Using fNIRS to examine occipital and temporal responses to stimulus repetition in young infants: Evidence of selective frontal cortex involvement

How does the developing brain respond to recent experience? Repetition suppression (RS) is a robust and well-characterized response of to recent experience found, predominantly, in the perceptual cortices of the adult brain. We use functional near-infrared spectroscopy (fNIRS) to investigate how perceptual (temporal and occipital) and frontal cortices in the infant brain respond to auditory and visual stimulus repetitions (spoken words and faces). In Experiment 1, we find strong evidence of repetition suppression in the frontal cortex but only for auditory stimuli. In perceptual cortices, we find only suggestive evidence of auditory RS in the temporal cortex and no evidence of visual RS in any ROI. In Experiments 2 and 3, we replicate and extend these findings. Overall, we provide the first evidence that infant and adult brains respond differently to stimulus repetition. We suggest that the frontal lobe may support the development of RS in perceptual cortices.     

Repetition suppression and semantic enhancement: an investigation of the neural correlates of priming

The priming of a stimulus by another has become an important tool for exploring the neural underpinnings of conceptual representations. However, priming effects can derive from many different types of relationships and it is important to distinguish between them in order to be able to develop theoretical accounts of the representation of conceptual knowledge. While it is well known that repetition priming (the repeated presentation of the same stimulus) is associated with a reduced neural response, called repetition suppression (RS), the neural correlates of semantic priming (when two stimuli are related in meaning but not identical) are not so well established. We compared the neural correlates of repetition and semantic priming using written words, independently manipulating form and meaning. In an fMRI study, subjects saw single words and made a concrete-abstract decision. Two consecutive words were identical (town-town) or varied along a continuum of semantic relatedness, from highly related (cord-string) to unrelated (face-sail). We found distinct patterns of activation for repetition and semantic priming. Repetition priming was associated with RS in LIFG, bilateral parahippocampal gyrus and R fusiform gyrus. We also observed increased activation for word repetition in the RMFG and RMTG/STG, which may reflect recognition of item's earlier presentation. There was no evidence of suppression for semantic relatedness. Semantic priming was associated with enhanced activation in multiple bilateral fronto-temporal areas, i.e. semantic enhancement. The results suggest that repetition and semantic priming in visual word recognition depend on distinct cognitive processes and neural substrates.     

Decoding Object-Based Auditory Attention from Source-Reconstructed MEG Alpha Oscillations

How do we attend to relevant auditory information in complex naturalistic scenes? Much research has focused on detecting which information is attended, without regarding underlying top-down control mechanisms. Studies investigating attentional control generally manipulate and cue specific features in simple stimuli. However, in naturalistic scenes it is impossible to dissociate relevant from irrelevant information based on low-level features. Instead, the brain has to parse and select auditory objects of interest. The neural underpinnings of object-based auditory attention remain not well understood. Here we recorded MEG while 15 healthy human subjects (9 female) prepared for the repetition of an auditory object presented in one of two overlapping naturalistic auditory streams. The stream containing the repetition was prospectively cued with 70% validity. Crucially, this task could not be solved by attending low-level features, but only by processing the objects fully. We trained a linear classifier on the cortical distribution of source-reconstructed oscillatory activity to distinguish which auditory stream was attended. We could successfully classify the attended stream from alpha (8–14 Hz) activity in anticipation of repetition onset. Importantly, attention could only be classified from trials in which subjects subsequently detected the repetition, but not from miss trials. Behavioral relevance was further supported by a correlation between classification accuracy and detection performance. Decodability was not sustained throughout stimulus presentation, but peaked shortly before repetition onset, suggesting that attention acted transiently according to temporal expectations. We thus demonstrate anticipatory alpha oscillations to underlie top-down control of object-based auditory attention in complex naturalistic scenes.SIGNIFICANCE STATEMENT In everyday life, we often find ourselves bombarded with auditory information, from which we need to select what is relevant to our current goals. Previous research has highlighted how we attend to specific highly controlled aspects of the auditory input. Although invaluable, it is still unclear how this relates to attentional control in naturalistic auditory scenes. Here we used the high precision of magnetoencephalography in space and time to investigate the brain mechanisms underlying top-down control of object-based attention in ecologically valid sound scenes. We show that rhythmic activity in auditory association cortex at a frequency of ∼10 Hz (alpha waves) controls attention to currently relevant segments within the auditory scene and predicts whether these segments are subsequently detected.     

Appearing and disappearing stimuli trigger a reflexive modulation of visual cortical activity

From the vast array of stimuli continually inundating our senses, only a very small portion is selected for higher-order processing. This selection is influenced by voluntary and reflexive mechanisms that may act at multiple stages of analysis. Extensive research has revealed that top-down voluntary mechanisms modulate information processing at both "early" (e.g., perceptual) and "late" (e.g., semantic) stages. Bottom-up sensory-driven mechanisms, however, are less well understood. Previous investigations of bottom-up mechanisms may have been influenced by top-down mechanisms because the stimuli were task-relevant and required overt responses. Here, we directly measured bottom-up influences on visual information processing by recording event-related brain potentials (ERP) to sequences of task-irrelevant visual stimuli. We found that abrupt visual events triggered an automatic enhancement of extrastriate visual activity (the P1 ERP component) to subsequent visual stimuli occurring at the same location. In contrast to theories suggesting that the abrupt appearance of a new object is unique in being able to trigger bottom-up effects, we found that disappearing objects triggered the same enhancement of subsequent stimulus processing as did appearing objects. The present data, however, also provide new electrophysiological evidence for a level of analysis in the brain that may be specific to the appearance of new objects. These data thus provide evidence that abruptly appearing objects may evoke specialized processing at certain stages of analysis in the brain but that, despite this difference, appearing and disappearing objects both trigger reflexive mechanisms that bias neural activity in human extrastriate visual cortex.     

Attentional control of the processing of neural and emotional stimuli

A typical scene contains many different objects that compete for neural representation due to the limited processing capacity of the visual system. At the neural level, competition among multiple stimuli is evidenced by the mutual suppression of their visually evoked responses and occurs most strongly at the level of the receptive field. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that biasing signals due to selective attention can modulate neural activity in visual cortex not only in the presence but also in the absence of visual stimulation. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals likely derives from a distributed network of areas in frontal and parietal cortex. Competition suggests that once attentional resources are depleted, no further processing is possible. Yet, existing data suggest that emotional stimuli activate brain regions "automatically," largely immune from attentional control. We tested the alternative possibility, namely, that the neural processing of stimuli with emotional content is not automatic and instead requires some degree of attention. Our results revealed that, contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, similar to the processing of other stimulus categories, the processing of facial expression is under top-down control.     

Dissociable effects of top-down and bottom-up attention during episodic encoding

It is well established that the formation of memories for life's experiences-episodic memory-is influenced by how we attend to those experiences, yet the neural mechanisms by which attention shapes episodic encoding are still unclear. We investigated how top-down and bottom-up attention contribute to memory encoding of visual objects in humans by manipulating both types of attention during fMRI of episodic memory formation. We show that dorsal parietal cortex-specifically, intraparietal sulcus (IPS)-was engaged during top-down attention and was also recruited during the successful formation of episodic memories. By contrast, bottom-up attention engaged ventral parietal cortex-specifically, temporoparietal junction (TPJ)-and was also more active during encoding failure. Functional connectivity analyses revealed further dissociations in how top-down and bottom-up attention influenced encoding: while both IPS and TPJ influenced activity in perceptual cortices thought to represent the information being encoded (fusiform/lateral occipital cortex), they each exerted opposite effects on memory encoding. Specifically, during a preparatory period preceding stimulus presentation, a stronger drive from IPS was associated with a higher likelihood that the subsequently attended stimulus would be encoded. By contrast, during stimulus processing, stronger connectivity with TPJ was associated with a lower likelihood the stimulus would be successfully encoded. These findings suggest that during encoding of visual objects into episodic memory, top-down and bottom-up attention can have opposite influences on perceptual areas that subserve visual object representation, suggesting that one manner in which attention modulates memory is by altering the perceptual processing of to-be-encoded stimuli.     

Self-face enhances processing of immediately preceding invisible faces

The self-face is thought to be an especially salient stimulus. Behavioral evidence suggests that self-face processing advantage is associated with enhanced processing of temporally adjacent subliminal stimuli. However, the neural basis of this self-related processing modulation has not been investigated.We studied self-face induced signal amplification through masked priming and repetition suppression (fMRI adaptation). Subjects performed a gender-categorization task on self- and non-self target faces preceded by subliminal (17 ms) prime faces. The relationship between prime and target was varied between task-incongruent (when prime and target belonged to a different gender) and task-congruent (when prime and target belonged to the same gender) pairs.We found that, in the presence of the visible self-face (but not of other non-self faces), a bilateral fronto-parietal network exhibited repetition suppression to subliminal prime faces belonging to the same gender (task-congruent) as the target, consistent with the notion that, in the presence of the self-face, subliminal stimuli access high-level processing systems. These results are in agreement with the notion of self-specific top-down amplification of subliminal task-relevant information, and suggest that the self-face, through its high salience, is particularly efficacious in focusing attention.     

Audiovisual temporal fusion in 6-month-old infants

The aim of this study was to investigate neural dynamics of audiovisual temporal fusion processes in 6-month-old infants using event-related brain potentials (ERPs). In a habituation-test paradigm, infants did not show any behavioral signs of discrimination of an audiovisual asynchrony of 200 ms, indicating perceptual fusion. In a subsequent EEG experiment, audiovisual synchronous stimuli and stimuli with a visual delay of 200 ms were presented in random order. In contrast to the behavioral data, brain activity differed significantly between the two conditions. Critically, N1 and P2 latency delays were not observed between synchronous and fused items, contrary to previously observed N1 and P2 latency delays between synchrony and perceived asynchrony. Hence, temporal interaction processes in the infant brain between the two sensory modalities varied as a function of perceptual fusion versus asynchrony perception. The visual recognition components Pb and Nc were modulated prior to sound onset, emphasizing the importance of anticipatory visual events for the prediction of auditory signals. Results suggest mechanisms by which young infants predictively adjust their ongoing neural activity to the temporal synchrony relations to be expected between vision and audition.     

Dishabituation of laser-evoked EEG responses: dissecting the effect of certain and uncertain changes in stimulus modality

The repetition of nociceptive stimuli of identical modality, intensity, and location at short and constant interstimulus intervals (ISIs) determines a strong habituation of the corresponding EEG responses, without affecting the subjective perception of pain. To understand what determines this response habituation, we (i) examined the effect of introducing a change in the modality of the repeated stimulus, and (ii) dissected the relative contribution of bottom-up, stimulus-driven changes in modality and top-down, cognitive expectations of such a change, on both laser-evoked and auditory-evoked EEG responses. Multichannel EEG was recorded while participants received trains of three stimuli (S1-S2-S3, a triplet) delivered to the hand dorsum at 1-sec ISI. S3 belonged either to the same modality as S1 and S2 or to the other modality. In addition, participants were either explicitly informed or not informed of the modality of S3. We found that introducing a change in stimulus modality produced a significant dishabituation of the laser-evoked N1, N2, and P2 waves; the auditory N1 and P2 waves; and the laser- and auditory-induced event-related synchronization and desynchronization. In contrast, the lack of explicit knowledge of a possible change in the sensory modality of the stimulus (i.e., uncertainty) only increased the ascending portion of the laser-evoked and auditory-evoked P2 wave. Altogether, these results indicate that bottom-up novelty resulting from the change of stimulus modality, and not top-down cognitive expectations, plays a major role in determining the habituation of these brain responses.     

Does surprise enhancement or repetition suppression explain visual mismatch negativity?

A long tradition of electrophysiological studies, using oddball sequences, showed that the neural responses to a given stimulus differ when their presentation occurs frequently (standards) as compared to rare, infrequent presentations (deviants). This difference, originally described in acoustic perception, can also be detected in the visual modality and is termed as visual mismatch negativity (vMMN). Also, a large number of studies detected the reduction of the neuronal response after the repetition of a given stimulus (repetition suppression – RS) and it was suggested that RS is the major mechanism of MMN, an explanation currently also supported by animal studies. However, human studies have proposed that a surprise‐related response enhancement for the deviant stimuli might also underlie vMMN. Therefore, the aim of the current study was to disentangle which neural mechanism explains vMMN better: the surprise related response enhancement for the presentation of rare deviants or the RS related to the frequent presentation of the standards. Since the MMN depends strongly on the applied categories, we tested the neural mechanisms of vMMN for different stimulus categories (faces, chairs, real and false characters) using a visual oddball paradigm. We found significant vMMN for every stimulus category. Interestingly, the neural mechanisms behind vMMN were found to be category dependent (assuming no cross‐adaptation effects): for faces and chairs it was largely driven by RS, whereas for real and false characters it was mainly due to surprise‐related changes.     

Accentuate or repeat? Brain signatures of developmental periods in infant word recognition

Language acquisition has long been discussed as an interaction between biological preconditions and environmental input. This general interaction seems particularly salient in lexical acquisition, where infants are already able to detect unknown words in sentences at 7 months of age, guided by phonological and statistical information in the speech input. While this information results from the linguistic structure of a given language, infants also exploit situational information, such as speakers' additional word accentuation and word repetition. The current study investigated the developmental trajectory of infants' sensitivity to these two situational input cues in word recognition. Testing infants at 6, 9, and 12 months of age, we hypothesized that different age groups are differentially sensitive to accentuation and repetition. In a familiarization–test paradigm, event-related brain potentials (ERPs) revealed age-related differences in infants' word recognition as a function of situational input cues: at 6 months infants only recognized previously accentuated words, at 9 months both accentuation and repetition played a role, while at 12 months only repetition was effective. These developmental changes are suggested to result from infants' advancing linguistic experience and parallel auditory cortex maturation. Our data indicate very narrow and specific input-sensitive periods in infant word recognition, with accentuation being effective prior to repetition.     

A practical guide to applying machine learning to infant EEG data

Electroencephalography (EEG) has been widely adopted by the developmental cognitive neuroscience community, but the application of machine learning (ML) in this domain lags behind adult EEG studies. Applying ML to infant data is particularly challenging due to the low number of trials, low signal-to-noise ratio, high inter-subject variability, and high inter-trial variability. Here, we provide a step-by-step tutorial on how to apply ML to classify cognitive states in infants. We describe the type of brain attributes that are widely used for EEG classification and also introduce a Riemannian geometry based approach for deriving connectivity estimates that account for inter-trial and inter-subject variability. We present pipelines for learning classifiers using trials from a single infant and from multiple infants, and demonstrate the application of these pipelines on a standard infant EEG dataset of forty 12-month-old infants collected under an auditory oddball paradigm. While we classify perceptual states induced by frequent versus rare stimuli, the presented pipelines can be easily adapted for other experimental designs and stimuli using the associated code that we have made publicly available.     

Facilitative effect of repetitive presentation of one stimulus on cortical responses to other stimuli in macaque monkeys – a possible neural mechanism for mismatch negativity

The event‐related potential ‘mismatch negativity’ (MMN) is an indicator of a perceiver's ability to detect deviations in sensory signal streams. MMN and its homologue in animals, mismatch activity (MMA), are differential neural responses to a repeatedly presented stimulus and a subsequent deviant stimulus (oddball). Because neural mechanisms underlying MMN and MMA remain unclear, there is a controversy as to whether MMN and MMA arise solely from stimulus‐specific adaptation (SSA), in which the response to a stimulus cumulatively attenuates with its repetitive presentation. To address this issue, we used electrocorticography and the auditory roving‐oddball paradigm in two awake macaque monkeys. We examined the effect of stimulus repetition number on MMA and on responses to repeated stimuli and oddballs across the cerebral cortex in the time–frequency domain. As the repetition number increased, MMA spread across the temporal, frontal and parietal cortices, and each electrode yielded a larger MMA. Surprisingly, this increment in MMA largely depended on response augmentation to the oddball rather than on SSA to the repeated stimulus. Following sufficient repetition, the oddball evoked a spectral power increment in some electrodes on the frontal cortex that had shown no power increase to the stimuli with less or no preceding repetition. We thereby revealed that repetitive presentation of one stimulus not only leads to SSA but also facilitates the cortical response to oddballs involving a wide range of cortical regions. This facilitative effect might underlie the generation of MMN‐like scalp potentials in macaques that potentially shares similar neural mechanisms with MMN in humans.     

Affective interoceptive inference: Evidence from heart‐beat evoked brain potentials

The perception of internal bodily signals (interoception) is central to many theories of emotion and embodied cognition. According to recent theoretical views, the sensory processing of visceral signals such as one's own heartbeat is determined by top‐down predictions about the expected interoceptive state of the body (interoceptive inference). In this EEG study we examined neural responses to heartbeats following expected and unexpected emotional stimuli. We used a modified stimulus repetition task in which pairs of facial expressions were presented with repeating or alternating emotional content, and we manipulated the emotional valence and the likelihood of stimulus repetition. We found that affective predictions of external socially relevant information modulated the heartbeat‐evoked potential, a marker of cardiac interoception. Crucially, the HEP changes highly relied on the expected emotional content of the facial expression. Thus, expected negative faces led to a decreased HEP amplitude, whereas such an effect was not observed after an expected neutral face. These results suggest that valence‐specific affective predictions, and their uniquely associated predicted bodily sensory state, can reduce or amplify cardiac interoceptive responses. In addition, the affective repetition effects were dependent on repetition probability, highlighting the influence of top‐down exteroceptive predictions on interoception. Our results are in line with recent models of interoception supporting the idea that predicted bodily states influence sensory processing of salient external information.     

Context‐dependent coding and gain control in the auditory system of crickets

Sensory systems process stimuli that greatly vary in intensity and complexity. To maintain efficient information transmission, neural systems need to adjust their properties to these different sensory contexts, yielding adaptive or stimulus‐dependent codes. Here, we demonstrated adaptive spectrotemporal tuning in a small neural network, i.e. the peripheral auditory system of the cricket. We found that tuning of cricket auditory neurons was sharper for complex multi‐band than for simple single‐band stimuli. Information theoretical considerations revealed that this sharpening improved information transmission by separating the neural representations of individual stimulus components. A network model inspired by the structure of the cricket auditory system suggested two putative mechanisms underlying this adaptive tuning: a saturating peripheral nonlinearity could change the spectral tuning, whereas broad feed‐forward inhibition was able to reproduce the observed adaptive sharpening of temporal tuning. Our study revealed a surprisingly dynamic code usually found in more complex nervous systems and suggested that stimulus‐dependent codes could be implemented using common neural computations.     

Attention Distributed across Sensory Modalities Enhances Perceptual Performance

This study investigated the interaction between top-down attentional control and multisensory processing in humans. Using semantically congruent and incongruent audiovisual stimulus streams, we found target detection to be consistently improved in the setting of distributed audiovisual attention versus focused visual attention. This performance benefit was manifested as faster reaction times for congruent audiovisual stimuli and as accuracy improvements for incongruent stimuli, resulting in a resolution of stimulus interference. Electrophysiological recordings revealed that these behavioral enhancements were associated with reduced neural processing of both auditory and visual components of the audiovisual stimuli under distributed versus focused visual attention. These neural changes were observed at early processing latencies, within 100-300 ms poststimulus onset, and localized to auditory, visual, and polysensory temporal cortices. These results highlight a novel neural mechanism for top-down driven performance benefits via enhanced efficacy of sensory neural processing during distributed audiovisual attention relative to focused visual attention.     

Repetition suppression of induced gamma activity predicts enhanced orienting toward a novel stimulus in 6-month-old infants

Habituation refers to a decline in orienting or responding to a repeated stimulus, and can be inferred to reflect learning about the properties of the repeated stimulus when followed by increased orienting to a novel stimulus (i.e., novelty detection). Habituation and novelty detection paradigms have been used for over 40 years to study perceptual and mnemonic processes in the human infant, yet important questions remain about the nature of these processes in infants. The aim of the present study was to examine the neural mechanisms underlying habituation and novelty detection in infants. Specifically, we investigated changes in induced alpha, beta, and gamma activity in 6-month-old infants during repeated presentations of either a face or an object, and examined whether these changes predicted behavioral responses to novelty at test. We found that induced gamma activity over occipital scalp regions decreased with stimulus repetition in the face condition but not in the toy condition, and that greater decreases in the gamma band were associated with enhanced orienting to a novel face at test. The pattern and topography of these findings are consistent with observations of repetition suppression in the occipital-temporal visual processing pathway, and suggest that encoding in infant habituation paradigms may reflect a form of perceptual learning. Implications for the role of repetition suppression in infant habituation and novelty detection are discussed with respect to a biased competition model of visual attention.     

Is developmental dyslexia modality specific? A visual-auditory comparison of Italian dyslexics

Although developmental dyslexia is often referred to as a cross-modal disturbance, tests of different modalities using the same stimuli are lacking. We compared the performance of 23 children with dyslexia and 42 chronologically matched control readers on reading versus repetition tasks and visual versus auditory lexical decision using the same stimuli. With respect to control readers, children with dyslexia were impaired only on stimuli in the visual modality; they had no deficit on the repetition and auditory lexical decision tasks. By applying the rate-amount model (Faust et al., 1999), we showed that performance of children with dyslexia on visual (but not auditory) tasks was associated with that of control readers by a linear relationship (with a 1.78 slope), suggesting that a global factor accounts for visual (but not auditory) task performance.We conclude that the processing of linguistic stimuli in the visual and auditory modalities is carried out by independent processes and that dyslexic children have a selective deficit in the visual modality.     

Dissociable neural mechanisms for encoding predictable and unpredictable events

Attention is a necessary condition for the formation of new episodic memories, yet little is known about how dissociable attentional mechanisms for "top-down" and "bottom-up" orienting contribute to encoding. Here, subjects performed an intentional encoding task in which to-be-learned items were interspersed with irrelevant stimuli such that subjects could anticipate the appearance of some study items but not others. Subjects were more likely to later remember stimuli whose appearance was predictable at encoding. Electroencephalographic data were acquired during the study phase of the experiment to assess how synchronous neural activity related to later memory for predictable stimuli (to which attention could be oriented in a top-down fashion) and unpredictable stimuli (which rely to a greater extent on bottom-up attentional orienting). Over left frontal regions, gamma-band activity (25-55 Hz) early (approximately 150 msec) in the epoch was a robust predictor of later memory for predictable items, consistent with an emerging view that links high-frequency neural synchrony to top-down attention. By contrast, later (approximately 400 msec) theta-band activity (4-8 Hz) over the left and midline frontal cortex predicted subsequent memory for unpredictable items, suggesting a role in bottom-up attentional orienting. These results reveal for the first time the contribution of dissociable attentional mechanisms to successful encoding and contribute to a growing literature dedicated to understanding the role of neural synchrony in cognition.     

Auditory evoked transient and sustained potentials in the human EEG: I. Effects of expectation of stimuli

The characteristics of auditory evoked transient and sustained potentials were recorded using trains of four-tone stimuli of 1-second duration (interstimulus interval = 1 second) presented once every minute. The subject either attentively expected the stimuli or ignored them while reading. The electroencephalogram was recorded from derivations Cz-Al and Fz-Al. Expectation of the stimuli was associated with increased amplitudes of the transient responses both at the first stimulus of the train and during stimulus repetition. In contrast, the sustained potential at the first stimulus of the train was unchanged or smaller when the subject expected the stimuli. During stimulus repetition, however, the amplitude of the potential was enhanced by expectation of the stimuli. The results support the hypothesis of two sustained potential components and stress the importance of stimulus repetition rate when sustained potentials are studied.