Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus

By Joshua P. Neunuebel, James J. Knierim. 2012

161 citations recorded by the source corpus.

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 with 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- 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 long-standing computational theories that the DG performs a pattern separation function using a very sparse coding strategy.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Developmental Neuroscience

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Citations in the corpus

Re-evaluating circuit mechanisms underlying pattern separation (2019, neutral): “Moreover, histological localisation can be insufficient to identify granule cells, as electrodes in the granule cell layer may pick up signals from large mossy cells in the hilus (Neunuebel and Knierim, 2012).”
Constitutive and Synaptic Activation of GIRK Channels Differentiates Mature and Newborn Dentate Granule Cells (2018, background): “The DG exhibits sparse neural activity wherein only a small fraction of the principal granule cells (GCs) are active at any given time and active GCs have generally low firing rates (Jung and McNaughton, 1993; Chawla et al., 2005; Leutgeb et al., 2007; Neunuebel and Knierim, 2012).”
Sparse activity of identified dentate granule cells during spatial exploration (2016, result): “Our data thus support a sparse coding scheme in the dentate gyrus and provide a possible link between structural and functional heterogeneity among the GC population.”
CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation (2014, background): “As discussed at length in a paper that presented data from the same animals as those reported here (Neunuebel and Knierim, 2012), it is impossible to distinguish from histology alone whether any individual, extracellularly recorded unit is a mature granule cell; an adult-born, immature granule cell;”
Hippocampal Memory Traces Are Differentially Modulated by Experience, Time, and Adult Neurogenesis (2014, result): “These results are somewhat surprising given the reported stabil- ity usually observed in place field recordings over time (Leutgeb et al., 2007, but see also Neunuebel and Knierim, 2012 for a different interpretation).”
Low excitatory innervation balances high intrinsic excitability of immature dentate neurons (2016, methodology): “Since the binomial relationship in equation (8) was not well suited for an analytical optimization of the parameters that globally minimize the error in equation (9), we used a Monte Carlo exploration of the space to find combinations of Nind, Nshared, and p that gave good fits.”
Tracking the Flow of Hippocampal Computation: Pattern Separation, Pattern Completion, and Attractor Dynamics (2015, background): “Although these criteria presumably excluded interneurons, it is not clear how many cells were fully mature granule cells, immature (newborn) granule cells, or mossy cells of the hilus region (Neunuebel & Knierim, 2012).”
Spatial representations of granule cells and mossy cells of the dentate gyrus (2017, background): “It was therefore essential to record long periods of sleep in order to identify granule cells, as it was otherwise easy tomove electrodes through the GCLwithout recording any cells (Jung and McNaughton, 1993; Skaggs et al., 1996; Neunuebel and Knierim, 2012).”
In vivo imaging of dentate gyrus mossy cells in behaving mice (2017, background): “, 2007), perhaps with preference toward adult-born GCs located closer to the hilar border (Neunuebel and Knierim, 2012), exhibit multiple firing fields.”
Distinct Determinants of Sparse Activation during Granule Cell Maturation (2013, background): “…It is well established that the DG uses sparse population coding with only a small percentage of GCs activated in response to physiological stimuli (Jung and McNaughton, 1993; Chawla et al., 2005; Ramirez-Amaya et al., 2006; Kee et al., 2007; Stone et al., 2011; Neunuebel and Knierim, 2012).”
Physiological properties and behavioral correlates of hippocampal granule cells and mossy cells (2017, unknown): “Such results are in keeping with Neunuebel and Knierim (2012), who distinguished between dentate neurons with single and multiple place fields, tentatively classifying neurons with single place fields as granule cells.”
Distinct Contribution of Adult-Born Hippocampal Granule Cells to Context Encoding (2016, unknown): “The level of activity was dependent on the animal’s behavioral state (Leutgeb et al., 2007; Neunuebel and Knierim, 2012), as calcium transients during running were observed at nearly 2-fold higher rate than during nonrunning epochs (Figure S2C).”
Theta-Gamma-Modulated Synaptic Currents in Hippocampal Granule Cells In Vivo Define a Mechanism for Network Oscillations (2014, background): “This seemed critical, since recent work raised doubts regarding the identity of previously recorded cells in the dentate gyrus (Neunuebel and Knierim, 2012).”