Showed Repetition Suppression Research Articles

Attention is required for canonical brain signature of prediction error despite early encoding of the stimuli.

Prediction error is a basic component of predictive-coding theory of brain processing. According to the theory, each stage of brain processing of sensory information generates a model of the current sensory input; subsequent input is compared against the model and only if there is a mismatch, a prediction error, is further processing performed. Recently, Smout and colleagues found that a signature of prediction error, the visual (v) mismatch negativity (MMN), for a fundamental property of visual input-its orientation-was absent without endogenous attention on the stimuli. This is remarkable because the weight of evidence for MMNs from audition and vision is that they occur without endogenous attention. To resolve this discrepancy, we conducted an experiment addressing 2 alternative explanations for Smout and colleagues' finding: that it was from a lack of reproducibility or that participants' visual systems did not encode the stimuli when attention was on something else. We conducted a similar experiment to that of Smout and colleagues. We showed 21 participants sequences of identically oriented Gabor patches, standards, and, unpredictably, otherwise identical, Gabor patches differing in orientation by ±15°, ±30°, and ±60°, deviants. To test whether participants encoded the orientation of the standards, we varied the number of standards preceding a deviant, allowing us to search for a decrease in activity with the number of repetitions of standards-repetition suppression. We diverted participants' attention from the oriented stimuli with a central, letter-detection task. We reproduced Smout and colleagues' finding of no vMMN without endogenous attention, strengthening their finding. We found that our participants showed repetition suppression: They did encode the stimuli preattentively. We also found early processing of deviants. We discuss various explanations why the earlier processing did not extend into the vMMN time window, including low precision of prediction.

Face processing in the infant brain after pandemic lockdown.

The role of visual experience in the development of face processing has long been debated. We present a new angle on this question through a serendipitous study that cannot easily be repeated. Infants viewed short blocks of faces during fMRI in a repetition suppression task. The same identity was presented multiple times in half of the blocks (repeat condition) and different identities were presented once each in the other half (novel condition). In adults, the fusiform face area (FFA) tends to show greater neural activity for novel versus repeat blocks in such designs, suggesting that it can distinguish same versus different face identities. As part of an ongoing study, we collected data before the COVID-19 pandemic and after an initial local lockdown was lifted. The resulting sample of 12 infants (9-24 months) divided equally into pre- and post-lockdown groups with matching ages and data quantity/quality. The groups had strikingly different FFA responses: pre-lockdown infants showed repetition suppression (novel>repeat), whereas post-lockdown infants showed the opposite (repeat>novel), often referred to as repetition enhancement. These findings provide speculative evidence that altered visual experience during the lockdown, or other correlated environmental changes, may have affected face processing in the infant brain.

Adaptation in models of visual object recognition

Convolutional neural network (CNN) models of the ventral stream provide an unprecedented opportunity to relate neural mechanisms to sensory representations and even perception. Current CNNs lack the temporal dynamics of biological vision such as adaptation to previous stimulation. Perceptually, adaptation has been widely studied in the form of aftereffects (Webster, 2015), while in single neurons adaptation is often equated to repetition suppression (Vogels, 2016). Whereas the two are often thought to be associated, they remain to be integrated in a truly general framework. One proposed mechanism underlying repetition suppression is a reduced excitability depending on previous neural activity, called response fatigue. Here, we implemented fatigue in each unit of a CNN (Krizhevsky et al., 2012) and asked whether it could account for more complex phenomena of neural and visual adaptation. Specifically, we assigned a latent fatigue variable to each unit that increased after high, but decreased after lower activation. The activation of a unit was then obtained by subtracting its fatigue from its input activity (before the linear rectifier). The resulting CNN units showed repetition suppression matching neural adaptation on several hallmark properties: stimulus-specificity, increased adaptation in higher layers, adaptation degree proportional with the number of repetitions (Vinken et al., 2017), and decreased adaptation with longer interstimulus intervals (Sawamura et al., 2006). Furthermore, the response patterns could account for the perceptual effects we tested: from afterimages in the first layer to a face gender aftereffect in later layers (Webster et al., 2004). Thus, when considered in a CNN, a simple mechanism of response fatigue operating at the level of single neurons can account for complex adaptation effects. In addition to providing a general model for adaptation, these results demonstrate the strength of using deep neural networks to connect low-level canonical neural properties or computations to high-level neural and perceptual phenomena.

FMRI repetition suppression reveals no sensitivity to trait judgments from faces in face perception or theory-of-mind networks.

The human face cues a wealth of social information, but the neural mechanisms that underpin social attributions from faces are not well known. In the current fMRI experiment, we used repetition suppression to test the hypothesis that populations of neurons in face perception and theory-of-mind neural networks would show sensitivity to faces that cue distinct trait judgments. Although faces were accurately discriminated based on associated traits, our results showed no evidence that face or theory-of-mind networks showed repetition suppression for face traits. Thus, we do not provide evidence for population coding models of face perception that include sensitivity to high and low trait features. Due to aspects of the experimental design, which bolstered statistical power and sensitivity, we have reasonable confidence that we could detect effects of a moderate size, should they exist. The null findings reported here, therefore, add value to models of neural organisation in social perception by showing instances where effects are absent or small. To test the generalisability of our findings, future work should test different types of trait judgment and different types of facial stimuli, in order to further probe the neurobiological bases of impression formation based on facial appearance.

Brain regions that show repetition suppression and enhancement: A meta-analysis of 137 neuroimaging experiments.

Repetition suppression and enhancement refer to the reduction and increase in the neural responses for repeated rather than novel stimuli, respectively. This study provides a meta-analysis of the effects of repetition suppression and enhancement, restricting the data used to that involving fMRI/PET, visual stimulus presentation, and healthy participants. The major findings were as follows. First, the global topography of the repetition suppression effects was strikingly similar to that of the "subsequent memory" effects, indicating that the mechanism for repetition suppression is the reduced engagement of an encoding system. The lateral frontal cortex effects involved the frontoparietal control network regions anteriorly and the dorsal attention network regions posteriorly. The left fusiform cortex effects predominantly involved the dorsal attention network regions, whereas the right fusiform cortex effects mainly involved the visual network regions. Second, the category-specific meta-analyses and their comparisons indicated that most parts of the alleged category-specific regions showed repetition suppression for more than one stimulus category. In this regard, these regions may not be "dedicated cortical modules," but are more likely parts of multiple overlapping large-scale maps of simple features. Finally, the global topography of the repetition enhancement effects was similar to that of the "retrieval success" effects, suggesting that the mechanism for repetition enhancement is voluntary or involuntary explicit retrieval during an implicit memory task. Taken together, these results clarify the network affiliations of the regions showing reliable repetition suppression and enhancement effects and contribute to the theoretical interpretations of the local and global topography of these two effects. Hum Brain Mapp 38:1894-1913, 2017. © 2017 Wiley Periodicals, Inc.

Repetition suppression for visual actions in the macaque superior temporal sulcus

In many brain areas, repetition of a stimulus usually weakens the neural response. This "adaptation" or repetition suppression effect has been observed with mass potential measures such as event-related potentials (ERPs), in fMRI BOLD responses, and locally with local field potentials (LFPs) and spiking activity. Recently, it has been reported that macaque F5 mirror neurons do not show repetition suppression of their spiking activity for single repetitions of hand actions, which disagrees with human fMRI adaptation studies. This finding also contrasts with numerous studies showing repetition suppression in macaque inferior temporal cortex, including the rostral superior temporal sulcus (STS). Since the latter studies employed static stimuli, we assessed here whether the use of dynamic action stimuli abolishes repetition suppression in the awake macaque STS. To assess adaptation effects in the STS, we employed the same hand action movies as used when examining adaptation in F5. The upper bank STS neurons showed repetition suppression during the approaching phase of the hand action, which corresponded to the phase of the action for which these neurons responded overall the strongest. The repetition suppression was present for the spiking activity measured in independent single-unit and multiunit recordings as well as for the LFP power at frequencies > 50 Hz. Together with previous data in F5, these findings suggest that adaptation effects differ between F5 mirror neurons and the STS neurons.

A two-part preliminary investigation of encoding-related activation changes after moderate to severe traumatic brain injury: hyperactivation, repetition suppression, and the role of the prefrontal cortex.

Traumatic brain injury (TBI) survivors typically exhibit significant learning and memory deficits and also frequently demonstrate hyperactivation during functional magnetic resonance imaging (fMRI) tasks involving working memory encoding and maintenance. However, it remains unclear whether the hyperactivation observed during such working memory tasks is also present during long-term memory encoding. The preliminary experiments presented here were designed to examine this question. In Experiment 1, 7 healthy controls (HC) and 7 patients with moderate to severe TBI encoded ecologically relevant object location associations (OLA) while undergoing fMRI and then completed a memory test outside of the fMRI environment. fMRI data analysis included only the correctly encoded trials and revealed hyperactivation in the TBI relative to HC group in regions critical for OLA encoding, including bilateral dorsal and ventral visual processing areas, bilateral frontoparietal working memory network regions, and the left medial temporal lobe. There was also an incidental finding that this hyperactivation persisted after multiple exposures to the same stimulus, which may indicate an attenuated repetition suppression effect that could ultimately contribute to cognitive fatigue and inefficient memory encoding after TBI. Experiment 2 directly assessed repetition suppression in some of the same HC and TBI participants. During early encoding trials, the TBI group showed large areas of hyperactivation in the right prefrontal cortex and bilateral posterior parietal cortices relative to the HC. Following additional exposure to these stimuli, the TBI group showed repetition suppression in visual and spatial processing regions, but continued to show hyperactivation in the right dorsolateral prefrontal cortex. Findings from these preliminary studies may reflect that increased reliance on cognitive control mechanisms following TBI extends to memory encoding.

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.

Repetition suppression in macaque superior temporal sulcus (STS) for dynamic visual stimuli depicting hand actions.

Repetition suppression in macaque superior temporal sulcus (STS) for dynamic visual stimuli depicting hand actions.

Modeling activation and effective connectivity of VWFA in same script bilinguals.

Previous neuroimaging research revealed a small area in the inferior occipito-temporal cortex (VWFA), which seems to be involved in recognition of written words. The specialized response of the VWFA to words could result from repeated exposure to print in the course of functional fine-tuning of the brain. Research with bilingual speakers holds promise in helping to reveal response properties of the VWFA by assessing its sensitivity to language proficiency, word-form similarity, and meaning overlap across two languages. Using fMRI, we compared VWFA activity for cognate and homograph prime-target pairs in a group of fluent Spanish-English speakers. Cognates share form and meaning in two languages, while homographs only share form. Relative to baseline, the VWFA showed repetition suppression to pairs of homographs, but not to pairs of cognates, suggesting that this area is sensitive to word meaning. The different response to cognates and homographs was only observed when English was the prime language and Spanish was the target language. To help explain this result we compared patterns of effective connectivity between the VWFA and other parts of the reading network implicated in semantic and phonological processing. Our neural models showed that English targets engaged a direct ventral route from the VWFA to the frontal lobe and Spanish targets engaged an indirect dorsal route. Considering that frontal cortex has been implicated in semantic processing, a direct connection to this area could signal a fast and automatic access to meaning and would facilitate early semantic influences in visual word recognition.

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.

The Neural Correlates of Crowding-Induced Changes in Appearance

SummaryObject recognition in the peripheral visual field is limited by crowding: the disruptive influence of nearby clutter [1, 2]. Despite its severity, little is known about the cortical locus of crowding. Here, we examined the neural correlates of crowding by combining event-related fMRI adaptation with a change-detection paradigm [3]. Crowding can change the appearance of objects, such that items become perceptually matched to surrounding objects; we used this change in appearance as a signature of crowding and measured brain activity that correlated with the crowded percept. Observers adapted to a peripheral patch of noise surrounded by four Gabor flankers. When crowded, the noise appears oriented and perceptually indistinguishable from the flankers. Consequently, substitution of the noise for a Gabor identical to the flankers (“change-same”) is rarely detected, whereas substitution for an orthogonal Gabor (“change-different”) is rarely missed. We predicted that brain areas representing the crowded percept would show repetition suppression in change-same trials but release from adaptation in change-different trials. This predicted pattern was observed throughout cortical visual areas V1–V4, increasing in strength from early to late visual areas. These results depict crowding as a multistage process, involving even the earliest cortical visual areas, with perceptual consequences that are increasingly influenced by later visual areas.

From Reference to Sense: How the Brain Encodes Meaning for Speaking

In speaking, semantic encoding is the conversion of a non-verbal mental representation (the reference) into a semantic structure suitable for expression (the sense). In this fMRI study on sentence production we investigate how the speaking brain accomplishes this transition from non-verbal to verbal representations. In an overt picture description task, we manipulated repetition of sense (the semantic structure of the sentence) and reference (the described situation) separately. By investigating brain areas showing response adaptation to repetition of each of these sentence properties, we disentangle the neuronal infrastructure for these two components of semantic encoding. We also performed a control experiment with the same stimuli and design but without any linguistic task to identify areas involved in perception of the stimuli per se. The bilateral inferior parietal lobes were selectively sensitive to repetition of reference, while left inferior frontal gyrus showed selective suppression to repetition of sense. Strikingly, a widespread network of areas associated with language processing (left middle frontal gyrus, bilateral superior parietal lobes and bilateral posterior temporal gyri) all showed repetition suppression to both sense and reference processing. These areas are probably involved in mapping reference onto sense, the crucial step in semantic encoding. These results enable us to track the transition from non-verbal to verbal representations in our brains.

The Neural Correlates of Crowding-Induced Changes in Appearance

Summary Object recognition in the peripheral visual field is limited by crowding: the disruptive influence of nearby clutter [1, 2]. Despite its severity, little is known about the cortical locus of crowding. Here, we examined the neural correlates of crowding by combining event-related fMRI adaptation with a change-detection paradigm [3]. Crowding can change the appearance of objects, such that items become perceptually matched to surrounding objects; we used this change in appearance as a signature of crowding and measured brain activity that correlated with the crowded percept. Observers adapted to a peripheral patch of noise surrounded by four Gabor flankers. When crowded, the noise appears oriented and perceptually indistinguishable from the flankers. Consequently, substitution of the noise for a Gabor identical to the flankers (change-same) is rarely detected, whereas substitution for an orthogonal Gabor (change-different) is rarely missed. We predicted that brain areas representing the crowded percept would show repetition suppression in change-same trials but release from adaptation in change-different trials. This predicted pattern was observed throughout cortical visual areas V1–V4, increasing in strength from early to late visual areas. These results depict crowding as a multistage process, involving even the earliest cortical visual areas, with perceptual consequences that are increasingly influenced by later visual areas.

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.

Repetition suppression in occipital–temporal visual areas is modulated by physical rather than semantic features of objects

Functional magnetic-resonance imaging was used to identify areas involved in naming objects and to examine which of these areas adapted to either physical or semantics features of objects. We presented successive pairs of objects that were either the same exemplar of an object, different exemplars of that object, or different objects. By controlling for differences in physical features between pairs of different exemplars and different objects, visual areas in the occipital–temporal cortex were subject to repetition suppression when the same exemplars of an object were repeated, but not when different exemplars of an object were repeated. This was true independent of whether or not participants named objects. Repetition suppression in visual areas appeared therefore bound to physical features. Nevertheless, repetition suppression for physical features was greater in left visual areas when objects were named, suggesting that naming, known to depend on mechanisms in the left hemisphere, may induce greater attentional modulation in the left than in the right visual areas. Taken together, we propose that the difference between our findings and those of earlier studies that report semantic influences can be explained by the failure of those studies to control for differences in the appearance of different exemplars. Left frontal areas showed repetition suppression when either the same or different exemplars of an object were repeated, but only when participants named objects. These results suggest that visual areas process information about physical features without semantic modulation by higher-order areas, and that left frontal areas process semantic features, but the engagement of these processes is task modulated.

Spatial dynamics of masked picture repetition effects

The aim of this study was to further elucidate the mechanisms of early and automatic object processing using a masked picture priming paradigm with both identity and exemplar repetition in functional MRI (fMRI). Masked repetition priming has been commonly used with words to isolate automatic, rapidly occurring mechanisms involved in visual word recognition; however, studies using the technique of masked priming with rapid presentation of pictures have been limited. This study demonstrates how the masked priming technique can be used to study early, automatic processing of rapidly presented complex objects. Temporal-occipital regions previously found to be sensitive to repetition priming in both masked word and unmasked picture studies were found to show repetition suppression for the identity primes only. Most notably, when divided into anterior and posterior divisions, the fusiform gyrus showed anatomically specific repetition suppression only in the posterior portion. This finding is comparable to that found in a previous study of masked word priming, and the similarity may suggest an overlap in the early identification processes for visual word form and visual object processing in this region. Finally, masked repetition of different exemplar objects did not result in reliable neural effects, suggesting that the underlying mechanisms of the more semantic-based, different exemplar priming may occur later or require the intervention of conscious processes.

Two approaches to repetition suppression

Repetition suppression refers to the phenomenon that prior processing of stimuli (or stimulus attributes) decreases activation elicited by processing subsequent stimuli with identical attributes. We present two complementary approaches to identify regions that show repetition suppression for subsequent sentences with either identical: (1) sentence forms or (2) speakers. The first categorical approach simply compares sentences that are presented in Same and Different blocks. The second factorial approach operationally defines repetition suppression as decreased activation for the subsequent Same stimulus relative to its preceding sentence. To account for nonspecific time confounds, this approach tests for a repetition x condition (Same or Different) interaction. Surprisingly, the two approaches revealed different results: Only the categorical analysis detected sentence repetition effects in multiple regions within a bilateral frontotemporal system that has previously been implicated in sentence processing. These discrepancies might be due to the different efficiencies with which the particular contrasts were estimated or spurious differences in stimuli or attentional set that could not be entirely controlled within a single subject. Finally, we combined the two approaches in a [global null] conjunction analysis.

Distinct unimodal and multimodal regions for word processing in the left temporal cortex

How are word recognition circuits organized in the left temporal lobe? We used functional magnetic resonance imaging (fMRI) to dissect cortical word-processing circuits using three diagnostic criteria: the capacity of an area (1) to respond to words in a single modality (visual or auditory) or in both modalities, (2) to modulate its response in a top-down manner as a function of the graphemic or phonemic emphasis of the task, and (3) to show repetition suppression in response to the conscious repetition of the target word within the same sensory modality or across different modalities. The results clarify the organization of visual and auditory word-processing streams. In particular, the visual word form area (VWFA) in the left occipitotemporal sulcus appears strictly as a visual unimodal area. It is, however, bordered by a second lateral inferotemporal area which is multimodal [lateral inferotemporal multimodal area (LIMA)]. Both areas might have been confounded in past work. Our results also suggest a possible homolog of the VWFA in the auditory stream, the auditory word form area, located in the left anterior superior temporal sulcus.