Multimodal imaging of repetition priming: Using fMRI, MEG, and intracranial EEG to reveal spatiotemporal profiles of word processing

Abstract

Repetition priming is a core feature of memory processing whose anatomical correlates remain poorly understood. In this study, we use advanced multimodal imaging (functional magnetic resonance imaging (fMRI) and magnetoencephalography; MEG) to investigate the spatiotemporal profile of repetition priming. We use intracranial electroencephalography (iEEG) to validate our fMRI/MEG measurements. Twelve controls completed a semantic judgment task with fMRI and MEG that included words presented once (new, 'N') and words that repeated (old, 'O'). Six patients with epilepsy completed the same task during iEEG recordings. Blood-oxygen level dependent (BOLD) responses for N vs. O words were examined across the cortical surface and within regions of interest. MEG waveforms for N vs. O words were estimated using a noise-normalized minimum norm solution, and used to interpret the timecourse of fMRI. Spatial concordance was observed between fMRI and MEG repetition effects from 350 to 450 ms within bilateral occipitotemporal and medial temporal, left prefrontal, and left posterior temporal cortex. Additionally, MEG revealed widespread sources within left temporoparietal regions, whereas fMRI revealed bilateral reductions in occipitotemporal and left superior frontal, and increases in inferior parietal, precuneus, and dorsolateral prefrontal activity. BOLD suppression in left posterior temporal, left inferior prefrontal, and right occipitotemporal cortex correlated with MEG repetition-related reductions. IEEG responses from all three regions supported the timecourse of MEG and localization of fMRI. Furthermore, iEEG decreases to repeated words were associated with decreased gamma power in several regions, providing evidence that gamma oscillations are tightly coupled to cognitive phenomena and reflect regional activations seen in the BOLD signal.

Figure 1

Cluster-thresholded t-stat maps of the fMRI N > O (red/yellow) and O > N (cyan/blue) contrasts (left panel) and the MEG N vs O difference waveform for four time windows (right panel). Activity clusters are shown on the lateral and ventral inflated surfaces of both hemispheres (gyri = light gray; sulci = dark gray). Significance values range from a p<.001 to p <.00001 and represent significant clusters of activity exceeding a t-stat and size threshold.

Figure 2

fMRI cluster-thresholded t-stat maps of the N > O and O < N contrasts with MEG waveforms extracted from each significant fMRI cluster. MEG waveforms are shown from 0–600ms for new words (red) and old words (blue) within each ROI. Significance (*) denotes regions producing a condition x time interaction. Y-axis values reflect noise-normalized dipole strengths and can be conceptualized as estimates of the average signal-to-noise within an ROI.

Figure 3

Example ERPs from iEEG recordings in patients with intractable epilepsy. The y-axis represents the amplitudes (μV) of the N vs O words, scaled individually for each patient. Shaded areas reflect time windows during which N vs O words showed significantly different temporal clusters in the ERPs using randomization statistics. OCT = occipitotemporal.

Figure 4

Gamma power waves (integrated from 70–190 Hz) from iEEG recordings in patients with intractable epilepsy. The y-axis represents gamma power and is scaled for each plot to optimize visibility of the response. Shaded areas reflect time windows during which N vs O words showed significantly different temporal clusters in high gamma power using randomization statistics. OCT = occipitotemporal; DLPF = dorsolateral prefrontal; VLPF = ventrolateral prefrontal.