Independent rate and temporal coding in hippocampal pyramidal cells

By J. Huxter, Neil Burgess, John O'Keefe. Nature, 2003

598 citations recorded by the source corpus.

In the brain, hippocampal pyramidal cells use temporal as well as rate coding to signal spatial aspects of the animal's environment or behaviour. The temporal code takes the form of a phase relationship to the concurrent cycle of the hippocampal electroencephalogram theta rhythm. These two codes could each represent a different variable. However, this requires the rate and phase to vary independently, in contrast to recent suggestions that they are tightly coupled, both reflecting the amplitude of the cell's input. Here we show that the time of firing and firing rate are dissociable, and can represent two independent variables: respectively the animal's location within the place field, and its speed of movement through the field. Independent encoding of location together with actions and stimuli occurring there may help to explain the dual roles of the hippocampus in spatial and episodic memory, or may indicate a more general role of the hippocampus in relational/declarative memory.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/2e4dd28d8cd2be13ea8db59bf40e425db1e3ab43

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Citations in the corpus

Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory (2005, background): “Recently, Huxter et al. (2003) suggested that firing rate is of secondary importance for place coding and that the liberated rate dimension is available for coding something else.”
An oscillatory interference model of grid cell firing (2007, background): “In addition, the phase of firing continues to accurately represent location despite large variations in the firing rate (which may encode nonspatial variables such as speed, Huxter et al., 2003).”
Neural syntax: cell assemblies, synapsembles and readers (2010, unknown): “…mechanisms may simultaneously monitor the activity of the same assembly patterns and may extract different types of meanings, for example temporal relationships for one feature and spiking intensity for another (Hirase et al., 1999; Huxter et al., 2003; Konishi, 1990; Niessing and Friedrich, 2010).”
What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data (2005, background): “…cells’’ in the hippocampus (O’Keefe and Dostrovsky, 1971; O’Keefe, 1976; McNaughton et al., 1983; Muller et al., 1987; Eichenbaum et al., 1989; Muller and Kubie, 1989; Wiener et al., 1989; Skaggs et al., 1996; Wood et al., 2000; Huxter et al., 2003) and EC (Barnes et al., 1990; Frank et al., 2000).”
Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point (2007, background): “Place fields were defined as a contiguous region with an average firing rate exceeding 20% peak field rate (Huxter et al., 2003; Leutgeb et al., 2004).”
Place cells, grid cells, and the brain's spatial representation system. (2008, background): “…earlier phases of the theta rhythm during traversal of the place field increases the information about the animal’s location in the environment, both in one-dimensional ( Jensen & Lisman 2000, Harris et al. 2003, Huxter et al. 2003) and two-dimensional (Huxter et al. 2007) environments.”
Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb (2014, unknown): “The general idea of dissociable rate and temporal codes has been explored e.g. in the hippocampus where firing rate and phase within a theta cycle have been suggested to represent different variables 48 .”
Temporal encoding of place sequences by hippocampal cell assemblies. (2006, methodology): “…that the linear nature of phase precession of place cell spikes through the entire theta cycle in mul- tiple cells serves to disambiguate the relative position of the animal, in accordance with the common theta drive model (O’Keefe and Recce, 1993; Jensen and Lisman, 2000; Huxter et al., 2003).”
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition (2010, background): “The spike timing of a hippocampal neuron systematically shifts to an earlier phase of the theta cycle as the rat moves across the cell’s place field, a phenomenon called “phase precession” (254, 456, 740, 881, 1080) (Fig.”
Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information (2008, background): “, 2001) or temporal codes based on spike timing relative to LFP phases (Buzsaki, 2002; Mehta et al., 2002; Huxter et al., 2003; Montemurro et al., 2008).”
Sequence Learning and the Role of the Hippocampus in Rodent Navigation (2012, unknown): “This variability, coupled with the variability of place cell firing rates from trial to trial [40] and the dependence of the rate of precession on the size of a place field [41,42], made the prediction of sequences nontrivial.”
Gamma-band synchronization in the neocortex: novel analysis methods and their application to sensory and motivational systems (2013, background): “One problem with this model however is that firing rates start to decrease when a rat has moved beyond the center of the place field, while the spike’s theta phases continue to advance (Huxter et al., 2003; O’Keefe & Burgess, 2005).”
Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. (2006, background): “In waking exploration, some of the neuronal and assembly firing patterns are independent of the location of the animal (Wood et al., 1999; Harris et al., 2003; Huxter et al., 2003).”
Hippocampal mechanisms for the context-dependent retrieval of episodes (2005, unknown): “…of the virtual rat had a higher resolution than the internal state vector, consistent with the fact that a single place cell may fire over an extended region of the environment (Huxter et al., 2003; Muller & Kubie, 1989; Muller, Kubie, & Ranck, 1987; Skaggs et al., 1996; Wood et al., 2000).”