Abstract

Local field potentials (LFPs) contain signals generated by individual neurons and by coordinated population activity, but distinguishing these contributions remains a challenge. We examined how hippocampal LFPs at different frequencies predict single-neuron spiking during spatial navigation in male rats using two datasets. At each frequency, we assessed the spatial distribution of LFP-based prediction across the electrode array and its generalization across behavioral contexts in which a neuron remained active, but its co-active peers changed. For pyramidal cells, spatially distributed LFP features, consistent with population-level activity, contributed primarily to spike prediction at theta (~10 Hz) and its harmonics. In contrast, spatially localized signals, consistent with the recorded neuron's activity, contributed predominantly at higher frequencies. Notably, gamma-band LFPs (30-80 Hz) provided comparatively little information about pyramidal-cell spiking, while distributed LFP features predicted interneuron spiking across a broader frequency range. Together, this predictive approach separates local and distributed correlates of spiking within the LFP. In hippocampal CA1, these correlates fell into two spatiotemporal regimes: a distributed regime expressed primarily at theta frequencies and a localized regime reflecting single-neuron activity at higher frequencies.