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de Lange, F. P.

Publications and source records attributed to de Lange, F. P..

At least 37 records · Page 2Linked to original sources

Seeing sounds: Neural mechanisms underlying auditory contributions to visual detection

Sounds enhance the detection of visual stimuli while concurrently biasing an observers decisions. To investigate the neural mechanisms that underlie such multisensory interactions, we decoded time-resolved signal detection theory (SDT) sensitivity and criterion parameters from neural activity using magnetoencalography, while participants performed a visual detection task. Using temporal generalization analysis, we found that sounds improve visual detection by enhancing the maintenance of the most informative perceptual samples over time. In parallel, criterion decoding analyses revealed that sounds evoke patterns of activity that resembled the patterns evoked by an actual visual stimulus. These two complementary mechanisms of audiovisual interaction differed in terms of their automaticity: Whereas the sound-induced enhancement in visual information maintenance depended on participants being actively engaged in a detection task, sounds evoked visual activity patterns in the visual cortex in a bottom-up fashion, challenging the classical assumption that sound- induced reductions in criterion correspond to decision-level biases.

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Prediction and preview strongly affect reading times but not skipping during natural reading

In a typical text, readers look much longer at some words than at others and fixate some words multiple times, while skipping others altogether. Historically, researchers explained this variation via low-level visual or oculomotor factors, but today it is primarily explained in terms of cognitive factors, such as how well word identity can be predicted from context or discerned from parafoveal preview. While the existence of these effects has been well established in experiments, the relative importance of prediction, preview and low-level factors for eye movement variation in natural reading is unclear. Here, we address this question in three large datasets (n=104, 1.5 million words), using a deep neural network and Bayesian ideal observer to model linguistic prediction and parafoveal preview from moment to moment in natural reading. Strikingly, neither prediction nor preview was important for explaining word skipping - the vast majority of skipping was explained by a simple oculomotor model. For reading times, by contrast, we found strong but independent contributions of both prediction and preview, with effect sizes matching those from controlled experiments. Together, these results challenge dominant models of eye movements in reading by showing that linguistic prediction and parafoveal preview are not important determinants of word skipping.

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Adaptation and serial choice bias are unaltered in autism

Autism Spectrum Disorder (ASD) or autism is characterized by social and non-social symptoms, including sensory hyper- and hyposensitivities. A suggestion has been put forward that some of these symptoms could be explained by differences in how sensory information is integrated with its context, including a lower tendency to leverage the past in the processing of new perceptual input. At least two history-dependent effects of opposite directions have been described in the visual perception literature: a repulsive adaptation effect, where perception of a stimulus is biased away from an adaptor stimulus, and an attractive serial choice bias, where perceptual choices are biased towards the previous choice. In this study, we investigated whether autistic participants differed in either bias from typically developing controls (TD). Sixty-four adolescent participants (31 with ASD, 33 TD) were asked to categorize oriented line stimuli in two tasks which were designed so that we would induce either adaptation or serial choice bias. Although our tasks successfully induced both biases, in comparing the two groups, we found no differences in the magnitude of adaptation nor in the modulation of perceptual choices by the previous choice. In conclusion, we find no evidence of a decreased integration of the past in visual perception of autistic individuals.

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Brief stimuli cast a long-term trace in visual cortex

Visual processing is strongly influenced by the recent stimulus history - a phenomenon termed adaptation. Prominent theories cast adaptation as a consequence of optimized encoding of visual information, by exploiting the temporal statistics of the world. However, this would require the visual system to track the history of individual briefly experienced events, within a stream of visual input, to build up statistical representations over longer timescales. Here, using an openly available dataset from the Allen Brain Observatory, we show that neurons in the early visual cortex of the mouse indeed maintain long-term traces of individual past stimuli that persist despite the presentation of several intervening stimuli, leading to long-term and stimulus-specific adaptation over dozens of seconds. Long-term adaptation was selectively expressed in cortical, but not in thalamic neurons, which only showed short-term adaptation. Early visual cortex thus maintains concurrent stimulusspecific memory traces of past input, enabling the visual system to build up a statistical representation of the world to optimize the encoding of new information in a changing environment. Significance StatementIn the natural world, previous sensory input is predictive of current input over multi-second timescales. The visual system could exploit these predictabilities by adapting current visual processing to the long-term history of visual input. However, it is unclear whether the visual system can track the history of individual briefly experienced images, within a stream of input, to build up statistical representations over such long timescales. Here, we show that neurons in early visual cortex of the mouse brain exhibit remarkably long-term adaptation to brief stimuli, persisting over dozens of seconds, and despite the presentation of several intervening stimuli. The visual cortex thus maintains long-term traces of individual briefly experienced past images, enabling the formation of statistical representations over extended timescales.

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Alpha oscillations shape sensory representation and perceptual accuracy

Alpha activity (8-14 Hz) is the dominant rhythm in the awake brain, and thought to play an important role in setting the brains internal state. Previous work has associated states of decreased alpha power with enhanced neural excitability. However, evidence is mixed on whether and how such excitability enhancement modulates sensory signals of interest versus noise differently, and what, if any, the consequences are for subsequent perception. Here, human subjects (male and female) performed a visual detection task in which we manipulated their decision criteria in a block-wise manner. While our manipulation led to substantial criterion shifts, these shifts were not reflected in pre-stimulus alpha-band changes. Rather, lower pre-stimulus alpha power in occipital-parietal areas improved perceptual sensitivity and enhanced information content decodable from neural activity patterns. Additionally, oscillatory alpha phase immediately before stimulus presentation modulated accuracy. Together, our results suggest that alpha-band dynamics modulate sensory signals of interest more strongly than noise. Significance statementThe internal state of our brain fluctuates, giving rise to variability in perception and action. Neural oscillations, most prominently in the alpha-band, have been suggested to play a role in setting this internal state. Here, we show that ongoing alpha-band activity in occipital-parietal regions predicts the quality of visual information decodable in neural activity patterns, and subsequently human observers sensitivity in a visual detection task. Our results provide comprehensive evidence that visual representation is modulated by ongoing alpha-band activity, and advance our understanding on how, when faced with unchanging external stimuli, internal neural fluctuations influence perception and behavior.

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A hierarchy of linguistic predictions during natural language comprehension

Understanding spoken language requires transforming ambiguous acoustic streams into a hierarchy of representations, from phonemes to meaning. It has been suggested that the brain uses prediction to guide the interpretation of incoming input. However, the role of prediction in language processing remains disputed, with disagreement about both the ubiquity and representational nature of predictions. Here, we address both issues by analysing brain recordings of participants listening to audiobooks, and using a deep neural network (GPT-2) to precisely quantify contextual predictions. First, we establish that brain responses to words are modulated by ubiquitous, probabilistic predictions. Next, we disentangle model-based predictions into distinct dimensions, revealing dissociable signatures of syntactic, phonemic and semantic predictions. Finally, we show that high-level (word) predictions inform low-level (phoneme) predictions, supporting hierarchical predictive processing. Together, these results underscore the ubiquity of prediction in language processing, showing that the brain spontaneously predicts upcoming language at multiple levels of abstraction.

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Temporal prediction elicits rhythmic pre-activation of relevant sensory cortices

Being able to anticipate events before they happen facilitates stimulus processing. The anticipation of the contents of events is thought to be implemented by the elicitation of prestimulus templates in sensory cortex. In contrast, the anticipation of the timing of events is typically associated with entrainment of neural oscillations. It is so far unknown whether and in which conditions temporal expectations interact with feature-based expectations, and, consequently, whether entrainment modulates the generation of content-specific sensory templates. In this study, we investigated the role of temporal expectations in a sensory discrimination task. We presented participants with rhythmically interleaved visual and auditory streams of relevant and irrelevant stimuli while measuring neural activity using magnetoencephalography. We found no evidence that rhythmic stimulation induced prestimulus feature templates. However, we did observe clear anticipatory rhythmic pre-activation of the relevant sensory cortices. This oscillatory activity peaked at behaviourally relevant, in-phase, intervals. Our results suggest that temporal expectations about stimulus features do not behave similarly to explicitly cued, non-rhythmic, expectations; yet elicit a distinct form of modality-specific pre-activation. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=165 SRC="FIGDIR/small/347005v3_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@fce8corg.highwire.dtl.DTLVardef@1c16c3corg.highwire.dtl.DTLVardef@1a90d62org.highwire.dtl.DTLVardef@1adaa17_HPS_FORMAT_FIGEXP M_FIG C_FIG The brain extracts temporal regularities from the environment to anticipate upcoming events. Furthermore, with prior knowledge about their contents, the brain is thought to leverage this by instantiating anticipatory sensory templates. We investigated if sensory templates occur in response to a rhythmic stimulus stream with predictable temporal structure. We found that temporal rhythmic predictions did not induce sensory templates, but rather modulated the excitability in early sensory cortices.

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Does dopamine synthesis capacity predict individual variation in curiosity?

Curiosity, which can be defined as "intrinsically motivated information-seeking", is an important driving force in our everyday lives. Based on previous evidence demonstrating a link between information prediction errors and dopamine neuronal firing rates, we asked whether the drive to seek information varies with individual differences in dopamine synthesis capacity. In order to investigate this, we let participants perform a lottery task in which we independently manipulated outcome uncertainty, outcome valence (gains versus losses) and expected value, and asked participants to indicate their curiosity for each presented lottery. In a separate session, participants underwent an [18F]DOPA PET scan to quantify their dopamine synthesis capacity. We replicate previous behavioral results, showing that curiosity is a function of outcome uncertainty as well as outcome valence (gain versus loss). However, we found no evidence that curiosity or the sensitivity to outcome uncertainty, outcome valence and expected value was related to participants dopamine synthesis capacity in the ventral striatum, the caudate nucleus or the putamen. These findings stress the need for further studies into the role of dopamine in (different types of) curiosity.

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No exploitation of temporal predictive context during visual search

The human visual system can rapidly extract regularities from our visual environment, generating predictive context. It has been shown that spatial predictive context can be used during visual search. We set out to see whether observers can additionally exploit temporal predictive context, using an extended version of a contextual cueing paradigm. Though we replicated the contextual cueing effect, repeating search scenes in a structured order versus a random order yielded no additional behavioural benefit. This was true both for participants who were sensitive to spatial predictive context, and for those who were not. We argue that spatial predictive context during visual search is more readily learned and subsequently exploited than temporal predictive context, potentially rendering the latter redundant. In conclusion, unlike spatial context, temporal context is not automatically extracted and used during visual search.

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Spatial and temporal context jointly modulate the sensory response within the ventral visual stream

Both spatial and temporal context play an important role in visual perception and behavior. Humans can extract statistical regularities from both forms of context to help processing the present and to construct expectations about the future. Numerous studies have found reduced neural responses to expected stimuli compared to unexpected stimuli, for both spatial and temporal regularities. However, it is largely unclear whether and how these forms of context interact. In the current fMRI study, thirty-three human volunteers were exposed to object stimuli that could be expected or surprising in terms of their spatial and temporal context. We found a reliable independent contribution of both spatial and temporal context in modulating the neural response. Specifically, neural responses to stimuli in expected compared to unexpected contexts were suppressed throughout the ventral visual stream. Interestingly, the modulation by spatial context was stronger in magnitude and more reliable than modulations by temporal context. These results suggest that while both spatial and temporal context serve as a prior that can modulate sensory processing in a similar fashion, predictions of spatial context may be a more powerful modulator in the visual system. Significance StatementBoth temporal and spatial context can affect visual perception, however it is largely unclear if and how these different forms of context interact in modulating sensory processing. When manipulating both temporal and spatial context expectations, we found that they jointly affected sensory processing, evident as a suppression of neural responses for expected compared to unexpected stimuli. Interestingly, the modulation by spatial context was stronger than that by temporal context. Together, our results suggest that spatial context may be a stronger modulator of neural responses than temporal context within the visual system. Thereby, the present study provides new evidence how different types of predictions jointly modulate perceptual processing.

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Action enhances predicted touch

It is widely believed that predicted tactile action outcomes are perceptually attenuated. The present experiments determined whether predictive mechanisms always generate attenuation, or instead can enhance perception - as typically observed in sensory cognition domains outside of action. We manipulated probabilistic expectations in a paradigm often used to demonstrate tactile attenuation. Participants produced actions and subsequently rated the intensity of forces on a passive finger. Experiment 1 confirmed previous findings that action outcomes are perceived less intensely than passive stimulation, but demonstrated more intense perception when active finger stimulation was removed. Experiments 2 and 3 manipulated prediction explicitly and found that expected touch during action is perceived more intensely than unexpected touch. Computational modelling suggested that expectations increase the gain afforded to expected tactile signals. These findings challenge a central tenet of prominent motor control theories and demonstrate that sensorimotor predictions do not exhibit a qualitatively distinct influence on tactile perception. Statement of RelevancePerception of expected action outcomes is thought to be attenuated. Such a mechanism may be adaptive because surprising inputs are more useful - e.g., signalling the need to take new courses of action - and is thought to explain why we cannot tickle ourselves and unusual aspects of action and awareness in clinical populations. However, theories outside of action purport that predicted events are perceptually facilitated, allowing us to generate largely accurate representations of our noisy sensory world. We do not know whether action predictions really alter perception differently from other predictions because different manipulations have been performed. Here we perform similar manipulations and demonstrate that action predictions can enhance, rather than attenuate, touch. We thereby demonstrate that action predictions may not have a qualitatively distinct influence on perception, such that we must re-examine theories concerning how predictions influence perception across domains and clinical theories based upon their assumptions.

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Opposite effects of choice history and stimulus history resolve a paradox of sequential choice bias

Perceptual decisions are biased towards previous decisions. Previous research suggests that this choice repetition bias is increased after previous decisions of high confidence, as inferred from response time measures (Urai et al., 2017), but also when previous decisions were based on weak sensory evidence (Akaishi et al., 2014). As weak sensory evidence is typically associated with low confidence, these previous findings appear conflicting. To resolve this conflict, we set out to investigate the effect of decision confidence on choice repetition more directly by measuring explicit confidence ratings in a motion coherence discrimination task. Moreover, we explored how choice and stimulus history jointly affect subsequent perceptual choices. We found that participants were more likely to repeat previous choices of high subjective confidence, as well as previous fast choices, confirming the boost of choice repetition with decision confidence. Furthermore, we discovered that current choices were biased away from the previous evidence direction, not previous choice, and that this effect grew with previous evidence strength. These findings point towards simultaneous biases of choice repetition, modulated by decision confidence, and adaptation, modulated by the strength of evidence, which bias current perceptual decisions in opposite directions.

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A Bayesian and efficient observer model explains concurrent attractive and repulsive history biases in visual perception

Perceptual decisions can be repelled away from (repulsive adaptation) or attracted towards recent visual experience (attractive serial dependence). It is currently unclear whether and how these repulsive and attractive biases interact during visual processing and what computational principles may underlie these history dependencies. In the current study, we disentangle repulsive and attractive biases by exploring the respective timescales over which current visual processing is influenced by previous experience. Across four experiments, we find that perceptual decisions about stimulus orientation are concurrently attracted towards the short-term perceptual history and repelled from stimuli experienced up to minutes into the past. We show that the temporal pattern of short-term attraction and long-term repulsion cannot be captured by an ideal Bayesian observer model alone. Instead, it is well captured by an ideal observer model with efficient encoding and Bayesian decoding of visual information in a slowly changing environment. Concurrent attractive and repulsive history biases in perceptual decisions may thus be the consequence of the need for visual processing to simultaneously satisfy constraints of both efficiency and stability.

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Temporal tuning of repetition suppression across the visual cortex

The visual system adapts to its recent history. A phenomenon related to this is repetition suppression (RS) - a reduction in neural responses to repeated compared to non-repeated visual input. An intriguing hypothesis is that the timescale over which RS occurs across the visual hierarchy is tuned to the temporal statistics of visual input features, which change rapidly in low-level areas but are more stable in higher-level areas. Here, we tested this hypothesis by studying the influence of the temporal lag between successive visual stimuli on RS throughout the visual system using fMRI. Twelve human volunteers engaged in four fMRI sessions in which we characterized the BOLD response to pairs of repeated and non-repeated natural images with inter-stimulus intervals (ISI) ranging from 50 to 1000 milliseconds to quantify the temporal tuning of RS along the posterior-anterior axis of the visual system. As expected, RS was maximal for short ISIs and decayed with increasing ISI. Furthermore, the overall magnitude of RS gradually increased from posterior to anterior visual areas. Crucially, however, and against our hypothesis, RS decayed at a similar rate in early and late visual areas. This finding challenges the prevailing view that the timescale of RS increases along the posterior-anterior axis of the visual system and suggests that RS is not tuned to temporal input regularities.

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Statistical learning attenuates visual activity only for attended stimuli

Perception and behavior can be guided by predictions, which are often based on learned statistical regularities. Neural responses to expected stimuli are frequently found to be attenuated after statistical learning. However, whether this sensory attenuation following statistical learning occurs automatically or depends on attention remains unknown. In the present fMRI study, we exposed human volunteers to sequentially presented object stimuli, in which the first object predicted the identity of the second object. We observed a strong attenuation of neural activity for expected compared to unexpected stimuli in the ventral visual stream. Crucially, this sensory attenuation was only apparent when stimuli were attended, and vanished when attention was directed away from the predictable objects. These results put important constraints on neurocomputational theories that cast perception as a process of probabilistic integration of prior knowledge and sensory information.

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Electrocorticographic dissociation of alpha and beta rhythmic activity in the human sensorimotor system

This study uses electrocorticography in humans to assess how alpha- and beta-band rhythms modulate excitability of the sensorimotor cortex during movement selection, as indexed through a psychophysically-controlled movement imagery task. Both rhythms displayed effector-specific modulations, tracked spectral markers of action potentials in the local neuronal population, and showed spatially systematic phase relationships (traveling waves). Yet, alpha- and beta-band rhythms differed in their anatomical and functional properties, were weakly correlated, and traveled along opposite directions across the sensorimotor cortex. Increased alpha-band power in the somatosensory cortex ipsilateral to the selected arm was associated with spatially-unspecific inhibition. Decreased beta-band power over contralateral motor cortex was associated with a focal shift from relative inhibition to excitation. These observations indicate the relevance of both inhibition and disinhibition mechanisms for precise spatiotemporal coordination of neuronal populations during movement selection. Those mechanisms are implemented through the substantially different neurophysiological properties of sensorimotor alpha- and beta-band rhythms.

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Implicit learning and exploitation of regularities involve hippocampal and prefrontal theta activity

Observers rapidly and seemingly automatically learn to predict where to expect relevant items when those items are repeatedly presented in the same spatial context. This form of statistical learning in visual search has been studied extensively using a paradigm known as contextual cueing. The neural mechanisms underlying the learning and exploiting of such regularities remain unclear. We sought to elucidate these by examining behaviour and recording neural activity using magneto-encephalography (MEG) while observers were implicitly acquiring and exploiting statistical regularities. Computational modelling of behavioural data suggested that after repeated exposures to a spatial context, participants behaviour was marked by an abrupt switch to an exploitation strategy of the learnt regularities. MEG recordings showed that the initial learning phase was associated with larger hippocampal theta band activity for repeated scenes, while the subsequent exploitation phase showed larger prefrontal theta band activity for these repeated scenes. Strikingly, the behavioural benefit of repeated exposures to certain scenes was inversely related to explicit awareness of such repeats, demonstrating the implicit nature of the expectations acquired. This elucidates how theta activity in the hippocampus and prefrontal cortex underpins the implicit learning and exploitation of spatial statistical regularities to optimize visual search behaviour.

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The role of feature-based attention in visual serial dependence

Perceptual decisions about current sensory input are biased towards input of the recent past - a phenomenon termed serial dependence. Serial dependence may serve to stabilize neural representations in the face of external and internal noise. However, it is unclear under which circumstances previous input attracts subsequent perceptual decisions, and thus, whether serial dependence reflects a broad smoothing or selective stabilization operation. Here, we investigated whether focusing attention on particular features of the previous stimulus modulates serial dependence. We found an attractive bias in orientation estimations when previous and current stimuli had similar orientations, and a repulsive bias when they had dissimilar orientations. The attractive bias was markedly reduced when observers attended to the size, rather than the orientation, of the previous stimulus. Conversely, the repulsive bias for stimuli with large orientation differences was not modulated by feature-based attention. This suggests separate sources of these positive and negative perceptual biases.

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