Abstract
The receptive field of a neuron describes the regions of a stimulus space where the neuron is consistently active. Sparse spiking outside of the receptive field is often considered to be noise, rather than a reflection of information processing. Whether this characterization is accurate remains unclear. We therefore contrasted the sparse, temporally isolated spiking of hippocampal CA1 place cells to the consistent, temporally adjacent spiking seen within their spatial receptive fields ("place fields"). We found that isolated spikes, which occur during locomotion, are strongly phase coupled to hippocampal theta oscillations and transiently express coherent nonlocal spatial representations. Further, prefrontal cortical activity is coordinated with and can predict the occurrence of future isolated spiking events. Rather than local noise within the hippocampus, sparse, isolated place cell spiking reflects a coordinated cortical-hippocampal process consistent with the generation of nonlocal scenario representations during active navigation.
Highlights
The concept of a receptive field [1,2,3] provides a fundamental model for how neural spiking can convey information about features in the external environment
In order to understand the extent of isolated spiking during active behavior and to identify a potential function of this activity, we took an unbiased approach where we surveyed CA1 place cell spiking across all movement periods as animals performed a spatial navigation task in a complex environment with multiple linear track segments [45,46] (Fig 1A and 1B)
Given that isolated spikes occur at late phases of theta and are separated from adjacent spiking both in time and space, could isolated spiking reflect the transient activity of cell assemblies with place field activity in another part of the environment? If so, we would expect that pairs of neurons that are coactive during periods of adjacent spiking, corresponding to cells that are likely to have overlapping place fields, would be coactive within a theta cycle containing isolated spiking events. We examined this possibility by using an approach that has been used to demonstrate reactivation of nonlocal spatial representations during sharp-wave ripple (SWR), where a pair of place cells is more likely to spike together if their place fields overlap [57,58] (Fig 5A)
Summary
The concept of a receptive field [1,2,3] provides a fundamental model for how neural spiking can convey information about features in the external environment. CA1 and CA3 place cells can emit spikes outside of their place fields as an animal approaches choice points [27,28] and during vicarious trial and error [27] or when an animal is traveling in the opposite direction over a location with a place field [28] These events are hypothesized to reflect noncurrent scenarios, such as simulating possible future scenarios when a decision needs to be made [28,29]. Our examination of isolated spiking of place cells revealed that these events reflect the coherent activation of hippocampal representations of physically distant locations and that these events are coordinated with ongoing activity in the PFC. These findings suggest that isolated spikes are a signature of distributed and coherent information processing in the brain
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