Spatial Firing Correlates of Physiologically Distinct Cell Types of the Rat Dentate Gyrus

Abstract

The dentate gyrus (DG) occupies a key position in information flow through the hippocampus. Its principal cell, the granule cell, has spatially selective place fields. However, the behavioral correlates of cells located in the hilus of the rat dentate gyrus are unknown. We report here that cells below the granule layer show spatially selective firing that consists of multiple subfields. Other cells recorded from the DG had single place fields. Compared to cells with multiple fields, cells with single fields fired at lower rates during sleep; were less bursty; and were more likely to be recorded simultaneously with large populations of neurons that were active during sleep and silent during behavior. We propose that cells with single fields are likely to be mature granule cells that use sparse encoding to potentially disambiguate input patterns. Furthermore, we hypothesize that cells with multiple fields might be cells of the hilus or newborn granule cells. These data are the first demonstration, based on physiological criteria, that single-field and multiple-field cells constitute at least two distinct cell classes in the DG. Because of the heterogeneity of firing correlates and cell types in the DG, understanding which cell types correspond to which firing patterns, and how these correlates change with behavioral state and between different environments, are critical questions for testing longstanding computational theories that the DG performs a pattern separation function using a very sparse coding strategy.

Adult neurogenesis in the mammalian hippocampus: Why the dentate gyrus?

“…Sparse DG activity was originally noted by O'Keefe and colleagues during their seminal work defining the in vivo firing properties of hippocampal neurons (O'Keefe and Nadel 1978) and very sparse activity is now viewed as a distinctive feature of the DG (Chawla et al 2005;Neunuebel and Knierim 2012). Over the subsequent three-and-half decades surprisingly few papers have been published on the natural firing patterns of DG GCs, indicative of the technical difficulties of recording in this area.…”

“…However, Neunuebel and Knierim (2012) have recently suggested that previous studies may not have been recording from matGCs. By systematically tracking the position of their recording electrodes through the GCL, these authors report that matGCs in the outer GCL have single, small, discrete place fields, i.e., each matGC represents a very specific aspect of a given environment.…”

“…Cells with multiple place fields were only observed at the GCL -hilus border, which led to the suggestion that previous reports (e.g., Jung and McNaughton 1993;Leutgeb et al 2007) may have reported the spiking of either mossy cells or abGCs. Neunuebel and Knierim (2012) only reported GC activity in a single environment. Clarification of these issues and further characterization of GC activity in vivo, hence, awaits further investigation.…”

“…To conclusively define if and how abGCs behave differently from matGCs, parallel characterization of the two populations' activity in awake-behaving animals will be required. We envisage that shortly the use of either in vivo single-unit electrophysiology (Leutgeb et al 2007;Neunuebel and Knierim 2012) or in vivo population-activity imaging (Dombeck et al 2010) coupled with genetic tools for identifying and/or manipulating abGCs and matGCs will shed significant light on these questions.…”

Theta-gamma-modulated synaptic currents in hippocampal granule cells in vivo define a mechanism for network oscillations

“…In Vivo The firing pattern of mature GCs in vivo is largely unclear (Neunuebel and Knierim, 2012). We therefore first determined the frequency of action potential initiation in rigorously identified mature GCs in vivo ( Figure 2; Table 1).…”