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Understanding how the human brain gives rise to complex cognitive processes remains one of the biggest challenges of contemporary neuroscience. While invasive recording in animal models can provide insight into neural processes that are conserved across species, our understanding of cognition more broadly relies upon investigation of the human brain itself. There is therefore an imperative to establish non-invasive tools that allow human brain activity to be measured at high spatial and temporal resolution. In recent years, various attempts have been made to refine the coarse signal available in functional magnetic resonance imaging (fMRI), providing a means to investigate neural activity at the meso-scale, i.e. at the level of neural populations. The most widely used techniques include repetition suppression and multivariate pattern analysis. Human neuroscience can now use these techniques to investigate how representations are encoded across neural populations and transformed by relevant computations. Here, we review the physiological basis, applications and limitations of fMRI repetition suppression with a brief comparison to multivariate techniques. By doing so, we show how fMRI repetition suppression holds promise as a tool to reveal complex neural mechanisms that underlie human cognitive function. This article is part of the themed issue ‘Interpreting BOLD: a dialogue between cognitive and cellular neuroscience’.

In the human electroencephalogram (EEG), induced oscillatory responses in various frequency bands are regarded as valuable indices to examine the neural mechanisms underlying human memory. While the advent of virtual reality (VR) drives the investigation of mnemonic processing under more lifelike settings, the joint application of VR and EEG methods is still in its infancy (e.g., due to technical limitations impeding the signal acquisition). The objective of the present EEG study was twofold. First, we examined whether the investigation of induced oscillations under VR conditions yields equivalent results compared to standard paradigms. Second, we aimed at obtaining further insights into basic memory-related brain mechanisms in VR. To these ends, we relied on a standard implicit memory design, namely repetition priming, for which the to-be-expected effects are well-documented for conventional studies. Congruently, we replicated a suppression of the evoked potential after stimulus onset. Regarding the induced responses, we observed a modulation of induced alphaband in response to a repeated stimulus. Importantly, our results revealed a repetition-related suppression of the high-frequency induced gammaband response (>30 Hz), indicating the sharpening of a cortical object representation fostering behavioral priming effects. Noteworthy, the analysis of the induced gammaband responses required a number of measures to minimize the influence of external and internal sources of artefacts (i.e., the electrical shielding of the technical equipment and the control for miniature eye movements). In conclusion, joint VR–EEG studies with a particular focus on induced oscillatory responses offer a promising advanced understanding of mnemonic processing under lifelike conditions.

The oddball paradigm is commonly used to investigate human time perception. Trains of identical repeated events (‘standards’) are presented, only to be interrupted by a different ‘oddball’ that seems to have a relatively protracted duration. One theoretical account has been that this effect is driven by repetition suppression for repeated standards. The idea is that repeated events seem shorter as they incur a progressively reduced neural response, which is supported by the finding that oddball perceived duration increases linearly with the number of preceding repeated standards. However, typical oddball paradigms confound the probability of oddball presentations with variable numbers of standard repetitions on each trial, allowing people to increasingly anticipate an oddball presentation as more standards are presented. We eliminated this by making participants aware of what fixed number of standards they would encounter before a final test input and tested different numbers of standards in separate experimental sessions. The final event of sequences, the test event, was equally likely to be an oddball or another repeat. We found a positive linear relationship between the number of preceding repeated standards and the perceived duration of oddball test events. However, we also found this for repeat tests events, which speaks against the repetition suppression account of the temporal oddball effect.

In this review, we attempt to integrate the empirical evidence regarding stimulus-specific adaptation (SSA) and mismatch negativity (MMN) under a predictive coding perspective (also known as Bayesian or hierarchical-inference model). We propose a renewed methodology for SSA study, which enables a further decomposition of deviance detection into repetition suppression and prediction error, thanks to the use of two controls previously introduced in MMN research: the many-standards and the cascade sequences. Focusing on data obtained with cellular recordings, we explain how deviance detection and prediction error are generated throughout hierarchical levels of processing, following two vectors of increasing computational complexity and abstraction along the auditory neuraxis: from subcortical toward cortical stations and from lemniscal toward nonlemniscal divisions. Then, we delve into the particular characteristics and contributions of subcortical and cortical structures to this generative mechanism of hierarchical inference, analyzing what is known about the role of neuromodulation and local microcircuitry in the emergence of mismatch signals. Finally, we describe how SSA and MMN are occurring at similar time frame and cortical locations, and both are affected by the manipulation of N-methyl-D-aspartate receptors. We conclude that there is enough empirical evidence to consider SSA and MMN, respectively, as the microscopic and macroscopic manifestations of the same physiological mechanism of deviance detection in the auditory cortex. Hence, the development of a common theoretical framework for SSA and MMN is all the more recommendable for future studies. In this regard, we suggest a shared nomenclature based on the predictive coding interpretation of deviance detection.

Frequency specific synchronisation of neuronal firing within the gamma-band (30–70Hz) appears to be a fundamental correlate of both basic sensory and higher cognitive processing. In-vitro studies suggest that the neurochemical basis of gamma-band oscillatory activity is based on interactions between excitatory (i.e. glutamate) and inhibitory (i.e. GABA) neurotransmitter concentrations. However, the nature of the relationship between excitatory neurotransmitter concentration and changes in gamma band activity in humans remains undetermined. Here, we examine the links between dynamic glutamate concentration and the formation of functional gamma-band oscillatory networks. Using concurrently acquired event-related magnetic resonance spectroscopy and electroencephalography, during a repetition-priming paradigm, we demonstrate an interaction between stimulus type (object vs. abstract pictures) and repetition in evoked gamma-band oscillatory activity, and find that glutamate levels within the lateral occipital cortex, differ in response to these distinct stimulus categories. Importantly, we show that dynamic glutamate levels are related to the amplitude of stimulus evoked gamma-band (but not to beta, alpha or theta or ERP) activity. These results highlight the specific connection between excitatory neurotransmitter concentration and amplitude of oscillatory response, providing a novel insight into the relationship between the neurochemical and neurophysiological processes underlying cognition. •Evoked gamma-band activity changes in response to both object and abstract stimuli.•Glutamate levels in the LOC differ in response to distinct visual stimuli.•Glutamate levels correlate with concurrently measured gamma-band oscillatory power.•ER-MRS can quantify neurochemical concentration changes related to the EEG signal.

An increasing number of studies investigate the visual mismatch negativity (vMMN) or use the vMMN as a tool to probe various aspects of human cognition. This paper reviews the theoretical underpinnings of vMMN in the light of methodological considerations and provides recommendations for measuring and interpreting the vMMN. The following key issues are discussed from the experimentalist's point of view in a predictive coding framework: (1) experimental protocols and procedures to control \"refractoriness\" effects; (2) methods to control attention; (3) vMMN and veridical perception.

[Display omitted] The auditory cortex (AC) encompasses distinct fields subserving partly different aspects of sound processing. One essential function of the AC is the detection of unpredicted sounds, as revealed by differential neural activity to predictable and unpredictable sounds. According to the predictive coding framework, this effect can be explained by repetition suppression and/or prediction error signaling. The present study investigates functional specialization of the rat AC fields in repetition suppression and prediction error by combining a tone frequency oddball paradigm (involving high-probable standard and low-probable deviant tones) with two different control sequences (many-standards and cascade). Tones in the control sequences were comparable to deviant events with respect to neural adaptation but were not violating a regularity. Therefore, a difference in the neural activity between deviant and control tones indicates a prediction error effect, whereas a difference between control and standard tones indicates a repetition suppression effect. Single-unit recordings revealed by far the largest prediction error effects for the posterior auditory field, while the primary auditory cortex, the anterior auditory field, the ventral auditory field, and the suprarhinal auditory field were dominated by repetition suppression effects. Statistically significant repetition suppression effects occurred in all AC fields, whereas prediction error effects were less robust in the primary auditory cortex and the anterior auditory field. Results indicate that the non-lemniscal, posterior auditory field is more engaged in context-dependent processing underlying deviance-detection than the other AC fields, which are more sensitive to stimulus-dependent effects underlying differential degrees of neural adaptation.

Repeated stimulus presentation leads to reductions in responses of cortical neurons, known as repetition suppression or stimulus-specific adaptation. Circuit-based models of repetition suppression provide a framework for investigating patterns of repetition effects that propagate through cortical hierarchies. To further develop such models it is critical to determine whether (and if so, when) repetition effects are modulated by factors such as expectation and attention. We investigated whether repetition effects are influenced by perceptual expectations, and whether the time courses of each effect are similar or distinct, by presenting pairs of repeated and alternating face images and orthogonally manipulating expectations regarding the likelihood of stimulus repetition. Event-related potentials (ERPs) were recorded from n = 39 healthy adults, to map the spatiotemporal progression of stimulus repetition and stimulus expectation effects, and interactions between these, using mass univariate analyses. We also tested for another expectation effect that may contribute to repetition effects in many previous experiments: that repeated stimulus identities are predictable after seeing the first stimulus in a trial, but unrepeated stimulus identities cannot be predicted. Separate blocks were presented with predictable and unpredictable alternating face identities. Multiple repetition and expectation effects were identified between 99 and 800ms from stimulus onset, which did not statistically interact at any point and exhibited distinct spatiotemporal patterns of effects. Repetition effects in blocks with predictable alternating faces were smaller than in unpredictable alternating face blocks between 117-179 ms and 506–652ms, and larger between 246 and 428ms. The distinct spatiotemporal patterns of repetition and expectation effects support separable mechanisms underlying these phenomena. However, previous studies of repetition effects, in which the repeated (but not unrepeated) stimulus was predictable, are likely to have conflated repetition and stimulus predictability effects. •ERP face image repetition effects were apparent between 99 and 800ms from stimulus onset.•Expectations of stimulus image properties did not modulate face repetition effects.•The predictability of unrepeated stimuli influenced repetition effect magnitudes.

•fMRI-based adaptation, which has been developed as a tool to identify functional selectivity in the human brain, can also reveal the influence of neighboring neuronal populations.•Our data reveals neural evidence for a disinhibition effect as a result of the adaptation of adjacent populations, which is in line with the adapting reciprocal inhibition model.•Reciprocal inhibition can, thus, be tracked in the human brain using fMRI, adding to the understanding of human multistable perception and the neural coding of visual information.•Our results also provide a mechanism for reversal of repetition suppression effects. A model based on inhibitory coupling has been proposed to explain perceptual oscillations. This 'adapting reciprocal inhibition' model postulates that it is the strength of inhibitory coupling that determines the fate of competition between percepts. Here, we used an fMRI-based adaptation technique to reveal the influence of neighboring neuronal populations, such as reciprocal inhibition, in motion-selective hMT+/V5. If reciprocal inhibition exists in this region, the following predictions should hold: 1. stimulus-driven response would not simply decrease, as predicted by simple repetition-suppression of neuronal populations, but instead, increase due to the activity from adjacent populations; 2. perceptual decision involving competing representations, should reflect decreased reciprocal inhibition by adaptation; 3. neural activity for the competing percept should also later on increase upon adaptation. Our results confirm these three predictions, showing that a model of perceptual decision based on adapting reciprocal inhibition holds true. Finally, they also show that the net effect of the well-known repetition suppression phenomenon can be reversed by this mechanism.

•Repeated face images cause decreased fMRI signal in early visual cortex (EVC), occipital face area (OFA), and fusiform face area (FFA).•The repetition suppression (RS) effect can be explained by the modulation of connectivity between EVC and OFA/FFA.•The between-region modulation supports synchronization and predictive coding theories of RS.•Face perception modulates nearly all within- and between-region connectivity, including direct connections from EVC to FFA. Stimulus repetition normally causes reduced neural activity in brain regions that process that stimulus. Some theories claim that this “repetition suppression” reflects local mechanisms such as neuronal fatigue or sharpening within a region, whereas other theories claim that it results from changed connectivity between regions, following changes in synchrony or top-down predictions. In this study, we applied dynamic causal modeling (DCM) on a public fMRI dataset involving repeated presentations of faces and scrambled faces to test whether repetition affected local (self-connections) and/or between-region connectivity in left and right early visual cortex (EVC), occipital face area (OFA) and fusiform face area (FFA). Face “perception” (faces versus scrambled faces) modulated nearly all connections, within and between regions, including direct connections from EVC to FFA, supporting a non-hierarchical view of face processing. Face “recognition” (familiar versus unfamiliar faces) modulated connections between EVC and OFA/FFA, particularly in the left hemisphere. Most importantly, immediate and delayed repetition of stimuli were also best captured by modulations of connections between EVC and OFA/FFA, but not self-connections of OFA/FFA, consistent with synchronization or predictive coding theories, though also possibly reflecting local mechanisms like synaptic depression.