Repetition Suppression Effects Research Articles

Dissociation of part-based and integrated neural responses to faces by means of electroencephalographic frequency tagging.

In order to isolate the repetition suppression effects for each part of a whole-face stimulus, the left and right halves of face stimuli were flickered at different frequency rates (5.88 or 7.14 Hz), changing or not changing identity at every stimulation cycle. The human electrophysiological (electroencephalographic) responses to each face half increased in amplitude when different rather than repeated face half identities were presented at every stimulation cycle. Contrary to the repetition suppression effects for whole faces, which are usually found over the right occipito-temporal cortex, these part-based repetition suppression effects were found on all posterior electrode sites and were unchanged when the two face halves were manipulated by separation, lateral misalignment, or inversion. In contrast, intermodulation components (e.g. 7.14-5.88 = 1.26 Hz) were found mainly over the right occipito-temporal cortex and were significantly reduced following the aforementioned manipulations. In addition, the intermodulation components decreased substantially for face halves belonging to different identities, which form a less coherent face than when they belong to the same face identity. These observations provide objective evidence for dissociation between part-based and integrated (i.e. holistic/configural) responses to faces in the human brain, suggesting that only responses to integrated face parts reflect high-level, possibly face-specific, representations.

Intracerebral electrical stimulation of a face-selective area in the right inferior occipital cortex impairs individual face discrimination

During intracerebral stimulation of the right inferior occipital cortex, a patient with refractory epilepsy was transiently impaired at discriminating two simultaneously presented photographs of unfamiliar faces. The critical electrode contact was located in the most posterior face-selective brain area of the human brain (right “occipital face area”, rOFA) as shown both by low- (ERP) and high-frequency (gamma) electrophysiological responses as well as a face localizer in fMRI. At this electrode contact, periodic visual presentation of 6 different faces by second evoked a larger electrophysiological periodic response at 6Hz than when the same face identity was repeated at the same rate. This intracerebral EEG repetition suppression effect was markedly reduced when face stimuli were presented upside-down, a manipulation that impairs individual face discrimination. These findings provide original evidence for a causal relationship between the face-selective right inferior occipital cortex and individual face discrimination, independently of long-term memory representations. More generally, they support the functional value of electrophysiological repetition suppression effects, indicating that these effects can be used as an index of a necessary neural representation of the changing stimulus property.

Hippocampal control of repetition effects for associative stimuli.

Recent findings suggest that repetition effects interact with episodic memory processes that are putatively supported by the hippocampus. Thus, the formation or refinement of episodic memories may be related to a modulating signal from the hippocampus to the neocortex which leads to sparser or more extended stimulus representations (repetition suppression or enhancement), depending on the type of stimulus and the brain site. This framework suggests that hippocampal activity during the initial presentation of a stimulus correlates with the magnitude of repetition effects. Here, we tested this hypothesis in an fMRI study in which associations between faces and buildings were presented twice. BOLD responses showed repetition suppression in fusiform face area (FFA) and parahippocampal place area (PPA), most likely due to a refinement of existing category representations. Hippocampal activity during the first presentations was correlated with the amount of repetition suppression, in particular in the FFA. Repetition enhancement effects were observed on BOLD responses in posterior parietal cortex, possibly related to the formation of new representations of associative stimuli. The magnitude of parietal BOLD repetition effects depended on successful memory formation. These findings suggest that both repetition enhancement and repetition suppression effects are influenced by a modulating signal from the hippocampus.

Neural repetition suppression: evidence for perceptual expectation in object-selective regions.

It is an established finding that neuronal activity is decreased for repeated stimuli. Recent studies revealed that repetition suppression (RS) effects are altered by manipulating the probability with which stimuli are repeated. RS for faces is more pronounced when the probability of repetition is high than when it is low. This response pattern is interpreted with reference to the predictive coding (PC) account, which assumes that RS is influenced by top-down expectations. Recent findings challenge the generality of PC accounts of RS by showing repetition probability does not modulate RS for other visual stimuli than faces. However, a number of findings on visual processing are in line with PC. Thus, the influence of repetition probability on RS effects during object processing requires careful reinvestigations. In the present fMRI study, object pictures were presented in a high (75%) or low (25%) repetition probability context. We found increased RS in the high-probability context compared to the low-probability context in the left lateral occipital complex (LOC). The dorsal-caudal and the ventral-anterior subdivisions of the LOC revealed similar neuronal responses. These results indicate that repetition probability effects can be found for other visual objects than faces and provide evidence in favor of the PC account.

A little more conversation – the influence of communicative context on syntactic priming in brain and behavior

We report on an functional magnetic resonance imaging (fMRI) syntactic priming experiment in which we measure brain activity for participants who communicate with another participant outside the scanner. We investigated whether syntactic processing during overt language production and comprehension is influenced by having a (shared) goal to communicate. Although theory suggests this is true, the nature of this influence remains unclear. Two hypotheses are tested: (i) syntactic priming effects (fMRI and behavioral) are stronger for participants in the communicative context than for participants doing the same experiment in a non-communicative context, and (ii) syntactic priming magnitude (behavioral) is correlated with the syntactic priming magnitude of the speaker’s communicative partner. Results showed that across conditions, participants were faster to produce sentences with repeated syntax, relative to novel syntax. This behavioral result converged with the fMRI data: we found repetition suppression effects in the left insula extending into left inferior frontal gyrus (BA 47/45), left middle temporal gyrus (BA 21), left inferior parietal cortex (BA 40), left precentral gyrus (BA 6), bilateral precuneus (BA 7), bilateral supplementary motor cortex (BA 32/8), and right insula (BA 47). We did not find support for the first hypothesis: having a communicative intention does not increase the magnitude of syntactic priming effects (either in the brain or in behavior) per se. We did find support for the second hypothesis: if speaker A is strongly/weakly primed by speaker B, then speaker B is primed by speaker A to a similar extent. We conclude that syntactic processing is influenced by being in a communicative context, and that the nature of this influence is bi-directional: speakers are influenced by each other.

Gamma oscillations distinguish mere exposure from other likability effects

Repeated exposure to neutral stimuli enhances liking for those, which is called mere exposure effect (MEE) (Zajonc, 1968). Its behavioral effects have been extensively investigated. However, the mechanism by which it is generated remains unclear. To elucidate the neural mechanism of the MEE, we recorded electroencephalograms while subjects indicated their preferences for face stimuli with and without MEE induction. According to behavioral data, participants were divided into two groups, one with, and one without MEE tendency. In participants with an MEE tendency, gamma activity (40–60 [Hz]) in the parieto-occipital area was significantly weaker for exposed faces than unexposed ones, indicating a repetition-suppression effect. Gamma activity from sites exhibiting peak repetition-suppression effects was significantly weaker in theoretically genuine MEE trials than non-MEE trials, indicating that emotion processing might influence the MEE. These results suggest that existing theories regarding mechanisms underlying the MEE, namely, fluency misattribution and apprehensiveness reduction might not be mutually exclusive. Moreover, gamma activity might be a potential indicator to distinguish the MEE from other likability effects, at least in the case of human face stimuli.

Temporal frequency tuning of cortical face-sensitive areas for individual face perception

In a highly dynamic visual environment the human brain needs to rapidly differentiate complex visual patterns, such as faces. Here, we defined the temporal frequency tuning of cortical face-sensitive areas for face discrimination. Six observers were tested with functional magnetic resonance imaging (fMRI) when the same or different faces were presented in blocks at 11 frequency rates (ranging from 1 to 12Hz). We observed a larger fMRI response for different than same faces – the repetition suppression/adaptation effect – across all stimulation frequency rates. Most importantly, the magnitude of the repetition suppression effect showed a typical Gaussian-shaped tuning function, peaking on average at 6Hz for all face-sensitive areas of the ventral occipito-temporal cortex, including the fusiform and occipital “face areas” (FFA and OFA), as well as the superior temporal sulcus. This effect was due both to a maximal response to different faces in a range of 3 to 6Hz and to a sharp drop of the blood oxygen level dependent (BOLD) signal from 6Hz onward when the same face was repeated during a block. These observations complement recent scalp EEG observations (Alonso-Prieto et al., 2013), indicating that the cortical face network can discriminate each individual face when these successive faces are presented every 160–170ms. They also suggest that a relatively fast 6Hz rate may be needed to isolate the contribution of high-level face perception processes during behavioral discrimination tasks. Finally, these findings carry important practical implications, allowing investigators to optimize the stimulation frequency rates for observing the largest repetition suppression effects to faces and other visual forms in the occipito-temporal cortex.

Pharmacological Dissociation of Novelty Responses in the Human Brain

Repeated processing of the same information is associated with decreased neuronal responses, termed repetition suppression (RS). Although RS effects (i.e., the difference in activity between novel and repeated stimuli) have been demonstrated within several brain regions, such as the medial temporal lobe, their precise neural mechanisms still remain unclear. Here, we used functional magnetic resonance imaging together with psychopharmacology in 48 healthy human subjects, demonstrating that RS effects within the mesolimbic system are differentially modulated by cholinergic and dopaminergic stimulation. The dopamine precursor levodopa (100 mg) attenuated RS within the hippocampus, parahippocampal cortex, and substantia nigra/ventral tegmental area, and the degree of this reduction correlated with recognition memory performance 24 h later. The acetylcholinesterase inhibitor galantamine (8 mg), in contrast, reversed RS into repetition enhancement, showing no relationship to subsequent recognition memory. This suggests that novelty sensitive neural populations of the mesolimbic system can dynamically shift their responses depending on the balance of cholinergic and dopaminergic neurotransmission, and these shifts can influence memory retention.

Epoch-specific functional networks involved in working memory

Working memory (WM) is not a unitary construct. There are distinct processes involved in encoding information, maintaining it on-line, and using it to guide responses. The anatomical configurations of these processes are more accurately analyzed as functionally connected networks than collections of individual regions. In the current study we analyzed event-related functional magnetic resonance imaging (fMRI) data from a Sternberg Item Recognition Paradigm WM task using a multivariate analysis method that allowed the linking of functional networks to temporally-separated WM epochs. The length of the delay epochs was varied to optimize isolation of the hemodynamic response (HDR) for each task epoch. All extracted functional networks displayed statistically significant sensitivity to delay length. Novel information extracted from these networks that was not apparent in the univariate analysis of these data included involvement of the hippocampus in encoding/probe, and decreases in BOLD signal in the superior temporal gyrus (STG), along with default-mode regions, during encoding/delay. The bilateral hippocampal activity during encoding/delay fits with theoretical models of WM in which memoranda held across the short term are activated long-term memory representations. The BOLD signal decreases in the STG were unexpected, and may reflect repetition suppression effects invoked by internal repetition of letter stimuli. Thus, analysis methods focusing on how network dynamics relate to experimental conditions allowed extraction of novel information not apparent in univariate analyses, and are particularly recommended for WM experiments for which task epochs cannot be randomized.

The Repetition Paradigm: Enhancement of novel metaphors and suppression of conventional metaphors in the left inferior parietal lobe

The neural mechanisms underlying the process of understanding novel and conventional metaphoric expressions remain unclear largely because the specific brain regions that support the formation of novel semantic relations are still unknown. A well established way to study distinct cognitive processes specifically associated with an event of interest is to repeatedly present the same stimulus. The aim of the current study is to examine the neural signatures associated with forming new metaphoric concepts by repeatedly presenting novel as well as conventional metaphors. In an fMRI study, 11 subjects read novel and conventional two-word metaphoric expressions and decided whether the expressions were meaningful. Prior to the study, participants were presented with half of the conventional metaphors and half of the novel metaphoric expressions. The present results revealed that whereas repeated exposure to conventional metaphors elicited repetition suppression within the left supramarginal gyrus, no brain areas showed repetition suppression effects during the repeated exposure of novel metaphors. However, repetition enhancement effects for novel metaphors were found in several brain areas including the bilateral inferior parietal gyri. These findings suggest that the left and right supramarginal gyri are both involved in the conceptualization and the storage of novel semantic relations. This study is important to develop theoretical accounts of the formation of conceptual knowledge for both familiar and novel information.

Different neural mechanisms within occipitotemporal cortex underlie repetition suppression across same and different-size faces.

Repetition suppression (RS) (or functional magnetic resonance imaging adaptation) refers to the reduction in blood oxygen level–dependent signal following repeated presentation of a stimulus. RS is frequently used to investigate the role of face-selective regions in human visual cortex and is commonly thought to be a “localized” effect, reflecting fatigue of a neuronal population representing a given stimulus. In contrast, predictive coding theories characterize RS as a consequence of “top-down” changes in between-region modulation. Differentiating between these accounts is crucial for the correct interpretation of RS effects in the face-processing network. Here, dynamic causal modeling revealed that different mechanisms underlie different forms of RS to faces in occipitotemporal cortex. For both familiar and unfamiliar faces, repetition of identical face images (same size) was associated with changes in “forward” connectivity between the occipital face area (OFA) and the fusiform face area (FFA) (OFA-to-FFA). In contrast, RS across image size was characterized by altered “backward” connectivity (FFA-to-OFA). In addition, evidence was higher for models in which information projected directly into both OFA and FFA, challenging the role of OFA as the input stage of the face-processing network. These findings suggest “size-invariant” RS to faces is a consequence of interactions between regions rather than being a localized effect.

Dissociable roles of human inferior frontal gyrus during action execution and observation

There has been recent controversy about whether activation in the human inferior frontal gyrus (IFG) and Brodmann Area (BA) 6 when observing actions indicates operation of mirror neurons. Recent functional magnetic resonance imaging (fMRI) data have demonstrated repetition suppression (RS) effects in posterior IFG which are consistent with the presence of mirror neurons in humans. Here we investigated whether there were similar RS effects elsewhere in the IFG and BA6, or whether, instead, activation in other locations may signal operation of alternative mechanisms. Replicating previous findings, we found RS effects in posterior IFG consistent with the operation of mirror neurons. However, these effects were not found in other locations in IFG and BA6. Additionally, activation patterns in anterior regions of IFG suggested dissociable operations when observing and executing actions. Therefore, caution should be exercised when claiming that activations in many locations during action observation indicate the operation of mirror neurons. Activation may instead reflect alternative mechanisms, such as encoding of the semantic features of actions.

Oscillatory MEG gamma band activity dissociates perceptual and conceptual aspects of visual object processing: A combined repetition/conceptual priming study

We used a combined repetition/conceptual priming task to investigate attenuations of induced gamma-band activity (iGBA) due to prior experience. We hypothesized that distinguishable iGBA suppression effects can be related to the processing of (a) perceptual aspects, and (b) conceptual aspects of cortical object representations. Participants were asked to perform a semantic classification task with pictures of real world objects and their semantically corresponding words, using a design that isolated distinct levels of the neural suppression effect. By means of volumetric source analysis we located stimulus domain-specific iGBA repetition suppression effects (60-90 Hz) in temporal, parietal, and occipital areas of the human cortex. In contrast, domain-unspecific iGBA repetition suppression, corresponding to conceptual priming, was restricted to left temporal brain regions. We propose that the selective involvement of left temporal areas points to the activation of conceptual representations, whereas more posterior temporal, parietal, and occipital areas probably reflect perceptual aspects of higher-order visual object processing.

The Role of Perceptual Expectation on Repetition Suppression: A Quest to Dissect the Differential Contribution of Probability of Occurrence and Event Predictability

The Role of Perceptual Expectation on Repetition Suppression: A Quest to Dissect the Differential Contribution of Probability of Occurrence and Event Predictability

Phonological repetition-suppression in bilateral superior temporal sulci

Evidence has accumulated that posterior superior temporal sulcus (STS) is critically involved in phonological processing during speech perception, although there are conflicting accounts regarding the degree of lateralization. The current fMRI experiment aimed to identify phonological processing during speech perception through repetition-suppression effects. Repetition-suppression occurs when brain activity decreases from repetitive presentation of stimulus characteristics, in regions of cortex that process those characteristics. We manipulated the degree of phonological repetition among words in short lists to obtain systematic decreases in brain response, indicative of phonological processing. The fMRI experiment presented seventeen participants with recorded wordlists, of low, medium, or high phonological repetition, defined by how many phonemes were shared among words. Bilaterally, middle STS demonstrated activity differences consistent with our prediction of repetition-suppression, as responses decreased systematically with each increase in phonological repetition. Phonological repetition-suppression in bilateral STS converges with neuroimaging evidence for phonological processing, and word deafness resulting from bilateral superior temporal lesions.

Syntactic priming in German–English bilinguals during sentence comprehension

A longstanding question in bilingualism is whether syntactic information is shared between the two language processing systems. We used an fMRI repetition suppression paradigm to investigate syntactic priming in reading comprehension in German–English late-acquisition bilinguals. In comparison to conventional subtraction analyses in bilingual experiments, repetition suppression has the advantage of being able to detect neuronal populations that are sensitive to properties that are shared by consecutive stimuli. In this study, we manipulated the syntactic structure between prime and target sentences. A sentence with a passive sentence structure in English was preceded either by a passive or by an active sentence in English or German. We looked for repetition suppression effects in left inferior frontal, left precentral and left middle temporal regions of interest. These regions were defined by a contrast of all non-target sentences in German and English versus the baseline of sentence-format consonant strings. We found decreases in activity (repetition suppression effects) in these regions of interest following the repetition of syntactic structure from the first to the second language and within the second language.Moreover, a separate behavioural experiment using a word-by-word reading paradigm similar to the fMRI experiment showed faster reading times for primed compared to unprimed English target sentences regardless of whether they were preceded by an English or a German sentence of the same structure.We conclude that there is interaction between the language processing systems and that at least some syntactic information is shared between a bilingual's languages with similar syntactic structures.

Movement-Specific Repetition Suppression in Ventral and Dorsal Premotor Cortex during Action Observation

There are several models of premotor cortex contributions to sensorimotor behavior. For instance, the ventral premotor cortex (PMv) appears to be involved in processing visuospatial object properties for grasping, whereas the dorsal premotor cortex (PMd) is involved in using arbitrary rules to guide advance motor planning. These models have focused on individual movements. Here, we examine the premotor responses evoked during the processing of individual movements functionally embedded in an action. We tested whether processing hand–object interactions and action end states would differentially engage PMv and PMd. We used a repetition suppression (RS)–functional magnetic resonance imaging paradigm in which we independently manipulated the observed grip, the end position of the object (independent of its spatial location), and the hand trajectory. By comparing novel and repeated trials for each of these action components, we could isolate RS effects specific to each of them. Repeating the grasp component attenuated activity in right PMv, whereas repeating the end state of the action reduced blood oxygen level–dependent activity in the left PMd. These results suggest that PMv is involved in controlling the kinematic means of an appropriate hand–object interaction, whereas PMd is focused on specifying the desired end state of an action.

Repetition suppression for performed hand gestures revealed by fMRI

The functional components of the human motor system that are used to retrieve and execute simple intransitive hand gestures were identified with a repetition suppression (RS) paradigm. Participants performed movements with the right hand to text instructions in a rapid event related design with a pseudo-random stimulus order. Brain areas associated with action retrieval were identified by comparing trials where an action was repeated to trials that involved a new action. Performance of a novel action, collapsed across individual actions, resulted in significantly greater activity in a left hemisphere predominant fronto-parietal circuit involving inferior frontal gyrus and inferior parietal cortex (supramarginal gyrus). This is consistent with previous action retrieval tasks using go, no-go paradigms and lesion studies of patients with apraxia that emphasize a role of these areas in action organization. In addition, RS effects were present in left primary sensorimotor cortex. These effects cannot be ascribed to kinematic differences, simple action related activity or differences of cognitive set. Significant RS effects for action retrieval could be identified with as little as 5 min of fMRI data and underscores the potential of using RS to characterize representational structure within the motor system.

Repetition suppression and reactivation in auditory-verbal short-term recognition memory.

The neural response to stimulus repetition is not uniform across brain regions, stimulus modalities, or task contexts. For instance, it has been observed in many functional magnetic resonance imaging (fMRI) studies that sometimes stimulus repetition leads to a relative reduction in neural activity (repetition suppression), whereas in other cases repetition results in a relative increase in activity (repetition enhancement). In the present study, we hypothesized that in the context of a verbal short-term recognition memory task, repetition-related “increases” should be observed in the same posterior temporal regions that have been previously associated with “persistent activity” in working memory rehearsal paradigms. We used fMRI and a continuous recognition memory paradigm with short lags to examine repetition effects in the posterior and anterior regions of the superior temporal cortex. Results showed that, consistent with our hypothesis, the 2 posterior temporal regions consistently associated with working memory maintenance, also show repetition increases during short-term recognition memory. In contrast, a region in the anterior superior temporal lobe showed repetition suppression effects, consistent with previous research work on perceptual adaptation in the auditory–verbal domain. We interpret these results in light of recent theories of the functional specialization along the anterior and posterior axes of the superior temporal lobe.

Gamma Band Synchronization and the Formation of Representations in Visual Word Processing: Evidence from Repetition and Homophone Priming

The formation of an object's cortical representation seems to rely on synchronized neuronal activity within the gamma band frequency range (gamma band activity [GBA]). In this study, we investigated whether electroencephalogram (EEG) GBA, and its phase synchronization between electrodes, is necessary for the formation of nonobject higher-order cognitive representations, using both repetition and homophone priming tasks. In a repetition priming task, the formation of orthographic, phonological, and semantic representations is promoted by a prime word, whereas in the homophone priming task, the formation of only phonological representations is promoted. In the present study, the lexical processing of a target word induced GBA. In the repetition priming task, induced GBA and phase synchronization were decreased by presentation of the prime word (i.e., a repetition suppression effect) within both 200-300 msec and 400-500 msec time windows. In the homophone priming task, the repetition suppression effect was observed only within the 400-500 msec time window. The fact that repetition suppression effects were found in both priming tasks indicates that GBA and phase synchronization are necessary for the formation of phonological and semantic representations of a word. These results also suggest that formation of orthographic and higher-order cognitive representations occurred over different time courses.