Elsevier

NeuroImage

Volume 53, Issue 2, 1 November 2010, Pages 707-717
NeuroImage

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

https://doi.org/10.1016/j.neuroimage.2010.06.069Get rights and content

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.

Research Highlights

► MEG, FMRI, and iEEG recordings can unveil the timing, location, and spectral features of repetition priming effects. ► BOLD suppression in left perisylvian regions shows strong spatial concordance to MEG N400 reductions. ► Gamma oscillations seen in iEEG recordings reflect regional activations in the BOLD signal.

Introduction

Repetition priming has been studied extensively in cognitive neuroscience, but its exact neural correlates remain poorly understood. fMRI studies have demonstrated response suppression, the main neural correlate of priming, in a number of cortical regions following word repetitions. Reliable decreases in blood-oxygen level dependent (BOLD) responses are consistently reported in left ventral occipitotemporal, posterior temporal, and left inferior frontal cortex—regions implicated in word form identification (Allison et al., 1999), lexical access, and semantic processing (Marinkovic et al., 2003, Matsumoto et al., 2005). Repetition of words also has been associated with increased activity in bilateral precuneus, frontoparietal, and hippocampal cortex—regions implicated in resting state and episodic retrieval processes (Weiss et al., 2009). What is not clear from fMRI is precisely when repetition effects occur during the course of word processing.

Unlike fMRI, MEG provides a highly accurate picture of the temporal dynamics of cognitive processes, allowing one to visualize repetition effects in real time. MEG studies of priming have revealed reductions in the N400 response—an event-related field (ERF) implicated in semantic processing—to repeated words from ~ 350 to 450 ms following word presentation. MEG N400 reductions have been reported in previous studies in similar regions to those identified with fMRI (Marinkovic et al., 2003). In addition, MEG studies have generally revealed priming effects that are more widespread in temporoparietal regions, often extending into the anterior temporal pole—a region not always captured with fMRI due to signal loss (Devlin et al., 2000).

However, neuroimaging methods such as fMRI and MEG rely on noninvasively recorded responses, which cannot provide unequivocal evidence of local neuronal generators. In addition, it has been suggested that some discrepancies between fMRI and MEG patterns may stem from the fact that that the BOLD signal is closely coupled with power changes in high gamma activity (Lachaux et al., 2007)—a frequency range not always detected at the scalp due to the low amplitude characteristic of gamma waveforms (Dalal et al., 2009), contamination with EMG artifact (Whitham et al., 2008) and microsaccades (Yuval-Greenberg et al., 2008). Increased gamma oscillations have been associated with a number of cognitive processes, including language and memory (Lachaux et al., 2007, Sederberg et al., 2007). Therefore, understanding their local generation may further enhance knowledge of word priming effects. Intracranial electroencephalography (iEEG) is the only current method capable of localizing such sources unambiguously and providing validation of the temporal, spatial, and spectral features of the fMRI and MEG repetition priming effects (Halgren, 2004b).

The goal of this study was to utilize sophisticated multimodal imaging to evaluate the spatiotemporal dynamics of repetition priming. We leveraged the high temporal resolution of MEG and iEEG to examine the time course of regional fMRI activations. In addition, we explored the regions and time windows during which the electromagnetic and hemodynamic priming effects showed the strongest correlation across participants. IEEG recordings were evaluated in regions that showed strong MEG and/or fMRI repetition effects, and the spatiotemporal and spectral features of iEEG responses were analyzed. We hypothesized that fMRI and MEG would show repetition priming effects in left inferior frontal, ventral occipitotemporal, and superior temporal cortex. We predicted that the regions associated with response suppression in fMRI would show strong correlations with reductions in MEG sources between ~ 350 and 450 ms—capturing peak N400 effects. We predicted that iEEG recordings would support previous studies demonstrating local generators of the N400 in multiple perisylvian regions (Halgren, 2004a), and that N400 iEEG responses would be particularly evident in the high gamma range.

Section snippets

Participants

Twelve right-handed, healthy controls between the ages of 19 and 36 (six males) and six patients undergoing invasive inpatient monitoring at the New York University (NYU) Comprehensive Epilepsy Center for treatment of drug-resistant epilepsy participated in the study. The study was approved by the Institutional Review Board at NYU and each subject's consent was obtained in accordance with the ethical standards promulgated in the Declaration of Helsinki. Handedness in all control participants

MRI acquisition

MRI data were acquired using a 3 T Siemens Allegra head-only MRI scanner (TE = 3.25 ms, TR = 2530 ms, TI = 1100 ms, flip angle = 7°, FOV = 256 mm, matrix = 256 × 256 × 171, slice thickness = 1.3 mm). Two T1-weighted images were acquired, rigid body registered to each other, and reoriented into a common space, roughly similar to alignment based on the AC–PC line. Images were corrected for non-linear warping caused by non-uniform fields created by the gradient coils. Image intensities were further normalized and made

Results

Fig. 1 displays cluster-based t-stat surface maps of the N > O (red-yellow) and O > N (blue-cyan) contrasts for fMRI (left panel) and the N vs. O difference waveform (red-yellow) for MEG time windows of interest (right panel). Fig. 2 portrays the same fMRI cluster maps, with MEG timecourses extracted from significant ROIs identified on the fMRI surfaces.

Discussion

Using advanced multimodal imaging, we demonstrate spatial concordance between fMRI and MEG N400 priming effects within left inferior prefrontal extending into precentral, left posterior superior temporal, left medial temporal, right lateral occipitotemporal, and bilateral ventral occipitotemporal cortex, encompassing much of the lingual and fusiform cortex on the left. We also provide iEEG validation of our MEG/fMRI responses in key regions in multiple patients and reveal co-localization

Acknowledgments

The work was supported by National Institutes of Health (NIH) Grant K23NS056091 (C.R.M) and NS18741 (E.H.).

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