Individual differences in theta-band oscillations in a spatial memory network revealed by EEG predict rapid place learning

Spatial memory has been closely related to the medial temporal lobe (MTL), and theta-oscillations are thought to play a key role. However, it remains difficult to investigate medio-temporal lobe (MTL) activation related to spatial memory with non-invasive electrophysiological methods in humans. Here, we combined the virtual delayed-matching-to-place (DMP) task, reverse-translated from the watermaze DMP task in rats, with high-density electroencephalography (EEG) recordings. Healthy young volunteers performed this computerised task in a virtual circular arena, which contained a hidden target whose location moved to a new place every four trials, allowing the assessment of rapid memory formation. Using behavioural measures as predictor variables for source reconstructed frequency specific EEG power, we found that inter-individual differences in search preference during probe trials, a measure of 1-trial place learning known from rodent studies to be particularly hippocampus dependent, correlated predominantly with distinct theta-band oscillations (approx. 7 Hz), particularly in the right temporal lobe, the right striatum and inferior occipital cortex or cerebellum. Notably, this pattern was found with very high consistency during both encoding and retrieval/expression, but not in control analyses and could not be explained by motor confounds. Alpha-activity in sensorimotor and parietal cortex contralateral to the hand used for navigation also correlated with search preference, which likely reflected movement-related factors associated with task performance. Relating inter-individual differences in ongoing brain activity to behaviour in a continuous rapid place learning task that is suitable for a variety of populations, we could demonstrate that memory related theta-band activity in temporal lobe can be measured with EEG recordings, revealing a presumed network of MTL, striatum and cerebellum and/or inferior occipital cortex that may interact through theta oscillations. This approach holds great potential for further studies investigating the interactions within this network during encoding and retrieval, as well as neuromodulatory impacts and age-related changes.