Abstract
Theta rhythmic fluctuations in the hippocampal–entorhinal circuit are believed to reflect rapid transitions between modes of mnemonic processing. Specifically, activity at the trough and peak of CA1 pyramidal layer theta is thought to correspond to retrieval and encoding related processing, respectively. Spatially tuned “grid cells” in layers II and III of the medial entorhinal cortex preferentially spike during the trough and peak phases of theta, respectively. Such differences suggest differential involvement of these layers to the processes of retrieval and encoding. It remains unknown, however, if the properties of grid cells that spike preferentially at the trough vs. the peak of theta differ systematically. Such putative differences would offer insights into the differential processing that occurs during these two phases. The goal of the present work was to contrast these types of grid cells. We found that significant functional dissociations do exist: trough locked grid cells carried more spatial information, had a higher degree of head direction tuning, and were more likely to phase precess. Thus, grid cells that activate during the putative retrieval phase of theta (trough) have a greater degree of location, orientation, and temporal tuning specificity relative to grid cells that activate during the putative encoding phase (peak), potentially reflecting the influence of the retrieved content. Additionally, trough locked grid cells had a lower average firing rate, were more likely to burst, and were less phase locked to high-gamma (∼80 Hz). Further analyses revealed they had different waveforms profiles and that systemic blockade of muscarinic acetylcholine receptors reduced the spatial tuning of both types, although these differences were only significant for the peak locked grid cells. These differences suggest that trough and peak locked grid cells are distinct populations of neurons.
Highlights
The prominent 6–10 Hz theta rhythmic fluctuation in neural activity of the hippocampal–entorhinal circuit is believed to reflect rapid, frequent transitions between modes of neural information processing (Hasselmo et al, 2002; Norman et al, 2006; Douchamps et al, 2013)
Analyses of the basic physiology of trough and peak locked grid cells revealed different profiles of the extracellularly recorded waveforms and showed that, while systemic blockade of muscarinic acetylcholine receptors reduced the spatial tuning of both types, these differences were only significant for the peak locked grid cells
As described in detail below, we found that grid cells that lock to the peak and trough of layer III theta differed significantly with respect to the quality of spatial tuning, the degree of head direction tuning expressed, and the incidence of phase precession
Summary
The prominent 6–10 Hz theta rhythmic fluctuation in neural activity of the hippocampal–entorhinal circuit is believed to reflect rapid, frequent transitions between modes of neural information processing (Hasselmo et al, 2002; Norman et al, 2006; Douchamps et al, 2013). Entorhinal input, carrying information from cortical processing streams, for example, arrives in hippocampal area CA1 at the opposite phase of theta than does input from hippocampal autoassociation region CA3 (Buzsáki et al, 1983; Brankack et al, 1993) This temporal segregation led to the idea that distinct mnemonic encoding and retrieval phases exist, corresponding to the arrival of the entorhinal and CA3 input, respectively (Hasselmo et al, 2002). A reversal in theta phase locking preferences between layers II and III of the entorhinal cortex (Mizuseki et al, 2009) likewise suggests a differential involvement of these layers in these mnemonic processes Consistent with this idea, the projections from these layers into the hippocampus are largely segregated. Layer II, on the other hand, projects predominantly to the dentate gyrus (DG) and area CA3 (Steward and Scoville, 1976; Amaral and Witter, 1989), but a subset of layer II neurons synapse onto inhibitory interneurons among the distal dendrites of area CA1 (Kitamura et al, 2014)
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