Abstract
Encoding of behavioral episodes as spike sequences during hippocampal theta oscillations provides a neural substrate for computations on events extended across time and space. However, the mechanisms underlying the numerous and diverse experimentally observed properties of theta sequences remain poorly understood. Here we account for theta sequences using a novel model constrained by the septo-hippocampal circuitry. We show that when spontaneously active interneurons integrate spatial signals and theta frequency pacemaker inputs, they generate phase precessing action potentials that can coordinate theta sequences in place cell populations. We reveal novel constraints on sequence generation, predict cellular properties and neural dynamics that characterize sequence compression, identify circuit organization principles for high capacity sequential representation, and show that theta sequences can be used as substrates for association of conditioned stimuli with recent and upcoming events. Our results suggest mechanisms for flexible sequence compression that are suited to associative learning across an animal's lifespan.
Highlights
Whereas many behaviorally important events take place on timescales of seconds, neuronal membrane dynamics operate at a millisecond timescale
The discovery that during movement hippocampal place cells fire action potentials with timing that precesses relative to the hippocampal theta rhythm (O’Keefe and Recce, 1993), and that time-compressed representations of behavioral sequences occur as spike sequences within each theta cycle (Skaggs et al, 1996; Dragoi and Buzsaki, 2006; Foster and Wilson, 2007), suggests that hippocampal activity is organized so that computations on a millisecond neural timescale can address events on behavioral timescales
Whereas in many previous models precession is assumed to arise from oscillatory drive targeting place cells, the frequency of theta is established by septal GABAergic projections to hippocampal interneurons (Freund and Antal, 1988), which in turn coordinate the spiking activity of local CA1 pyramidal cells (Royer et al, 2012)
Summary
Whereas many behaviorally important events take place on timescales of seconds, neuronal membrane dynamics operate at a millisecond timescale. The discovery that during movement hippocampal place cells fire action potentials with timing that precesses relative to the hippocampal theta rhythm (O’Keefe and Recce, 1993), and that time-compressed representations of behavioral sequences occur as spike sequences within each theta cycle (Skaggs et al, 1996; Dragoi and Buzsaki, 2006; Foster and Wilson, 2007), suggests that hippocampal activity is organized so that computations on a millisecond neural timescale can address events on behavioral timescales. The rate at which action potentials precess relative to the theta rhythm depends on an animal’s speed of movement (Geisler et al, 2007). Theta sequences emerge within theta waves that propagate along the dorsoventral
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