eNeuro. 2024 Apr 15:ENEURO.0180-23.2024. doi: 10.1523/ENEURO.0180-23.2024. Online ahead of print.

ABSTRACT

Phase-entrainment of cells by theta oscillations is thought to globally coordinate the activity of cell assemblies across different structures, such as the hippocampus and neocortex. This coordination is likely required for optimal processing of sensory input during recognition and decision-making processes. In quadruple-area ensemble recordings from male rats engaged in a multisensory discrimination task, we investigated phase-entrainment of cells by theta oscillations in areas along the cortico-hippocampal hierarchy: somatosensory barrel (S1BF), secondary visual cortex (V2L), perirhinal cortex (PER) and dorsal hippocampus (dHC). Rats discriminated between two 3D objects presented in tactile-only, visual-only or both tactile and visual modalities. During task engagement, S1BF, V2L, PER and dHC LFP signals showed coherent theta-band activity. We found phase-entrainment of single-cell spiking activity to locally recorded as well as hippocampal theta activity in S1BF, V2L, PER and dHC. While phase-entrainment of hippocampal spikes to local theta oscillations occurred during sustained epochs of task trials and was nonselective for behavior and modality, somatosensory and visual cortical cells were only phase-entrained during stimulus presentation and mainly in their preferred modality (S1BF – tactile, V2L – visual). This effect could not be explained by modulations of firing rate or theta amplitude. Groups of cells in S1BF and V2L were phase-entrained in a cross-modal fashion (S1BF spikes to V2L LFP; V2L spikes to S1BF LFP). Whereas hippocampal cells are thus theta phase-entrained during prolonged task periods, sensory and perirhinal neurons are selectively entrained during a stimulus-locked period, providing a brief time window for coordination of activity.Significance Statement Neural activity during theta oscillations (6-12 Hz) has long been considered a mechanism for inter-areal communication, but its temporal dynamics in relation to sensory and mnemonic processing are still poorly understood. We report how sensory neocortical and hippocampal areas temporally coordinate their activity with local field potential activity in the theta-band during a behavioral task involving multisensory object discrimination and recognition. Theta phase entrainment in sensory cortical areas selectively occurred during behavioral task epochs where object information was presented in the preferred stimulus modality of a given area. This entrainment was largely independent of firing rate. These findings support the framework of theta-band synchrony as a mechanism for facilitating cortical-hippocampal communication during sensory and mnemonic processing.

PMID:38621992 | DOI:10.1523/ENEURO.0180-23.2024