988; Witter et al, 1989; Dolorfo and Amaral, 1998a; see Canto et al, 2008 for review) This is true for EC layer 2 projections to the DG and CA3 as well as layer 3 projections to CA1 (see Figure 1A).

The Hippocampal Theta Signal
Variation in Theta Inputs
Spatial Novelty and Experience Variation
Sensory Novelty
Cognition and the Hippocampal Formation
Conceptual Framework

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