Hippocampal and cortical oscillatory dynamics reflect semantic processing and predict behavioural performance

Semantic priming is thought to reflect that semantically related words activate overlapping neural tissue causing a behavioural facilitation effect for processing the subsequent stimulus, but this interpretation is speculative since most studies to date have not used tasks that require explicit semantic judgments. Here, 33 participants completed an explicit semantic priming task during magnetoencephalography (MEG). MEG data were transformed into the time-frequency domain and significant task-related oscillatory responses were source-imaged using a beamformer. Whole-brain paired-sample Student's t-tests were conducted to evaluate conditional differences in neural recruitment. Additionally, whole-brain subtraction maps were computed and correlated with conditional differences in reaction time (RT). Behaviourally, participants had significantly shorter RT in related trials compared to unrelated trials. Regarding the MEG data, we observed robust neural responses in theta, alpha and beta frequency bands in bilateral occipital and left temporo-parietal cortices. Whole-brain condition-wise analyses revealed stronger theta oscillations in bilateral hippocampi in the unrelated condition. Additionally, stronger decreases in alpha power in bilateral temporo-parietal, as well as beta power in temporal and medial occipital cortices were observed during related compared to unrelated trials. Finally, we found that conditional differences in theta activity in the lateral ventral occipitotemporal cortex (VOTC) and beta activity in the left inferior frontal gyrus (IFG) significantly predicted RT differences. These data suggest that there is bilateral recruitment of hippocampi, temporo-parietal and medial occipital regions during judgements of semantic relatedness. Additionally, these data promote the role of left VOTC and IFG in the executive control of semantic judgements. KEY POINTS: The brain regions and oscillatory dynamics underlying explicit semantic relatedness judgements are poorly understood. We leveraged the spatiotemporal precision of MEG to quantify the neuronal dynamics involved in judgements of semantic relatedness in healthy adult participants. We replicated classic behavioural findings and showed that a widespread network of multispectral hippocampal and cortical oscillatory activity underlies the semantic processing required to make judgements on relatedness, with behaviour correlating with neural responses in several areas. These findings reinforce the existing literature, add novel insight on the role of the hippocampus in semantic retrieval, and help illuminate the temporal brain dynamics that support semantic cognition during language processing.