Abstract
Hippocampal place cells encode an animal's past, current, and future location through sequences of action potentials generated within each cycle of the network theta rhythm. These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies. Instead, we find through simulations and analysis of experimental data that rate and phase coding in independent neurons is sufficient to explain the organization of CA1 population activity during theta states. We show that CA1 population activity can be described as an evolving traveling wave that exhibits phase coding, rate coding, spike sequences and that generates an emergent population theta rhythm. We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity. Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.
Highlights
Cognitive processes are thought to involve the organization of neuronal activity into phase sequences, reflecting sequential activation of different cell assemblies (Hebb, 1949; Harris, 2005; Buzsaki, 2010; Wallace and Kerr, 2010; Palm et al, 2014)
As an animal moves through the firing field of a single CA1 neuron, there is an advance in the phase of its action potentials relative to the extracellular theta cycle (O’Keefe and Recce, 1993)
The previous model addresses only the temporal dynamics of single unit activity and population average activity, without addressing the spatiotemporal patterns of spiking activity within the population, the nature of which is a central question in the present study
Summary
Cognitive processes are thought to involve the organization of neuronal activity into phase sequences, reflecting sequential activation of different cell assemblies (Hebb, 1949; Harris, 2005; Buzsaki, 2010; Wallace and Kerr, 2010; Palm et al, 2014). Populations of CA1 neurons active at a particular phase of theta encode the animal’s recent, current, or future positions (Figure 1A,B) One explanation for these observations is that synaptic output from an active cell assembly ensures its other members are synchronously activated and in addition drives subsequent activation of different assemblies to generate a phase sequence (Figure 1C) (Harris, 2005). We refer to this as the coordinated assembly hypothesis. An alternative possibility is that independent single cell coding is sufficient to account for population activity According to this hypothesis, currently active assemblies do not determine the identity of future assemblies (Figure 1D).
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