Multimodal MEG and microstructure-MRI investigations of the human hippocampal scene network

Although several studies have demonstrated that perceptual discrimination of complex scenes relies on an extended hippocampal posteromedial system, we currently have limited insight into the specific functional and structural properties of this system in humans. Here, combining electrophysiological (magnetoencephalography, MEG) and advanced microstructural (multi-shell diffusion MRI, dMRI; quantitative magnetisation transfer, qMT) imaging in healthy human adults (30 female/10 male), we show that both theta power modulation of the hippocampus, and fibre restriction/hindrance (reflecting axon packing/myelination) of the fornix (a major input/output pathway of the hippocampus), were independently related to scene, but not face, perceptual discrimination accuracy. Conversely, microstructural features of the inferior longitudinal fasciculus (a long-range occipito-anterotemporal tract) correlated with face, but not scene, perceptual discrimination accuracy. Our results provide new mechanistic insight into the neurocognitive systems underpinning complex scene discrimination, providing novel support for the idea of multiple processing streams within the human medial temporal lobe. Significance Statement In contrast to theories positing segregated cortical areas for perception and memory, the specialized representations of the hippocampus may support both the perception and memory of visual scenes. To investigate, we utilised the unique window into hippocampal electrophysiological activity offered by magnetoencephalography (MEG). We found hippocampal theta activity modulations in the hippocampus and posteromedial cortex during scene, versus face and shape-size, perceptual odd-one-out discrimination, the magnitude of which correlated with scene, but not face or shape-size, discrimination accuracy. Moreover, multimodal white matter imaging revealed that specific microstructural features of the fornix – the major hippocampal output tract - independently predicted scene discrimination performance. Our multimodal MEG-microstructure study provides novel evidence that the hippocampus and connected structures conjointly support online scene processing.