Neuronal Mechanisms of Repetition Priming in Occipitotemporal Cortex: Spatiotemporal Evidence from Functional Magnetic Resonance Imaging and Electroencephalography

Abstract

Repeated stimulus presentation (priming) is generally associated with a reduction in neuronal firing, macroscopically mirrored by a decrease in oscillatory electrophysiological markers as well as reduced hemodynamic responses. However, these repetition effects seem to be dependent on stimulus familiarity. We investigate the spatiotemporal correlates of repetition priming in cortical word-recognition networks and their modulation by stimulus familiarity (i.e., words vs pseudowords). Event-related functional magnetic resonance imaging results show reduced activation for repeated words in occipitotemporal cortical regions. Electroencephalogram recordings reveal a significant reduction of induced gamma-band responses (GBRs) between 200 and 350 ms after stimulus onset, accompanied by a decrease in phase synchrony between electrode positions. Pseudoword repetition, in contrast, leads to an activation increase in the same areas, to increased GBRs, and to an increased phase coupling. This spatiotemporal repetition by stimulus type interaction suggests that qualitatively distinct mechanisms are recruited during repetition priming of familiar and unfamiliar stimuli. Repetition of familiar stimuli leads to a "sharpening" of extrastriate object representations, whereas the repetition of unfamiliar stimuli results in the "formation" of a novel cortical network by means of synchronized oscillatory activity. In addition to isolating these mechanisms, the present study provides the first evidence for a possible link between induced electrophysiological and hemodynamic measures of brain activity.

Global familiarity of visual stimuli affects repetition-related neural plasticity but not repetition priming

“…It can be difficult; therefore, to interpret the absence of correlations between neural repetition effects, as measured by fMRI, and behavioral priming effects. For future studies on this topic, it would be fruitful to perform parallel or simultaneous fMRI and electrophysiological studies (i.e, EEG, ERP, MEG), which have a high temporal resolution (e.g., Fiebach et al, 2005).In conclusion, this study showed that repetition priming of globally familiar and unfamiliar visual objects produces qualitatively different brain patterns of repetition effects. The data are consistent with the view that behavioral priming effects may reflect facilitation at multiple stages along the processing pathway between stimulus and response, including perceptual, semantic, decision, and motor processes.…”

“…Thus, those studies reporting RS for both familiar and unfamiliar stimuli within the same task (van Turennout et al, 2000;Vuilleumier et al, 2002) have found that RS for unfamiliar objects was confined to more posterior regions of occipitaltemporal cortex, whereas RS for familiar stimuli encompassed both posterior and anterior of occipital-temporal regions as well as inferior frontal regions. Similarly, in the context of repetition priming tasks, RE in occipital-temporal regions for unfamiliar stimuli has been reported in very few and relatively small loci, including the anterior fusiform gyrus (Fiebach et al, 2005;Henson et al, 2000;Schacter et al, 1995;Thiel et al, 2002). In addition, Fiebach et al (2005) showed that within the same task, familiar stimuli (words) elicited RS in large areas of occipital-temporal cortex, as well as in frontal and parietal regions, whereas unfamiliar stimuli (pseudowords) produced RE in only a subset of occipital-temporal areas.…”

“…Similarly, in the context of repetition priming tasks, RE in occipital-temporal regions for unfamiliar stimuli has been reported in very few and relatively small loci, including the anterior fusiform gyrus (Fiebach et al, 2005;Henson et al, 2000;Schacter et al, 1995;Thiel et al, 2002). In addition, Fiebach et al (2005) showed that within the same task, familiar stimuli (words) elicited RS in large areas of occipital-temporal cortex, as well as in frontal and parietal regions, whereas unfamiliar stimuli (pseudowords) produced RE in only a subset of occipital-temporal areas.…”

“…Similarly, in the context of repetition priming tasks, RE in occipital-temporal regions for unfamiliar stimuli has been reported in very few and relatively small loci, including the anterior fusiform gyrus (Fiebach et al, 2005;Henson et al, 2000;Schacter et al, 1995;Thiel et al, 2002). In addition, Fiebach et al (2005) showed that within the same task, familiar stimuli (words) elicited RS in large areas of occipital-temporal cortex, as well as in frontal and parietal regions, whereas unfamiliar stimuli (pseudowords) produced RE in only a subset of occipital-temporal areas.In order to integrate these findings into a coherent framework, Henson (2000Henson ( , 2003 proposed in his component process model of priming that "repetition suppression occurs whenever the same process is performed on prime [the first presentation of a stimulus] and target [a repeated stimulus], whereas repetition enhancement occurs whenever priming causes a new process to occur on the target that did not occur on the prime" (Henson, 2003, pg. 71).…”

“…Other studies examining repetition priming of unfamiliar stimuli have reported increases in neural activity, or repetition enhancement (RE), in occipital-temporal cortex for repeated stimuli, including unfamiliar faces (Henson, Shallice, & Dolan, 2000;Thiel, Henson, & Dolan, 2002), meaningless symbols (Henson et al, 2000), line drawings of novel 3D objects (Schacter et al, 1995), and pseudowords (Fiebach, Gruber, & Supp, 2005). At least two of these studies (Fiebach et al, 2005;Schacter et al, 1995) only found RE and no RS in occipital-temporal Henson et al (2000) and Thiel et al (2002) did not report whether there were any regions that showed RS for the unfamiliar stimuli.Interestingly, both those studies finding RS and those finding RE for unfamiliar stimuli have reported fewer locations of significant neural repetition effects (either RS or RE) for unfamiliar stimuli compared to familiar ones. Thus, those studies reporting RS for both familiar and unfamiliar stimuli within the same task (van Turennout et al, 2000;Vuilleumier et al, 2002) have found that RS for unfamiliar objects was confined to more posterior regions of occipitaltemporal cortex, whereas RS for familiar stimuli encompassed both posterior and anterior of occipital-temporal regions as well as inferior frontal regions.…”