Richard F. Betzel; Lisa Byrge; Farnaz Zamani Esfahlani; Daniel P. Kennedy
Temporal fluctuations in the brain's modular architecture during movie-watching Journal Article
In: NeuroImage, vol. 213, pp. 116687, 2020.
Brain networks are flexible and reconfigure over time to support ongoing cognitive processes. However, tracking statistically meaningful reconfigurations across time has proven difficult. This has to do largely with issues related to sampling variability, making instantaneous estimation of network organization difficult, along with increased reliance on task-free (cognitively unconstrained) experimental paradigms, limiting the ability to interpret the origin of changes in network structure over time. Here, we address these challenges using time-varying network analysis in conjunction with a naturalistic viewing paradigm. Specifically, we developed a measure of inter-subject network similarity and used this measure as a coincidence filter to identify synchronous fluctuations in network organization across individuals. Applied to movie-watching data, we found that periods of high inter-subject similarity coincided with reductions in network modularity and increased connectivity between cognitive systems. In contrast, low inter-subject similarity was associated with increased system segregation and more rest-like architectures. We then used a data-driven approach to uncover clusters of functional connections that follow similar trajectories over time and are more strongly correlated during movie-watching than at rest. Finally, we show that synchronous fluctuations in network architecture over time can be linked to a subset of features in the movie. Our findings link dynamic fluctuations in network integration and segregation to patterns of inter-subject similarity, and suggest that moment-to-moment fluctuations in functional connectivity reflect shared cognitive processing across individuals.
Rodrigo M. Braga; Lauren M. DiNicola; Hannah C. Becker; Randy L. Buckner
Situating the left-lateralized language network in the broader organization of multiple specialized large-scale distributed networks Journal Article
In: Journal of neurophysiology, vol. 124, no. 5, pp. 1415–1448, 2020.
Using procedures optimized to explore network organization within the individual, the topography of a candidate language network was characterized and situated within the broader context of adjacent networks. The candidate network was first identified using functional connectivity and replicated across individuals, acquisition tasks, and analytical methods. In addition to classical language regions near the perisylvian cortex and temporal pole, regions were also observed in dorsal posterior cingulate, midcingulate, and anterior superior frontal and inferior temporal cortex. The candidate network was selectively activated when processing meaningful (as contrasted with nonword) sentences, whereas spatially adjacent networks showed minimal or even decreased activity. Results were replicated and triplicated across two prospectively acquired cohorts. Examined in relation to adjacent networks, the topography of the language network was found to parallel the motif of other association networks, including the transmodal association networks linked to theory of mind and episodic remembering (often collectively called the default network). The several networks contained juxtaposed regions in multiple association zones. Outside of these juxtaposed higher-order networks, we further noted a distinct frontotemporal network situated between language regions and a frontal orofacial motor region and a temporal auditory region. A possibility is that these functionally related sensorimotor regions might anchor specialization of neighboring association regions that develop into a language network. What is most striking is that the canonical language network appears to be just one of multiple similarly organized, differentially specialized distributed networks that populate the evolutionarily expanded zones of human association cortex.
Johannes Brand; Marco Piccirelli; Marie Claude Hepp-Reymond; Kynan Eng; Lars Michels
Brain activation during visually guided finger movements Journal Article
In: Frontiers in Human Neuroscience, vol. 14, pp. 309, 2020.
Computer interaction via visually guided hand movements often employs either abstract cursor-based feedback or virtual hand (VH) representations of varying degrees of realism. The effect of changing this visual feedback in virtual reality settings is currently unknown. In this study, 19 healthy right-handed adults performed index finger movements (“action”) and observed movements (“observation”) with four different types of visual feedback: a simple circular cursor (CU), a point light (PL) pattern indicating finger joint positions, a shadow cartoon hand (SH) and a realistic VH. Finger movements were recorded using a data glove, and eye-tracking was recorded optically. We measured brain activity using functional magnetic resonance imaging (fMRI). Both action and observation conditions showed stronger fMRI signal responses in the occipitotemporal cortex compared to baseline. The action conditions additionally elicited elevated bilateral activations in motor, somatosensory, parietal, and cerebellar regions. For both conditions, feedback of a hand with a moving finger (SH, VH) led to higher activations than CU or PL feedback, specifically in early visual regions and the occipitotemporal cortex. Our results show the stronger recruitment of a network of cortical regions during visually guided finger movements with human hand feedback when compared to a visually incomplete hand and abstract feedback. This information could have implications for the design of visually guided tasks involving human body parts in both research and application or training-related paradigms.
Batel Buaron; Daniel Reznik; Roee Gilron; Roy Mukamel
Voluntary actions modulate perception and neural representation of action-consequences in a hand-dependent manner Journal Article
In: Cerebral Cortex, vol. 30, no. 12, pp. 6097–6107, 2020.
Evoked neural activity in sensory regions and perception of sensory stimuli are modulated when the stimuli are the consequence of voluntary movement, as opposed to an external source. It has been suggested that such modulations are due to motor commands that are sent to relevant sensory regions during voluntary movement. However, given the anatomical-functional laterality bias of the motor system, it is plausible that the pattern of such behavioral and neural modulations will also exhibit a similar bias, depending on the effector triggering the stimulus (e.g., right/left hand). Here, we examined this issue in the visual domain using behavioral and neural measures (fMRI). Healthy participants judged the relative brightness of identical visual stimuli that were either self-triggered (using right/left hand button presses), or triggered by the computer. Stimuli were presented either in the right or left visual field. Despite identical physical properties of the visual consequences, we found stronger perceptual modulations when the triggering hand was ipsi- (rather than contra-) lateral to the stimulated visual field. Additionally, fMRI responses in visual cortices differentiated between stimuli triggered by right/left hand. Our findings support a model in which voluntary actions induce sensory modulations that follow the anatomical-functional bias of the motor system.
Nicoletta Cera; João Castelhano; Cátia Oliveira; Joana Carvalho; Ana Luísa Quinta Gomes; Maria Manuela Peixoto; Raquel Pereira; Erick Janssen; Miguel Castelo-Branco; Pedro Nobre
The role of anterior and posterior insula in male genital response and in visual attention: An exploratory multimodal fMRI study Journal Article
In: Scientific Reports, vol. 10, pp. 18463, 2020.
Several studies highlighted the role of insula on several functions and in sexual behavior. This exploratory study examines the relationships among genital responses, brain responses, and eye movements, to disentangle the role played by the anterior and posterior insula during different stages of male sexual response and during visual attention to sexual stimuli. In 19 healthy men, fMRI, eye movement, and penile tumescence data were collected during a visual sexual stimulation task. After a whole-brain analysis comparing neutral and sexual clips and confirming a role for the bilateral insulae, we selected two bilateral seed regions in anterior and posterior insula for functional connectivity analysis. Single-ROI-GLMs were run for the FC target regions. Single-ROI-GLMs were performed based on areas to which participants fixate: “Faces”, “Genitals,” and “Background” with the contrast “Genitals > Faces”. Single-ROI-GLMs with baseline, onset, and sustained PT response for the sexual clips were performed. We found stronger effects for the posterior than the anterior insula. In the target regions of the posterior insula, we found three different pathways: the first involved in visual attention, onset of erection, and sustained erection; the second involved only in the onset of erection, and the third limited to sustained erection.
Rutvik H. Desai; Wonil Choi; John M. Henderson
Word frequency effects in naturalistic reading Journal Article
In: Language, Cognition and Neuroscience, vol. 35, no. 5, pp. 1–12, 2020.
Word frequency is a central psycholinguistic variable that accounts for substantial variance in language processing. A number of neuroimaging studies have examined frequency at a single word level, typically demonstrating a strong negative, and sometimes positive correlation between frequency and hemodynamic response. Here, 40 subjects read passages of text in an MRI scanner while their eye movements were recorded. We used fixation-related analysis to identify neural activity tied to the frequency of each fixated word. We found that negative correlations with frequency were reduced, while strong positive correlations were found in the temporal and parietal areas associated with semantics. We propose that the processing cost of low frequency words is reduced due to contextual cues. Meanings of high frequency words are more readily accessed and integrated with context resulting in enhanced processing in the semantic system. The results demonstrate similarities and differences between single word and naturalistic text processing.
Lauren M. DiNicola; Rodrigo M. Braga; Randy L. Buckner
Parallel distributed networks dissociate episodic and social functions within the individual Journal Article
In: Journal of Neurophysiology, vol. 123, no. 3, pp. 1144–1179, 2020.
Association cortex is organized into large-scale distributed networks. One such network, the default network (DN), is linked to diverse forms of internal mentation, opening debate about whether shared or distinct anatomy supports multiple forms of cognition. Using within-individual analysis procedures that preserve idiosyncratic anatomical details, we probed whether multiple tasks from two domains, episodic projection and theory of mind (ToM), rely on the same or distinct networks. In an initial experiment (6 subjects, each scanned 4 times), we found evidence that episodic projection and ToM tasks activate separate regions distributed throughout the cortex, with adjacent regions in parietal, temporal, prefrontal, and midline zones. These distinctions were predicted by the hypothesis that the DN comprises two parallel, interdigitated networks. One network, linked to parahippocampal cortex (PHC), is preferentially recruited during episodic projection, including both remembering and imagining the future. A second juxtaposed network, which includes the temporoparietal junction (TPJ), is differentially engaged during multiple forms of ToM. In two prospectively acquired independent experiments, we replicated and triplicated the dissociation (each with 6 subjects scanned 4 times). Furthermore, the dissociation was found in all zones when analyzed independently, including robustly in midline regions previously described as hubs. The TPJ-linked network is interwoven with the PHC-linked network across the cortex, making clear why it is difficult to fully resolve the two networks in group-averaged or lower-resolution data. These results refine our understanding of the functional-anatomical organization of association cortex and raise fundamental questions about how specialization might arise in parallel, juxtaposed association networks.
Florin Dolcos; Yuta Katsumi; Chen Shen; Paul C. Bogdan; Suhnyoung Jun; Ryan Larsen; Wendy Heller; Kelly Freeman Bost; Sanda Dolcos
The impact of focused attention on emotional experience: A functional MRI investigation Journal Article
In: Cognitive, Affective and Behavioral Neuroscience, vol. 20, no. 5, pp. 1011–1026, 2020.
Emotional well-being depends on the ability to adaptively cope with various emotional challenges. Most studies have investigated the neural mechanisms of emotion regulation strategies deployed relatively later in the timing of processing that leads to full emotional experiences. However, less is known about strategies that are engaged in earlier stages of emotion processing, such as those involving attentional deployment. We investigated the neural mechanisms associated with self-guided Focused Attention (FA) in mitigating subjective negative emotional experiences. Functional magnetic resonance imaging (fMRI) data were recorded while participants viewed a series of composite negative and neutral images with distinguishable foreground (FG) and background (BG) areas. Participants were instructed to focus either on the FG or BG components of the images, and then rated their emotional experiences. Behavioral results showed that FA was successful in decreasing emotional ratings for negative images viewed in BG Focus condition. At the neural level, the BG Focus was associated with increased activity in regions typically implicated in top-down executive control (dorsolateral prefrontal cortex and lateral parietal cortex) and decreased activity in regions linked to affective processing (amygdala and ventrolateral prefrontal cortex). Dissociable brain activity linked to FA also was identified in visual cortices, including between the parahippocampal and fusiform gyri, showing increased versus decreased activity, respectively, during the BG Focus. These findings complement the evidence from prior FA studies with recollected emotional memories as internal stimuli and further demonstrate the effectiveness of self-guided FA in mitigating negative emotional experiences associated with processing of external unpleasant stimuli.
Laura Dugué; Elisha Merriam; David Heeger; Marisa Carrasco
Differential impact of endogenous and exogenous attention on activity in human visual cortex Journal Article
In: Scientific Reports, vol. 10, pp. 21274, 2020.
How do endogenous (voluntary) and exogenous (involuntary) attention modulate activity in visual cortex? Using ROI-based fMRI analysis, we measured fMRI activity for valid and invalid trials (target at cued/un-cued location, respectively), pre- or post-cueing endogenous or exogenous attention, while participants performed the same orientation discrimination task. We found stronger modulation in contralateral than ipsilateral visual regions, and higher activity in valid- than invalid-trials. For endogenous attention, modulation of stimulus-evoked activity due to a pre-cue increased along the visual hierarchy, but was constant due to a post-cue. For exogenous attention, modulation of stimulus-evoked activity due to a pre-cue was constant along the visual hierarchy, but was not modulated due to a post-cue. These findings reveal that endogenous and exogenous attention distinctly modulate activity in visuo-occipital areas during orienting and reorienting; endogenous attention facilitates both the encoding and the readout of visual information whereas exogenous attention only facilitates the encoding of information.
Benedetta Franceschiello; Lorenzo Di Sopra; Astrid Minier; Silvio Ionta; David Zeugin; Michael P. Notter; Jessica A. M. Bastiaansen; João Jorge; Jérôme Yerly; Matthias Stuber; Micah M. Murray
3-dimensional magnetic resonance imaging of the freely moving human eye Journal Article
In: Progress in Neurobiology, vol. 194, pp. 1–8, 2020.
Eye motion is a major confound for magnetic resonance imaging (MRI) in neuroscience or ophthalmology. Currently, solutions toward eye stabilisation include participants fixating or administration of paralytics/anaesthetics. We developed a novel MRI protocol for acquiring 3-dimensional images while the eye freely moves. Eye motion serves as the basis for image reconstruction, rather than an impediment. We fully reconstruct videos of the moving eye and head. We quantitatively validate data quality with millimetre resolution in two ways for individual participants. First, eye position based on reconstructed images correlated with simultaneous eye-tracking. Second, the reconstructed images preserve anatomical properties; the eye's axial length measured from MRI images matched that obtained with ocular biometry. The technique operates on a standard clinical setup, without necessitating specialized hardware, facilitating wide deployment. In clinical practice, we anticipate that this may help reduce burdens on both patients and infrastructure, by integrating multiple varieties of assessments into a single comprehensive session. More generally, our protocol is a harbinger for removing the necessity of fixation, thereby opening new opportunities for ethologically-valid, naturalistic paradigms, the inclusion of populations typically unable to stably fixate, and increased translational research such as in awake animals whose eye movements constitute an accessible behavioural readout.
Matthias Fritsche; Samuel J. D. Lawrence; Floris P. Lange
Temporal tuning of repetition suppression across the visual cortex Journal Article
In: Journal of Neurophysiology, vol. 123, no. 1, pp. 224–233, 2020.
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 with nonrepeated 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 functional (f)MRI. Twelve human volunteers engaged in four fMRI sessions in which we characterized the blood oxygen level-dependent response to pairs of repeated and nonrepeated natural images with interstimulus intervals (ISI) ranging from 50 to 1,000 ms 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. 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.
Mengyuan Gong; Taosheng Liu
Continuous and discrete representations of feature-based attentional priority in human frontoparietal network Journal Article
In: Cognitive Neuroscience, vol. 11, no. 1-2, pp. 47–59, 2020.
Previous studies suggest that human frontoparietal network represents feature-based attentional priority, yet the precise nature of the priority signals remains unclear. Here, we examined whether priority signals vary continuously or discretely as a function of feature similarity. In an fMRI experiment, we presented two superimposed dot fields moving along two linear directions (leftward and rightward) while varying the angular separation between the two directions. Subjects were cued to attend to one of the two dot fields and respond to a possible speed-up in the cued direction. We used multivariate analysis to evaluate how priority representation of the attended direction changes with feature similarity. We found that in early visual areas as well as posterior intraparietal sulcus and inferior frontal junction, the patterns of neural activity became more different as the feature similarity decreased, indicating a continuous representation of the attended feature. In contrast, patterns of neural activity in anterior intraparietal sulcus and frontal eye field remained invariant to changes in feature similarity, indicating a discrete representation of the attended feature. Such distinct neural coding of attentional priority across the frontoparietal network may make complementary contributions to enable flexible attentional control.
Tianlu Wang; Ronald Peeters; Dante Mantini; Céline R. Gillebert
Modulating the interhemispheric activity balance in the intraparietal sulcus using real-time fMRI neurofeedback: Development and proof-of-concept Journal Article
In: NeuroImage: Clinical, vol. 28, pp. 102513, 2020.
The intraparietal sulcus (IPS) plays a key role in the distribution of attention across the visual field. In stroke patients, an imbalance between left and right IPS activity has been related to a spatial bias in visual attention characteristic of hemispatial neglect. In this study, we describe the development and implementation of a real-time functional magnetic resonance imaging neurofeedback protocol to noninvasively and volitionally control the interhemispheric IPS activity balance in neurologically healthy participants. Six participants performed three neurofeedback training sessions across three weeks. Half of them trained to voluntarily increase brain activity in left relative to right IPS, while the other half trained to regulate the IPS activity balance in the opposite direction. Before and after the training, we estimated the distribution of attention across the visual field using a whole and partial report task. Over the course of the training, two of the three participants in the left-IPS group increased the activity in the left relative to the right IPS, while the participants in the right-IPS group were not able to regulate the interhemispheric IPS activity balance. We found no evidence for a decrease in resting-state functional connectivity between left and right IPS, and the spatial distribution of attention did not change over the course of the experiment. This study indicates the possibility to voluntarily modulate the interhemispheric IPS activity balance. Further research is warranted to examine the effectiveness of this technique in the rehabilitation of post-stroke hemispatial neglect.
Clifford I. Workman; Keith J. Yoder; Jean Decety
The dark side of morality–neural mechanisms underpinning moral convictions and support for violence Journal Article
In: AJOB Neuroscience, vol. 11, no. 4, pp. 269–284, 2020.
People are motivated by shared social values that, when held with moral conviction, can serve as compelling mandates capable of facilitating support for ideological violence. The current study examined this dark side of morality by identifying specific cognitive and neural mechanisms associated with beliefs about the appropriateness of sociopolitical violence, and determining the extent to which the engagement of these mechanisms was predicted by moral convictions. Participants reported their moral convictions about a variety of sociopolitical issues prior to undergoing functional MRI scanning. During scanning, they were asked to evaluate the appropriateness of violent protests that were ostensibly congruent or incongruent with their views about sociopolitical issues. Complementary univariate and multivariate analytical strategies comparing neural responses to congruent and incongruent violence identified neural mechanisms implicated in processing salience and in the encoding of subjective value. As predicted, neuro-hemodynamic response was modulated parametrically by individuals' beliefs about the appropriateness of congruent relative to incongruent sociopolitical violence in ventromedial prefrontal cortex, and by moral conviction in ventral striatum. Overall moral conviction was predicted by neural response to congruent relative to incongruent violence in amygdala. Together, these findings indicate that moral conviction about sociopolitical issues serves to increase their subjective value, overriding natural aversion to interpersonal harm.
Rick A. Adams; Daniel Bush; Fanfan Zheng; Sofie S. Meyer; Raphael Kaplan; Stelios Orfanos; Tiago Reis Marques; Oliver D. Howes; Neil Burgess
Impaired theta phase coupling underlies frontotemporal dysconnectivity in schizophrenia Journal Article
In: Brain, vol. 143, no. 3, pp. 1261–1277, 2020.
Frontotemporal dysconnectivity is a key pathology in schizophrenia. The specific nature of this dysconnectivity is unknown, but animal models imply dysfunctional theta phase coupling between hippocampus and medial prefrontal cortex (mPFC). We tested this hypothesis by examining neural dynamics in 18 participants with a schizophrenia diagnosis, both medicated and unmedicated; and 26 age, sex and IQ matched control subjects. All participants completed two tasks known to elicit hippocampal-prefrontal theta coupling: a spatial memory task (during magnetoencephalography) and a memory integration task. In addition, an overlapping group of 33 schizophrenia and 29 control subjects underwent PET to measure the availability of GABAARs expressing the a5 subunit (concentrated on hippocampal somatostatin interneurons). We demonstrate-in the spatial memory task, during memory recall-that theta power increases in left medial temporal lobe (mTL) are impaired in schizophrenia, as is theta phase coupling between mPFC and mTL. Importantly, the latter cannot be explained by theta power changes, head movement, antipsychotics, cannabis use, or IQ, and is not found in other frequency bands. Moreover, mPFC-mTL theta coupling correlated strongly with performance in controls, but not in subjects with schizophrenia, who were mildly impaired at the spatial memory task and no better than chance on the memory integration task. Finally, mTL regions showing reduced phase coupling in schizophrenia magnetoencephalography participants overlapped substantially with areas of diminished a5-GABAAR availability in the wider schizophrenia PET sample. These results indicate that mPFC-mTL dysconnectivity in schizophrenia is due to a loss of theta phase coupling, and imply a5-GABAARs (and the cells that express them) have a role in this process.
Yasaman Bagherzadeh; Daniel Baldauf; Dimitrios Pantazis; Robert Desimone
Alpha synchrony and the neurofeedback control of spatial attention Journal Article
In: Neuron, vol. 105, no. 3, pp. 577–587.e5, 2020.
During MEG neurofeedback training, subjects learned to manipulate the degree of alpha synchrony over the left versus right parietal cortex. The change in alpha synchrony was associated with a corresponding bias in visual processing and attention in the corresponding visual field.
Sonya Bells; Silvia L. Isabella; Donald C. Brien; Brian C. Coe; Douglas P. Munoz; Donald J. Mabbott; Douglas O. Cheyne
Mapping neural dynamics underlying saccade preparation and execution and their relation to reaction time and direction errors Journal Article
In: Human Brain Mapping, vol. 41, no. 7, pp. 1934–1949, 2020.
Our ability to control and inhibit automatic behaviors is crucial for negotiating complex environments, all of which require rapid communication between sensory, motor, and cognitive networks. Here, we measured neuromagnetic brain activity to investigate the neural timing of cortical areas needed for inhibitory control, while 14 healthy young adults performed an interleaved prosaccade (look at a peripheral visual stimulus) and antisaccade (look away from stimulus) task. Analysis of how neural activity relates to saccade reaction time (SRT) and occurrence of direction errors (look at stimulus on antisaccade trials) provides insight into inhibitory control. Neuromagnetic source activity was used to extract stimulus-aligned and saccade-aligned activity to examine temporal differences between prosaccade and antisaccade trials in brain regions associated with saccade control. For stimulus-aligned antisaccade trials, a longer SRT was associated with delayed onset of neural activity within the ipsilateral parietal eye field (PEF) and bilateral frontal eye field (FEF). Saccade-aligned activity demonstrated peak activation 10ms before saccade-onset within the contralateral PEF for prosaccade trials and within the bilateral FEF for antisaccade trials. In addition, failure to inhibit prosaccades on anti-saccade trials was associated with increased activity prior to saccade onset within the FEF contralateral to the peripheral stimulus. This work on dynamic activity adds to our knowledge that direction errors were due, at least in part, to a failure to inhibit automatic prosaccades. These findings provide novel evidence in humans regarding the temporal dynamics within oculomotor areas needed for saccade programming and the role frontal brain regions have on top-down inhibitory control.
Mathieu Bourguignon; Martijn Baart; Efthymia C. Kapnoula; Nicola Molinaro
Lip-reading enables the brain to synthesize auditory features of unknown silent speech Journal Article
In: Journal of Neuroscience, vol. 40, no. 5, pp. 1053–1065, 2020.
Lip-reading is crucial for understanding speech in challenging conditions. But how the brain extracts meaning from, silent, visual speech is still under debate. Lip-reading in silence activates the auditory cortices, but it is not known whether such activation reflects immediate synthesis of the corresponding auditory stimulus or imagery of unrelated sounds. To disentangle these possibilities, we used magnetoencephalography to evaluate how cortical activity in 28 healthy adult humans (17 females) entrained to the auditory speech envelope and lip movements (mouth opening) when listening to a spoken story without visual input (audio-only), and when seeing a silent video of a speaker articulating another story (video-only). In video-only, auditory cortical activity entrained to the absent auditory signal at frequencies <1 Hz more than to the seen lip movements. This entrainment process was characterized by an auditory-speech-to-brain delay of $sim$70 ms in the left hemisphere, compared with $sim$20 ms in audio-only. Entrainment to mouth opening was found in the right angular gyrus at <1 Hz, and in early visual cortices at 1– 8 Hz. These findings demonstrate that the brain can use a silent lip-read signal to synthesize a coarse-grained auditory speech representation in early auditory cortices. Our data indicate the following underlying oscillatory mechanism: seeing lip movements first modulates neuronal activity in early visual cortices at frequencies that match articulatory lip movements; the right angular gyrus then extracts slower features of lip movements, mapping them onto the corresponding speech sound features; this information is fed to auditory cortices, most likely facilitating speech parsing.
Nadine Dijkstra; Luca Ambrogioni; Diego Vidaurre; Marcel Gerven
Neural dynamics of perceptual inference and its reversal during imagery Journal Article
In: eLife, vol. 9, pp. 1–19, 2020.
After the presentation of a visual stimulus, neural processing cascades from low-level sensory areas to increasingly abstract representations in higher-level areas. It is often hypothesised that a reversal in neural processing underlies the generation of mental images as abstract representations are used to construct sensory representations in the absence of sensory input. According to predictive processing theories, such reversed processing also plays a central role in later stages of perception. Direct experimental evidence of reversals in neural information flow has been missing. Here, we used a combination of machine learning and magnetoencephalography to characterise neural dynamics in humans. We provide direct evidence for a reversal of the perceptual feed-forward cascade during imagery and show that, during perception, such reversals alternate with feed-forward processing in an 11 Hz oscillatory pattern. Together, these results show how common feedback processes support both veridical perception and mental imagery.
Leyla Isik; Anna Mynick; Dimitrios Pantazis; Nancy Kanwisher
The speed of human social interaction perception Journal Article
In: NeuroImage, vol. 215, pp. 116844, 2020.
The ability to perceive others' social interactions, here defined as the directed contingent actions between two or more people, is a fundamental part of human experience that develops early in infancy and is shared with other primates. However, the neural computations underlying this ability remain largely unknown. Is social interaction recognition a rapid feedforward process or a slower post-perceptual inference? Here we used magnetoencephalography (MEG) decoding to address this question. Subjects in the MEG viewed snapshots of visually matched real-world scenes containing a pair of people who were either engaged in a social interaction or acting independently. The presence versus absence of a social interaction could be read out from subjects' MEG data spontaneously, even while subjects performed an orthogonal task. This readout generalized across different people and scenes, revealing abstract representations of social interactions in the human brain. These representations, however, did not come online until quite late, at 300 ms after image onset, well after feedforward visual processes. In a second experiment, we found that social interaction readout still occurred at this same late latency even when subjects performed an explicit task detecting social interactions. We further showed that MEG responses distinguished between different types of social interactions (mutual gaze vs joint attention) even later, around 500 ms after image onset. Taken together, these results suggest that the human brain spontaneously extracts information about others' social interactions, but does so slowly, likely relying on iterative top-down computations.
Jakub Limanowski; Vladimir Litvak; Karl Friston
Cortical beta oscillations reflect the contextual gating of visual action feedback Journal Article
In: NeuroImage, vol. 222, pp. 117267, 2020.
In sensorimotor integration, the brain needs to decide how its predictions should accommodate novel evidence by ‘gating' sensory data depending on the current context. Here, we examined the oscillatory correlates of this process by recording magnetoencephalography (MEG) data during a new task requiring action under intersensory conflict. We used virtual reality to decouple visual (virtual) and proprioceptive (real) hand postures during a task in which the phase of grasping movements tracked a target (in either modality). Thus, we rendered visual information either task-relevant or a (to-be-ignored) distractor. Under visuo-proprioceptive incongruence, occipital beta power decreased (relative to congruence) when vision was task-relevant but increased when it had to be ignored. Dynamic causal modeling (DCM) revealed that this interaction was best explained by diametrical, task-dependent changes in visual gain. These results suggest a crucial role for beta oscillations in the contextual gating (i.e., gain or precision control) of visual vs proprioceptive action feedback, depending on current behavioral demands.
Brain dynamics for confidence-weighted learning Journal Article
In: PLoS Computational Biology, vol. 16, no. 6, pp. e1007935, 2020.
Learning in a changing, uncertain environment is a difficult problem. A popular solution is to predict future observations and then use surprising outcomes to update those predictions. However, humans also have a sense of confidence that characterizes the precision of their predictions. Bayesian models use a confidence-weighting principle to regulate learning: For a given surprise, the update is smaller when the confidence about the prediction was higher. Prior behavioral evidence indicates that human learning adheres to this confidence-weighting principle. Here, we explored the human brain dynamics sub-tending the confidenceweighting of learning using magneto-encephalography (MEG). During our volatile probability learning task, subjects' confidence reports conformed with Bayesian inference. MEG revealed several stimulus-evoked brain responses whose amplitude reflected surprise, and some of them were further shaped by confidence: Surprise amplified the stimulus-evoked response whereas confidence dampened it. Confidence about predictions also modulated several aspects of the brain state: Pupil-linked arousal and beta-range (15-30 Hz) oscillations. The brain state in turn modulated specific stimulus-evoked surprise responses following the confidence-weighting principle. Our results thus indicate that there exist, in the human brain, signals reflecting surprise that are dampened by confidence in a way that is appropriate for learning according to Bayesian inference. They also suggest a mechanism for confidence-weighted learning: Confidence about predictions would modulate intrinsic properties of the brain state to amplify or dampen surprise responses evoked by discrepant observations.
Anna M. Monk; Gareth R. Barnes; Eleanor A. Maguire
The effect of object type on building scene imagery — An MEG study Journal Article
In: Frontiers in Human Neuroscience, vol. 14, pp. 592175, 2020.
Previous studies have reported that some objects evoke a sense of local three-dimensional space (space-defining; SD), while others do not (space-ambiguous; SA), despite being imagined or viewed in isolation devoid of a background context. Moreover, people show a strong preference for SD objects when given a choice of objects with which to mentally construct scene imagery. When deconstructing scenes, people retain significantly more SD objects than SA objects. It, therefore, seems that SD objects might enjoy a privileged role in scene construction. In the current study, we leveraged the high temporal resolution of magnetoencephalography (MEG) to compare the neural responses to SD and SA objects while they were being used to build imagined scene representations, as this has not been examined before using neuroimaging. On each trial, participants gradually built a scene image from three successive auditorily-presented object descriptions and an imagined 3D space. We then examined the neural dynamics associated with the points during scene construction when either SD or SA objects were being imagined. We found that SD objects elicited theta changes relative to SA objects in two brain regions, the right ventromedial prefrontal cortex (vmPFC) and the right superior temporal gyrus (STG). Furthermore, using dynamic causal modeling, we observed that the vmPFC drove STG activity. These findings may indicate that SD objects serve to activate schematic and conceptual knowledge in vmPFC and STG upon which scene representations are then built.
Chun-Ting Hsu; Roy Clariana; Benjamin Schloss; Ping Li
Neurocognitive signatures of naturalistic reading of scientific texts: A fixation-related fMRI study Journal Article
In: Scientific Reports, vol. 9, pp. 10678, 2019.
How do students gain scientific knowledge while reading expository text? This study examines the underlying neurocognitive basis of textual knowledge structure and individual readers' cognitive differences and reading habits, including the influence of text and reader characteristics, on outcomes of scientific text comprehension. By combining fixation-related fMRI and multiband data acquisition, the study is among the first to consider self-paced naturalistic reading inside the MRI scanner. Our results revealed the underlying neurocognitive patterns associated with information integration of different time scales during text reading, and significant individual differences due to the interaction between text characteristics (e.g., optimality of the textual knowledge structure) and reader characteristics (e.g., electronic device use habits). Individual differences impacted the amount of neural resources deployed for multitasking and information integration for constructing the underlying scientific mental models based on the text being read. Our findings have significant implications for understanding science reading in a population that is increasingly dependent on electronic devices.
Ying Joey Zhou; Alexis Pérez-Bellido; Saskia Haegens; Floris P. Lange
Perceptual expectations modulate low-frequency activity: A statistical learning magnetoencephalographystudy Journal Article
In: Journal of Cognitive Neuroscience, pp. 1–12, 2019.
Perceptual expectations can change how a visual stimulus is perceived. Recent studies have shown mixed results in terms of whether expectations modulate sensory representations. Here, we used a statistical learning paradigm to study the temporal characteristics of perceptual expectations. We presented participants with pairs of object images organized in a predictive manner and then recorded their brain activity with magnetoencephalography while they viewed expected and unexpected image pairs on the subsequent day. We observed stronger alpha-band (7–14 Hz) activity in response to unexpected compared with expected object images. Specifically, the alpha-band modulation occurred as early as the onset of the stimuli and was most pronounced in left occipito-temporal cortex. Given that the differential response to expected versus unexpected stimuli occurred in sensory regions early in time, our results suggest that expectations modulate perceptual decision-making by changing the sensory response elicited by the stimuli.
Rotem Botvinik-Nezer; Roni Iwanir; Felix Holzmeister; Jürgen Huber; Magnus Johannesson; Michael Kirchler; Anna Dreber; Colin F. Camerer; Russell A. Poldrack; Tom Schonberg
fMRI data of mixed gambles from the Neuroimaging Analysis Replication and Prediction Study Journal Article
In: Scientific Data, vol. 6, pp. 106, 2019.
There is an ongoing debate about the replicability of neuroimaging research. It was suggested that one of the main reasons for the high rate of false positive results is the many degrees of freedom researchers have during data analysis. In the Neuroimaging Analysis Replication and Prediction Study (NARPS), we aim to provide the first scientific evidence on the variability of results across analysis teams in neuroscience. We collected fMRI data from 108 participants during two versions of the mixed gambles task, which is often used to study decision-making under risk. For each participant, the dataset includes an anatomical (T1 weighted) scan and fMRI as well as behavioral data from four runs of the task. The dataset is shared through OpenNeuro and is formatted according to the Brain Imaging Data Structure (BIDS) standard. Data pre-processed with fMRIprep and quality control reports are also publicly shared. This dataset can be used to study decision-making under risk and to test replicability and interpretability of previous results in the field.
Mariya E. Manahova; Eelke Spaak; Floris P. Lange
Familiarity increases processing speed in the visual system Journal Article
In: Journal of Cognitive Neuroscience, pp. 1–12, 2019.
Familiarity with a stimulus leads to an attenuated neural response to the stimulus. Alongside this attenuation, recent studies have also observed a truncation of stimulus-evoked activity for familiar visual input. One proposed function of this truncation is to rapidly put neurons in a state of readiness to respond to new input. Here, we examined this hypothesis by presenting human participants with target stimuli that were embedded in rapid streams of familiar or novel distractor stimuli at different speeds of presentation, while recording brain activity using magnetoencephalography and measuring behavioral performance. We investigated the temporal and spatial dynamics of signal truncation and whether this phenomenon bears relationship to participants' ability to categorize target items within a visual stream. Behaviorally, target categorization performance was markedly better when the target was embedded within familiar distractors, and this benefit became more pronounced with increasing speed of presentation. Familiar distractors showed a truncation of neural activity in the visual system. This truncation was strongest for the fastest presentation speeds and peaked in progressively more anterior cortical regions as presentation speeds became slower. Moreover, the neural response evoked by the target was stronger when this target was preceded by familiar distractors. Taken together, these findings demonstrate that item familiarity results in a truncated neural response, is associated with stronger processing of relevant target information, and leads to superior perceptual performance.
Jessica E. Goold; Wonil Choi; John M. Henderson
Cortical control of eye movements in natural reading: Evidence from MVPA Journal Article
In: Experimental Brain Research, vol. 237, no. 12, pp. 3099–3107, 2019.
Language comprehension during reading requires fine-grained management of saccadic eye movements. A critical question, therefore, is how the brain controls eye movements in reading. Neural correlates of simple eye movements have been found in multiple cortical regions, but little is known about how this network operates in reading. To investigate this question in the present study, participants were presented with normal text, pseudo-word text, and consonant string text in a magnetic resonance imaging (MRI) scanner with eyetracking. Participants read naturally in the normal text condition and moved their eyes “as if they were reading” in the other conditions. Multi-voxel pattern analysis was used to analyze the fMRI signal in the oculomotor network. We found that activation patterns in a subset of network regions differentiated between stimulus types. These results suggest that the oculomotor network reflects more than simple saccade generation and are consistent with the hypothesis that specific network areas interface with cognitive systems.
Benjamin T. Carter; Steven G. Luke
The effect of convolving word length, word frequency, function word predictability and first pass reading time in the analysis of a fixation-related fMRI dataset Journal Article
In: Data in Brief, vol. 25, pp. 1–21, 2019.
The data presented in this document was created to explore the effect of including or excluding word length, word frequency, the lexical predictability of function words and first pass reading time (or the duration of the first fixation on a word) as either baseline regressors or duration modulators on the final analysis for a fixation-related fMRI investigation of linguistic processing. The effect of these regressors was a central question raised during the review of Linguistic networks associated with lexical, semantic and syntactic predictability in reading: A fixation-related fMRI study . Three datasets were created and compared to the original dataset to determine their effect. The first examines the effect of adding word length and word frequency as baseline regressors. The second examines the effect of removing first pass reading time as a duration modulator. The third examines the inclusion of function word predictability into the baseline hemodynamic response function. Statistical maps were created for each dataset and compared to the primary dataset (published in ) across the linguistic conditions of the initial dataset (lexical predictability, semantic predictability or syntax predictability).
Kristin Koller; Christopher M. Hatton; Robert D. Rogers; Robert D. Rafal
Stria terminalis microstructure in humans predicts variability in orienting towards threat Journal Article
In: European Journal of Neuroscience, vol. 50, no. 11, pp. 3804–3813, 2019.
Current concepts of the extended amygdala posit that basolateral to central amygdala projections mediate fear-conditioned autonomic alerting, whereas projections to the bed nucleus of the stria terminalis mediate sustained anxiety. Using diffusion tensor imaging tractography in humans, we show that microstructure of the stria terminalis correlates with an orienting bias towards threat in a saccade decision task, providing the first evidence that this circuit supports decisions guiding evaluation of threatening stimuli.
Justin Riddle; Kai Hwang; Dillan Cellier; Sofia Dhanani; Mark D'esposito
Causal evidence for the role of neuronal oscillations in top–down and bottom–up attention Journal Article
In: Journal of Cognitive Neuroscience, vol. 31, no. 5, pp. 768–779, 2019.
Beta and gamma frequency neuronal oscillations have been implicated in top–down and bottom–up attention. In this study, we used rhythmic TMS to modulate ongoing beta and gamma frequency neuronal oscillations in frontal and parietal cortex while human participants performed a visual search task that manipulates bottom–up and top–down attention (single feature and conjunction search). Both task conditions will engage bottom–up attention processes, although the conjunction search condition will require more top–down attention. Gamma frequency TMS to superior precentral sulcus (sPCS) slowed saccadic RTs during both task conditions and induced a response bias to the contralateral visual field. In contrary, beta frequency TMS to sPCS and intraparietal sulcus decreased search accuracy only during the conjunction search condition that engaged more top–down attention. Furthermore, beta frequency TMS increased trial errors specifically when the target was in the ipsilateral visual field for the conjunction search condition. These results indicate that beta frequency TMS to sPCS and intraparietal sulcus disrupted top–down attention, whereas gamma frequency TMS to sPCS disrupted bottom–up, stimulus-driven attention processes. These findings provide causal evidence suggesting that beta and gamma oscillations have distinct functional roles for cognition.
Timothy H. Muller; Rogier B. Mars; Timothy E. Behrens; Jill X. O'Reilly
Control of entropy in neural models of environmental state Journal Article
In: eLife, vol. 8, pp. 1–30, 2019.
Humans and animals construct internal models of their environment in order to select appropriate courses of action. The representation of uncertainty about the current state of the environment is a key feature of these models that controls the rate of learning as well as directly affecting choice behaviour. To maintain flexibility, given that uncertainty naturally decreases over time, most theoretical inference models include a dedicated mechanism to drive up model uncertainty. Here we probe the long-standing hypothesis that noradrenaline is involved in determining the uncertainty, or entropy, and thus flexibility, of neural models. Pupil diameter, which indexes neuromodulatory state including noradrenaline release, predicted increases (but not decreases) in entropy in a neural state model encoded in human medial orbitofrontal cortex, as measured using multivariate functional MRI. Activity in anterior cingulate cortex predicted pupil diameter. These results provide evidence for top-down, neuromodulatory control of entropy in neural state models.
Jonathan F. O'rawe; Anna S. Huang; Daniel N. Klein; Hoi-Chung Leung
Posterior parietal influences on visual network specialization during development: An fMRI study of functional connectivity in children ages 9 to 12 Journal Article
In: Neuropsychologia, vol. 127, pp. 158–170, 2019.
Visual processing in the primate brain is highly organized along the ventral visual pathway, although it is still unclear how categorical selectivity emerges in this system. While many theories have attempted to explain the pattern of visual specialization within the ventral occipital and temporal areas, the biased connectivity hypothesis provides a framework which postulates extrinsic connectivity as a potential mechanism in shaping the development of category selectivity. As the posterior parietal cortex plays a central role in visual attention, we examined whether the pattern of parietal connectivity with the face and scene processing regions is closely linked with the functional properties of these two visually selective networks in a cohort of 60 children ages 9 to 12. Functionally localized face and scene selective regions were used in deriving each visual network's resting-state functional connectivity. The children's face and scene processing networks appeared to show a weak network segregation during resting state, which was confirmed when compared to that of a group of gender and handedness matched adults. Parietal regions of these children showed differential connectivity with the face and scene networks, and the extent of this differential parietal-visual connectivity predicted individual differences in the degree of segregation between the two visual networks, which in turn predicted individual differences in visual perception performance. Finally, the pattern of parietal connectivity with the face processing network also predicted the foci of face-related activation in the right fusiform gyrus across children. These findings provide evidence that extrinsic connectivity with regions such as the posterior parietal cortex may have important implications in the development of specialized visual processing networks.
Eduard Ort; Johannes J. Fahrenfort; Reshanne Reeder; Stefan Pollmann; Christian N. L. Olivers
Frontal cortex differentiates between free and imposed target selection in multiple-target search Journal Article
In: NeuroImage, vol. 202, pp. 116133, 2019.
Cognitive control can involve proactive (preparatory) and reactive (corrective) mechanisms. Using a gaze-contingent eye tracking paradigm combined with fMRI, we investigated the involvement of these different modes of control and their underlying neural networks, when switching between different targets in multiple-target search. Participants simultaneously searched for two possible targets presented among distractors, and selected one of them. In one condition, only one of the targets was available in each display, so that the choice was imposed, and reactive control would be required. In the other condition, both targets were present, giving observers free choice over target selection, and allowing for proactive control. Switch costs emerged only when targets were imposed and not when target selection was free. We found differential levels of activity in the frontoparietal control network depending on whether target switches were free or imposed. Furthermore, we observed core regions of the default mode network to be active during target repetitions, indicating reduced control on these trials. Free and imposed switches jointly activated parietal and posterior frontal cortices, while free switches additionally activated anterior frontal cortices. These findings highlight unique contributions of proactive and reactive control during visual search.
Abhijit Rajan; Sreenivasan Meyyappan; Harrison Walker; Immanuel Babu; Henry Samuel; Zhenhong Hu; Mingzhou Ding
Neural mechanisms of internal distraction suppression in visual attention Journal Article
In: Cortex, vol. 117, pp. 77–88, 2019.
When performing a demanding cognitive task, internal distraction in the form of task-irrelevant thoughts and mind wandering can shift our attention away from the task, negatively affecting task performance. Behaviorally, individuals with higher executive function indexed by higher working memory capacity (WMC) exhibit less mind wandering during cognitive tasks, but the underlying neural mechanisms are unknown. To address this problem, we recorded functional magnetic resonance imaging (fMRI) data from subjects performing a cued visual attention task, and assessed their WMC in a separate experiment. Applying machine learning and time-series analysis techniques, we showed that (1) higher WMC individuals experienced lower internal distraction through stronger suppression of posterior cingulate cortex (PCC) activity, (2) higher WMC individuals had better neural representations of attended information as evidenced by higher multivoxel decoding accuracy of cue-related activities in the dorsal attention network (DAN), (3) the positive relationship between WMC and DAN decoding accuracy was mediated by suppression of PCC activity, (4) the dorsal anterior cingulate (dACC) was a source of top-down signals that regulate PCC activity as evidenced by the negative association between Granger-causal influence dACC/PCC and PCC activity levels, and (5) higher WMC individuals exhibiting stronger dACC/PCC Granger-causal influence. These results shed light on the neural mechanisms underlying the executive suppression of internal distraction in tasks requiring externally oriented attention and provide an explanation of the individual differences in such suppression.
Birgit Rauchbauer; Bruno Nazarian; Morgane Bourhis; Magalie Ochs; Laurent Prévot; Thierry Chaminade
Brain activity during reciprocal social interaction investigated using conversational robots as control condition Journal Article
In: Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 374, pp. 1–8, 2019.
We present a novel functional magnetic resonance imaging paradigm for second-person neuroscience. The paradigm compares a human social interaction (human-human interaction, HHI) to an interaction with a conversational robot (human-robot interaction, HRI). The social interaction consists of 1 min blocks of live bidirectional discussion between the scanned participant and the human or robot agent. A final sample of 21 participants is included in the corpus comprising physiological (blood oxygen level-dependent, respiration and peripheral blood flow) and behavioural (recorded speech from all interlocutors, eye tracking from the scanned participant, face recording of the human and robot agents) data. Here, we present the first analysis of this corpus, contrasting neural activity between HHI and HRI. We hypothesized that independently of differences in behaviour between interactions with the human and robot agent, neural markers of mentalizing (temporoparietal junction (TPJ) and medial prefrontal cortex) and social motivation (hypothalamus and amygdala) would only be active in HHI. Results confirmed significantly increased response associated with HHI in the TPJ, hypothalamus and amygdala, but not in the medial prefrontal cortex. Future analysis of this corpus will include fine-grained characterization of verbal and non-verbal behaviours recorded during the interaction to investigate their neural correlates.
Ryan V. Raut; Anish Mitra; Abraham Z. Snyder; Marcus E. Raichle
On time delay estimation and sampling error in resting-state fMRI Journal Article
In: NeuroImage, vol. 194, pp. 211–227, 2019.
Accumulating evidence indicates that resting-state functional magnetic resonance imaging (rsfMRI) signals correspond to propagating electrophysiological infra-slow activity (<0.1 Hz). Thus, pairwise correlations (zero-lag functional connectivity (FC)) and temporal delays among regional rsfMRI signals provide useful, complementary descriptions of spatiotemporal structure in infra-slow activity. However, the slow nature of fMRI signals implies that practical scan durations cannot provide sufficient independent temporal samples to stabilize either of these measures. Here, we examine factors affecting sampling variability in both time delay estimation (TDE) and FC. Although both TDE and FC accuracy are highly sensitive to data quantity, we use surrogate fMRI time series to study how the former is additionally related to the magnitude of a given pairwise correlation and, to a lesser extent, the temporal sampling rate. These contingencies are further explored in real data comprising 30-min rsfMRI scans, where sampling error (i.e., limited accuracy owing to insufficient data quantity) emerges as a significant but underappreciated challenge to FC and, even more so, to TDE. Exclusion of high-motion epochs exacerbates sampling error; thus, both sides of the bias-variance (or data quality-quantity) tradeoff associated with data exclusion should be considered when analyzing rsfMRI data. Finally, we present strategies for TDE in motion-corrupted data, for characterizing sampling error in TDE and FC, and for mitigating the influence of sampling error on lag-based analyses.
Christiane S. Rohr; Dennis Dimond; Manuela Schuetze; Ivy Y. K. Cho; Limor Lichtenstein-Vidne; Hadas Okon-Singer; Deborah Dewey; Signe Bray
Girls' attentive traits associate with cerebellar to dorsal attention and default mode network connectivity Journal Article
In: Neuropsychologia, vol. 127, pp. 84–92, 2019.
Attention traits are a cornerstone to the healthy development of children's performance in the classroom, their interactions with peers, and in predicting future success and problems. The cerebellum is increasingly appreciated as a region involved in complex cognition and behavior, and moreover makes important connections to key brain networks known to support attention: the dorsal attention and default mode networks (DAN; DMN). The cerebellum has also been implicated in childhood disorders affecting attention, namely autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD), suggesting that attention networks extending to the cerebellum may be important to consider in relation to attentive traits. Yet, direct investigations into the association between cerebellar FC and attentive traits are lacking. Therefore, in this study we examined attentive traits, assessed using parent reports of ADHD and ASD symptoms, in a community sample of 52 girls aged 4–7 years, i.e. around the time of school entry, and their association with cerebellar connections with the DAN and DMN. We found that cortico-cerebellar functional connectivity (FC) jointly and differentially correlated with attentive traits, through a combination of weaker and stronger FC across anterior and posterior DAN and DMN nodes. These findings suggest that cortico-cerebellar integration may play an important role in the manifestation of attentive traits.
Pia Schröder; Timo Torsten Schmidt; Felix Blankenburg
Neural basis of somatosensory target detection independent of uncertainty, relevance, and reports Journal Article
In: eLife, vol. 8, pp. 1–19, 2019.
Research on somatosensory awareness has yielded highly diverse findings with putative neural correlates ranging from activity within somatosensory cortex to activation of widely distributed frontoparietal networks. Divergent results from previous studies may reside in cognitive processes that often coincide with stimulus awareness in experimental settings. To scrutinise the specific relevance of regions implied in the target detection network, we used functional magnetic resonance imaging (n = 27) on a novel somatosensory detection task that explicitly controls for stimulus uncertainty, behavioural relevance, overt reports, and motor responses. Using Bayesian Model Selection, we show that responses reflecting target detection are restricted to secondary somatosensory cortex, whereas activity in insular, cingulate, and motor regions is best explained in terms of stimulus uncertainty and overt reports. Our results emphasise the role of sensory-specific cortex for the emergence of perceptual awareness and dissect the contribution of the frontoparietal network to classical detection tasks.
Sarah E. Schwettmann; Joshua B. Tenenbaum; Nancy Kanwisher
Invariant representations of mass in the human brain Journal Article
In: eLife, vol. 8, pp. 1–26, 2019.
An intuitive understanding of physical objects and events is critical for successfully interacting with the world. Does the brain achieve this understanding by running simulations in a mental physics engine, which represents variables such as force and mass, or by analyzing patterns of motion without encoding underlying physical quantities? To investigate, we scanned participants with fMRI while they viewed videos of objects interacting in scenarios indicating their mass. Decoding analyses in brain regions previously implicated in intuitive physical inference revealed mass representations that generalized across variations in scenario, material, friction, and motion energy. These invariant representations were found during tasks without action planning, and tasks focusing on an orthogonal dimension (object color). Our results support an account of physical reasoning where abstract physical variables serve as inputs to a forward model of dynamics, akin to a physics engine, in parietal and frontal cortex.
Michael J. Spilka; Daniel J. Pittman; Signe L. Bray; Vina M. Goghari
Manipulating visual scanpaths during facial emotion perception modulates functional brain activation in schizophrenia patients and controls Journal Article
In: Journal of Abnormal Psychology, vol. 128, no. 8, pp. 855–866, 2019.
Individuals with schizophrenia exhibit deficits in facial emotion processing, which have been associated with abnormalities in visual gaze behavior and functional brain activation. However, the relationship between gaze behavior and brain activation in schizophrenia remains unexamined. Studies in healthy individuals and other clinical samples indicate a relationship between gaze behavior and functional activation in brain regions implicated in facial emotion processing deficits in schizophrenia (e.g., fusiform gyrus), prompting the question of whether a similar relationship exists in schizophrenia. This study examined whether manipulating visual scanpaths during facial emotion perception would modulate functional brain activation in a sample of 23 schizophrenia patients and 26 community controls. Participants underwent functional magnetic resonance imaging (MRI) while viewing pictures of emotional faces. During the typical viewing condition, a fixation cue directed participants' gaze primarily to the eyes and mouth, whereas during the atypical viewing condition gaze was directed to peripheral features. Both viewing conditions elicited a robust response throughout face-processing regions. Typical viewing led to greater activation in visual association cortex including the right inferior occipital gyrus/occipital face area, whereas atypical viewing elicited greater activation in primary visual cortex and regions involved in attentional control. There were no between-groups activation differences in response to faces or interaction between group and gaze manipulation. The results indicate that gaze behavior modulates functional activation in early face-processing regions in individuals with and without schizophrenia, suggesting that abnormal gaze behavior in schizophrenia may contribute to activation abnormalities during facial emotion perception.
Gabor Stefanics; Klaas Enno Stephan; Jakob Heinzle
Feature-specific prediction errors for visual mismatch Journal Article
In: NeuroImage, vol. 196, pp. 142–151, 2019.
Predictive coding (PC) theory posits that our brain employs a predictive model of the environment to infer the causes of its sensory inputs. A fundamental but untested prediction of this theory is that the same stimulus should elicit distinct precision weighted prediction errors (pwPEs) when different (feature-specific) predictions are violated, even in the absence of attention. Here, we tested this hypothesis using functional magnetic resonance imaging (fMRI) and a multi-feature roving visual mismatch paradigm where rare changes in either color (red, green), or emotional expression (happy, fearful) of faces elicited pwPE responses in human participants. Using a computational model of learning and inference, we simulated pwPE and prediction trajectories of a Bayes-optimal observer and used these to analyze changes in blood oxygen level dependent (BOLD) responses to changes in color and emotional expression of faces while participants engaged in a distractor task. Controlling for visual attention by eye-tracking, we found pwPE responses to unexpected color changes in the fusiform gyrus. Conversely, unexpected changes of facial emotions elicited pwPE responses in cortico-thalamo-cerebellar structures associated with emotion and theory of mind processing. Predictions pertaining to emotions activated fusiform, occipital and temporal areas. Our results are consistent with a general role of PC across perception, from low-level to complex and socially relevant object features, and suggest that monitoring of the social environment occurs continuously and automatically, even in the absence of attention.
Raphael Vallat; David Meunier; Alain Nicolas; Perrine Ruby
Hard to wake up? The cerebral correlates of sleep inertia assessed using combined behavioral, EEG and fMRI measures Journal Article
In: NeuroImage, vol. 184, pp. 266–278, 2019.
The first minutes following awakening from sleep are typically marked by reduced vigilance, increased sleepiness and impaired performance, a state referred to as sleep inertia. Although the behavioral aspects of sleep inertia are well documented, its cerebral correlates remain poorly understood. The present study aimed at filling this gap by measuring in 34 participants the changes in behavioral performance (descending subtraction task, DST), EEG spectral power, and resting-state fMRI functional connectivity across three time points: before an early-afternoon 45-min nap, 5 min after awakening from the nap and 25 min after awakening. Our results showed impaired performance at the DST at awakening and an intrusion of sleep-specific features (spectral power and functional connectivity) into wakefulness brain activity, the intensity of which was dependent on the prior sleep duration and depth for the functional connectivity (14 participants awakened from N2 sleep, 20 from N3 sleep). Awakening in N3 (deep) sleep induced the most robust changes and was characterized by a global loss of brain functional segregation between task-positive (dorsal attention, salience, sensorimotor) and task-negative (default mode) networks. Significant correlations were observed notably between the EEG delta power and the functional connectivity between the default and dorsal attention networks, as well as between the percentage of mistake at the DST and the default network functional connectivity. These results highlight (1) significant correlations between EEG and fMRI functional connectivity measures, (2) significant correlations between the behavioral aspect of sleep inertia and measures of the cerebral functioning at awakening (both EEG and fMRI), and (3) the important difference in the cerebral underpinnings of sleep inertia at awakening from N2 and N3 sleep.
Rozemarijn S. Kleef; Claudi L. H. Bockting; Evelien Valen; André Aleman; Jan Bernard C. Marsman; Marie José Tol
Neurocognitive working mechanisms of the prevention of relapse in remitted recurrent depression (NEWPRIDE): Protocol of a randomized controlled neuroimaging trial of preventive cognitive therapy Journal Article
In: BMC Psychiatry, vol. 19, pp. 1–11, 2019.
Background: Major Depressive Disorder (MDD) is a psychiatric disorder with a highly recurrent character, making prevention of relapse an important clinical goal. Preventive Cognitive Therapy (PCT) has been proven effective in preventing relapse, though not for every patient. A better understanding of relapse vulnerability and working mechanisms of preventive treatment may inform effective personalized intervention strategies. Neurocognitive models of MDD suggest that abnormalities in prefrontal control over limbic emotion-processing areas during emotional processing and regulation are important in understanding relapse vulnerability. Whether changes in these neurocognitive abnormalities are induced by PCT and thus play an important role in mediating the risk for recurrent depression, is currently unclear. In the Neurocognitive Working Mechanisms of the Prevention of Relapse In Depression (NEWPRIDE) study, we aim to 1) study neurocognitive factors underpinning the vulnerability for relapse, 2) understand the neurocognitive working mechanisms of PCT, 3) predict longitudinal treatment effects based on pre-treatment neurocognitive characteristics, and 4) validate the pupil dilation response as a marker for prefrontal activity, reflecting emotion regulation capacity and therapy success. Methods: In this randomized controlled trial, 75 remitted recurrent MDD (rrMDD) patients will be included. Detailed clinical and cognitive measurements, fMRI scanning and pupillometry will be performed at baseline and three-month follow-up. In the interval, 50 rrMDD patients will be randomized to eight sessions of PCT and 25 rrMDD patients to a waiting list. At baseline, 25 healthy control participants will be additionally included to objectify cross-sectional residual neurocognitive abnormalities in rrMDD. After 18 months, clinical assessments of relapse status are performed to investigate which therapy induced changes predict relapse in the 50 patients allocated to PCT. Discussion: The present trial is the first to study the neurocognitive vulnerability factors underlying relapse and mediating relapse prevention, their value for predicting PCT success and whether pupil dilation acts as a valuable marker in this regard. Ultimately, a deeper understanding of relapse prevention could contribute to the development of better targeted preventive interventions. Trial registration: Trial registration: Netherlands Trial Register, August 18, 2015, trial number NL5219.
Chayenne Van Meel; Annelies Baeck; Céline R. Gillebert; Johan Wagemans; Hans P. Op de Beeck
The representation of symmetry in multi-voxel response patterns and functional connectivity throughout the ventral visual stream Journal Article
In: NeuroImage, vol. 191, pp. 216–224, 2019.
Several computational models explain how symmetry might be detected and represented in the human brain. However, while there is an abundance of psychophysical studies on symmetry detection and several neural studies showing where and when symmetry is detected in the brain, important questions remain about how this detection happens and how symmetric patterns are represented. We studied the representation of (vertical) symmetry in regions of the ventral visual stream, using multi-voxel pattern analyses (MVPA) and functional connectivity analyses. Our results suggest that neural representations gradually change throughout the ventral visual stream, from very similar part-based representations for symmetrical and asymmetrical stimuli in V1 and V2, over increasingly different representations for symmetrical and asymmetrical stimuli which are nevertheless still part-based in both V3 and V4, to a more holistic representation for symmetrical compared to asymmetrical stimuli in high-level LOC. This change in representations is accompanied by increased communication between left and right retinotopic areas, evidenced by higher interhemispheric functional connectivity during symmetry perception in areas V2 and V4.
Sonja Well; John P. O'Doherty; Frans Winden
Relief from incidental fear evokes exuberant risk taking Journal Article
In: PLoS ONE, vol. 14, no. 1, pp. e0211018, 2019.
Incidental emotions are defined as feelings that are unrelated to a decision task at hand and thereby not normatively relevant for making choices. The precise influence and formal theoretical implications of incidental emotions regarding financial risk taking are still largely unclear. An effect of incidental emotion on decision-making would challenge the main extant formal theoretical economic models because such models do not allow for an effect of incidental emotions. As financial risk taking is pervasive in modern economies, the role of incidental emotions is an important issue. The goal of this experimental study is threefold. First, we examine the impact of incidental fear on the choice between a sure and a risky monetary option. A well-validated method of fear induction, using electric shocks, is employed for that purpose. Based on emotion studies we hypothesize less risk taking under fear and more risk taking when relieved of fear. Our second goal is to investigate the relative performance of the main existing formal theoretical economic models (based on Expected Utility Theory, Prospect Theory, or the Mean-Variance model) in explaining the behavioral data. We also investigate how these models can be adjusted to accommodate any observed influence of incidental emotion. For that reason, we first theoretically model the potential pathways of incidental fear (and the relief thereof) via the valuation of the choice option rewards or risk-assessment. We then estimate the relevant parameters allowing for both additive as well as interactive effects. Our third and final goal is to explore the neural basis of any observed influence of incidental emotions on decision-making by means of a model-based fMRI analysis, using the findings of existing neuroeconomic studies as the basis for our hypotheses. Our results indicate that the relief of fear can give a substantial boost to financial risk taking (suggestive of exuberance). This impact is best captured by Prospect Theory if we allow for an increase in participants' valuation of option outcomes when relieved of fear. Moreover, this impact is manifested at the neural level by the activity of the ventromedial prefrontal cortex (vmPFC), a brain area widely regarded as being central for valuation.
Maryam Vaziri-Pashkam; Yaoda Xu
An Information-Driven 2-Pathway Characterization of Occipitotemporal and Posterior Parietal Visual Object Representations Journal Article
In: Cerebral Cortex, vol. 29, no. 5, pp. 2034–2050, 2019.
Recent studies have demonstrated the existence of rich visual representations in both occipitotemporal cortex (OTC) and posterior parietal cortex (PPC). Using fMRI decoding and a bottom-up data-driven approach, we showed that although robust object category representations exist in both OTC and PPC, there is an information-driven 2-pathway separation among these regions in the representational space, with occipitotemporal regions arranging hierarchically along 1 pathway and posterior parietal regions along another pathway. We obtained 10 independent replications of this 2-pathway distinction, accounting for 58-81% of the total variance of the region-wise differences in visual representation. The separation of the PPC regions from higher occipitotemporal regions was not driven by a difference in tolerance to changes in low-level visual features, did not rely on the presence of special object categories, and was present whether or not object category was task relevant. Our information-driven 2-pathway structure differs from the well-known ventral-what and dorsal-where/how characterization of posterior brain regions. Here both pathways contain rich nonspatial visual representations. The separation we see likely reflects a difference in neural coding scheme used by PPC to represent visual information compared with that of OTC.
Lorenzo Vignali; Stefan Hawelka; Florian Hutzler; Fabio Richlan
Processing of parafoveally presented words. An fMRI study Journal Article
In: NeuroImage, vol. 184, pp. 1–9, 2019.
The present fMRI study investigated neural correlates of parafoveal preprocessing during reading and the type of information that is accessible from the upcoming - not yet fixated - word. Participants performed a lexical decision flanker task while the constraints imposed by the first three letters (the initial trigram) of parafoveally presented words were controlled. Behavioral results evidenced that the amount of information extracted from parafoveal stimuli, was affected by the difficulty of the foveal stimulus. Easy to process foveal stimuli (i.e., high frequency nouns) allowed parafoveal information to be extracted up to the lexical level. Conversely, when foveal stimuli were difficult to process (orthographically legal nonwords) only constraining trigrams modulated the task performance. Neuroimaging findings showed no effects of lexicality (i.e., difference between words and pseudowords) in the parafovea independently from the difficulty of the foveal stimulus. The constraints imposed by the initial trigrams, however, modulated the hemodynamic response in the left supramarginal gyrus. We interpreted the supramarginal activation as reflecting sublexical (phonological) processes. The missing parafoveal lexicality effect was discussed in relation to findings of experiments which observed effects of parafoveal semantic congruency on electrophysiological correlates.
Katharina Voigt; Carsten Murawski; Sebastian Speer; Stefan Bode
Hard decisions shape the neural coding of preferences Journal Article
In: Journal of Neuroscience, vol. 39, no. 4, pp. 718–726, 2019.
Hard decisions between equally valued alternatives can result in preference changes, meaning that subsequent valuations for chosen items increaseanddecrease for rejected items. Previous research suggests that thisphenomenon is aconsequenceofcognitive dissonance reduction after the decision, induced by the mismatch between initial preferences and decision outcomes. In contrast, this functional magnetic resonance imaging and eye-tracking study with male and female human participants found that preferences are already updated online during the process of decision-making. Preference changes were predicted from activity in left dorsolateral prefrontal cortexandprecuneus whilemakinghard decisions. Fixation durations during this phase predicted both choice outcomesandsubsequent preference changes. These preference adjustments became behaviorally relevant only for choices that were rememberedand were in turn associated with hippocampus activity. Our results suggest that preferences evolve dynamically as decisions arise, potentially as a mechanism to prevent stalemate situations in underdetermined decision scenarios.
Eelke Vries; Daniel Baldauf
Attentional weighting in the face processing network: A magnetic response image-guided magnetoencephalography study using multiple cyclic entrainments Journal Article
In: Journal of Cognitive Neuroscience, vol. 31, no. 10, pp. 1573–1588, 2019.
We recorded magnetoencephalography using a neural entrainment paradigm with compound face stimuli that allowed for entraining the processing of various parts of a face (eyes, mouth) as well as changes in facial identity. Our magnetic response image-guided magnetoencephalography analyses revealed that different subnodes of the human face processing network were entrained differentially according to their functional specialization. Whereas the occipital face area was most responsive to the rate at which face parts (e.g., the mouth) changed, and face patches in the STS were mostly entrained by rhythmic changes in the eye region, the fusiform face area was the only subregion that was strongly entrained by the rhythmic changes in facial identity. Furthermore, top–down attention to the mouth, eyes, or identity of the face selectively modulated the neural processing in the respective area (i.e., occipital face area, STS, or fusiform face area), resembling behavioral cue validity effects observed in the participants' RT and detection rate data. Our results show the attentional weighting of the visual processing of different aspects and dimensions of a single face object, at various stages of the involved visual processing hierarchy.
Liping Wang; Marie Amalric; Wen Fang; Xinjian Jiang; Christophe Pallier; Santiago Figueira; Mariano Sigman; Stanislas Dehaene
Representation of spatial sequences using nested rules in human prefrontal cortex Journal Article
In: NeuroImage, vol. 186, pp. 245–255, 2019.
Memory for spatial sequences does not depend solely on the number of locations to be stored, but also on the presence of spatial regularities. Here, we show that the human brain quickly stores spatial sequences by detecting geometrical regularities at multiple time scales and encoding them in a format akin to a programming language. We measured gaze-anticipation behavior while spatial sequences of variable regularity were repeated. Participants' behavior suggested that they quickly discovered the most compact description of each sequence in a language comprising nested rules, and used these rules to compress the sequence in memory and predict the next items. Activity in dorsal inferior prefrontal cortex correlated with the amount of compression, while right dorsolateral prefrontal cortex encoded the presence of embedded structures. Sequence learning was accompanied by a progressive differentiation of multi-voxel activity patterns in these regions. We propose that humans are endowed with a simple “language of geometry” which recruits a dorsal prefrontal circuit for geometrical rules, distinct from but close to areas involved in natural language processing.
Joseph C. Griffis; Nicholas V. Metcalf; Maurizio Corbetta; Gordon L. Shulman
Structural disconnections explain brain network dysfunction after stroke Journal Article
In: Cell Reports, vol. 28, no. 10, pp. 2527–2540, 2019.
Stroke causes focal brain lesions that disrupt functional connectivity (FC), a measure of activity synchronization, throughout distributed brain networks. It is often assumed that FC disruptions reflect damage to specific cortical regions. However, an alternative explanation is that they reflect the structural disconnection (SDC) of white matter pathways. Here, we compare these explanations using data from 114 stroke patients. Across multiple analyses, we find that SDC measures outperform focal damage measures, including damage to putative critical cortical regions, for explaining FC disruptions associated with stroke. We also identify a core mode of structure-function covariation that links the severity of interhemispheric SDCs to widespread FC disruptions across patients and that correlates with deficits in multiple behavioral domains. We conclude that a lesion's impact on the structural connectome is what determines its impact on FC and that interhemispheric SDCs may play a particularly important role in mediating FC disruptions after stroke.
Christoph Helmchen; Matthias Rother; Andreas Sprenger
Increased brain responsivity to galvanic vestibular stimulation in bilateral vestibular failure Journal Article
In: NeuroImage: Clinical, vol. 24, pp. 101942, 2019.
In this event-related functional magnetic resonance imaging (fMRI) study we investigated how the brain of patients with bilateral vestibular failure (BVF) responds to vestibular stimuli. We used imperceptible noisy galvanic vestibular stimulation (GVS) and perceptible bi-mastoidal GVS intensities and related the corresponding brain activity to the evoked motion perception. In contrast to caloric irrigation, GVS stimulates the vestibular organ at its potentially intact afferent nerve site. Motion perception thresholds and cortical responses were compared between 26 BVF patients to 27 age-matched healthy control participants. To identify the specificity of vestibular cortical responses we used a parametric design with different stimulus intensities (noisy imperceptible, low perceptible, high perceptible) allowing region-specific stimulus response functions. In a 2 × 3 flexible factorial design all GVS-related brain activities were contrasted with a sham condition that did not evoke perceived motion. Patients had a higher motion perception threshold and rated the vestibular stimuli higher than the healthy participants. There was a stimulus intensity related and region-specific increase of activity with steep stimulus response functions in parietal operculum (e.g. OP2), insula, superior temporal gyrus, early visual cortices (V3) and cerebellum while activity in the hippocampus and intraparietal sulcus did not correlate with vestibular stimulus intensity. Using whole brain analysis, group comparisons revealed increased brain activity in early visual cortices (V3) and superior temporal gyrus of patients but there was no significant interaction, i.e. stimulus response function in these regions were still similar in both groups. Brain activity in these regions during (high)GVS increased with higher dizziness-related handicap scores but was not related to the degree of vestibular impairment or disease duration. nGVS did not evoke cortical responses in any group. Our data indicate that perceptible GVS-related cortical responsivity is not diminished but increased in mul-tisensory (visual-vestibular) cortical regions despite bilateral failure of the peripheral vestibular organ. The increased activity in early visual cortices (V3) and superior temporal gyrus of BVF patients has several potential implications: (i) their cortical reciprocal inhibitory visuo-vestibular interaction is dysfunctional, (ii) it may contribute to the visual dependency of BVF patients, and (iii) it needs to be considered when BVF patients receive peripheral vestibular stimulation devices, e.g. vestibular implants or portable GVS devices. Imperceptible nGVS did not elicit cortical brain responses making it unlikely that the reported balance improvement of BVF by nGVS is mediated by cortical mechanisms.
Linda Henriksson; Marieke Mur; Nikolaus Kriegeskorte
Rapid invariant encoding of scene layout in human OPA Journal Article
In: Neuron, vol. 103, no. 1, pp. 161–171.e3, 2019.
Successful visual navigation requires a sense of the geometry of the local environment. How do our brains extract this information from retinal images? Here we visually presented scenes with all possible combinations of five scene-bounding elements (left, right, and back walls; ceiling; floor) to human subjects during functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG). The fMRI response patterns in the scene-responsive occipital place area (OPA) reflected scene layout with invariance to changes in surface texture. This result contrasted sharply with the primary visual cortex (V1), which reflected low-level image features of the stimuli, and the parahippocampal place area (PPA), which showed better texture than layout decoding. MEG indicated that the texture-invariant scene layout representation is computed from visual input within ∼100 ms, suggesting a rapid computational mechanism. Taken together, these results suggest that the cortical representation underlying our instant sense of the environmental geometry is located in the OPA.
Anna E. Hughes; John A. Greenwood; Nonie J. Finlayson; D. Samuel Schwarzkopf
Population receptive field estimates for motion-defined stimuli Journal Article
In: NeuroImage, vol. 199, pp. 245–260, 2019.
The processing of motion changes throughout the visual hierarchy, from spatially restricted ‘local motion' in early visual cortex to more complex large-field ‘global motion' at later stages. Here we used functional magnetic resonance imaging (fMRI) to examine spatially selective responses in these areas related to the processing of random-dot stimuli defined by differences in motion. We used population receptive field (pRF) analyses to map retinotopic cortex using bar stimuli comprising coherently moving dots. In the first experiment, we used three separate background conditions: no background dots (dot-defined bar-only), dots moving coherently in the opposite direction to the bar (kinetic boundary) and dots moving incoherently in random directions (global motion). Clear retinotopic maps were obtained for the bar-only and kinetic-boundary conditions across visual areas V1–V3 and in higher dorsal areas. For the global-motion condition, retinotopic maps were much weaker in early areas and became clear only in higher areas, consistent with the emergence of global-motion processing throughout the visual hierarchy. However, in a second experiment we demonstrate that this pattern is not specific to motion-defined stimuli, with very similar results for a transparent-motion stimulus and a bar defined by a static low-level property (dot size) that should have driven responses particularly in V1. We further exclude explanations based on stimulus visibility by demonstrating that the observed differences in pRF properties do not follow the ability of observers to localise or attend to these bar elements. Rather, our findings indicate that dorsal extrastriate retinotopic maps may primarily be determined by the visibility of the neural responses to the bar relative to the background response (i.e. neural signal-to-noise ratios) and suggests that claims about stimulus selectivity from pRF experiments must be interpreted with caution.
Andreas Jarvstad; Iain D. Gilchrist
Cognitive control of saccadic selection and inhibition from within the core cortical saccadic network Journal Article
In: Journal of Neuroscience, vol. 39, no. 13, pp. 2497–2508, 2019.
The ability to select the task-relevant stimulus for a saccadic eye movement, while inhibiting saccades to task-irrelevant stimuli, is crucial for active vision. Here, we present a novel saccade-contingent behavioral paradigm and investigate the neural basis of the central cognitive functions underpinning such behavior, saccade selection, saccade inhibition, and saccadic choice, in female and male human participants. The paradigm allows for exceptionally well-matched contrasts, with task demands formalized with stochastic accumulation-to-threshold models. Using fMRI, we replicated the core cortical eye-movement network for saccade generation (frontal eye fields, posterior parietal cortex, and higher-level visual areas). However, in contrast to previously published tasks, saccadic selection and inhibition recruited only this core network. Brain-behavior analyses further showed that inhibition efficiency may be underpinned by white-matter integrity of tracts between key saccade-generating regions, and that inhibition efficiency is associated with right inferior frontal gyrus engagement, potentially implementing general-purpose inhibition. The core network, however, was insufficient for saccadic choice, which recruited anterior regions commonly attributed to saccadic action selection, including dorsolateral prefrontal cortex and anterior cingulate cortex. Jointly, the results indicate that extra-saccadic activity observed for free choice, and in previously published tasks probing saccadic control, is likely due to increased load on higher-level cognitive processes, and not saccadic selection per se, which is achieved within the canonical cortical eye movement network.
Philip A. Kragel; Marianne C. Reddan; Kevin S. LaBar; Tor D. Wager
Emotion schemas are embedded in the human visual system Journal Article
In: Science Advances, vol. 5, no. 7, pp. eaaw4358, 2019.
Theorists have suggested that emotions are canonical responses to situations ancestrally linked to survival. If so, then emotions may be afforded by features of the sensory environment. However, few computational models describe how combinations of stimulus features evoke different emotions. Here, we develop a convolutional neural network that accurately decodes images into 11 distinct emotion categories. We validate the model using more than 25,000 images and movies and show that image content is sufficient to predict the category and valence of human emotion ratings. In two functional magnetic resonance imaging studies, we demonstrate that patterns of human visual cortex activity encode emotion category–related model output and can decode multiple categories of emotional experience. These results suggest that rich, category-specific visual features can be reliably mapped to distinct emotions, and they are coded in distributed representations within the human visual system.
Milosz Krala; Bianca Kemenade; Benjamin Straube; Tilo Kircher; Frank Bremmer
Predictive coding in a multisensory path integration task: An fMRI study Journal Article
In: Journal of vision, vol. 19, no. 11, pp. 1–15, 2019.
During self-motion through an environment, our sensory systems are confronted with a constant flow of information from different modalities. To successfully navigate, self-induced sensory signals have to be dissociated from externally induced sensory signals. Previous studies have suggested that the processing of self-induced sensory information is modulated by means of predictive coding mechanisms. However, the neural correlates of processing self-induced sensory information from different modalities during self-motion are largely unknown. Here, we asked if and how the processing of visually simulated self-motion and/or associated auditory stimuli is modulated by self-controlled action. Participants were asked to actively reproduce a previously observed simulated self-displacement (path integration). Blood oxygen level-dependent (BOLD) activation during this path integration was compared with BOLD activation during a condition in which we passively replayed the exact sensory stimulus that had been produced by the participants in previous trials. We found supramodal BOLD suppression in parietal and frontal regions. Remarkably, BOLD contrast in sensory areas was enhanced in a modality-specific manner. We conclude that the effect of action on sensory processing is strictly dependent on the respective behavioral task and its relevance.
Satwant Kumar; Ivo D. Popivanov; Rufin Vogels
Transformation of visual representations across ventral stream body-selective patches Journal Article
In: Cerebral Cortex, vol. 29, no. 1, pp. 215–229, 2019.
Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex.
Hai Lin; Wei-ping Li; Synnöve Carlson
A privileged working memory state and potential top-down modulation for faces, not scenes Journal Article
In: Frontiers in Human Neuroscience, vol. 13, pp. 2, 2019.
Top-down modulation is engaged during multiple stages of working memory (WM), including expectation, encoding, and maintenance. During WM maintenance period, an “incidental cue” can bring one of the two items into a privileged state and make the privileged item be recalled with higher precision, despite being irrelevant to which one to be probed as the target. With regard to the different representational states of WM, it's unclear whether there is top-down modulation on earth sensory cortical areas. Here, We used this behavioral paradigm of “incidental cue” and event-related fMRI to investigate whether there were a privileged WM state and top-down modulation for complex stimuli including faces and natural scenes. We found that faces, not scenes, could enter into the privileged state with improved accuracy and response time of WM task. Meanwhile, cue-driven baseline activity shifts in fusiform face area (FFA) were identified by univariate analysis in the recognition of privileged faces, compared to that of non-privileged ones. In addition, the functional connectivity between FFA and right inferior frontal junction (IFJ), middle frontal gyrus (MFG), inferior frontal gyrus, right intraparietal sulcus (IPS), right precuneus and supplementary motor area was significantly enhanced, corresponding to the improved WM performance. Moreover, FFA connectivity with IFJ and IPS could predict WM improvements. These findings indicated that privileged WM state and potential top-down modulation existed for faces, but not scenes, during WM maintenance period.
Sahil Luthra; Sara Guediche; Sheila E. Blumstein; Emily B. Myers
Neural substrates of subphonemic variation and lexical competition in spoken word recognition Journal Article
In: Language, Cognition and Neuroscience, vol. 34, no. 2, pp. 151–169, 2019.
In spoken word recognition, subphonemic variation influences lexical activation, with sounds near a category boundary increasing phonetic competition as well as lexical competition. The current study investigated the interplay of these factors using a visual world task in which participants were instructed to look at a picture of an auditory target (e.g. peacock). Eyetracking data indicated that participants were slowed when a voiced onset competitor (e.g. beaker) was also displayed, and this effect was amplified when acoustic-phonetic competition was increased. Simultaneously-collected fMRI data showed that several brain regions were sensitive to the presence of the onset competitor, including the supramarginal, middle temporal, and inferior frontal gyri, and functional connectivity analyses revealed that the coordinated activity of left frontal regions depends on both acoustic-phonetic and lexical factors. Taken together, results suggest a role for frontal brain structures in resolving lexical competition, particularly as atypical acoustic-phonetic information maps on to the lexicon.
Charles R. Marshall; Christopher J. D. Hardy; Lucy L. Russell; Rebecca L. Bond; Harri Sivasathiaseelan; Caroline Greaves; Katrina M. Moore; Jennifer L. Agustus; Janneke E. P. Leeuwen; Stephen J. Wastling; Jonathan D. Rohrer; James M. Kilner; Jason D. Warren
The functional neuroanatomy of emotion processing in frontotemporal dementias Journal Article
In: Brain, vol. 142, no. 9, pp. 2873–2887, 2019.
Impaired processing of emotional signals is a core feature of frontotemporal dementia syndromes, but the underlying neural mechanisms have proved challenging to characterize and measure. Progress in this field may depend on detecting functional changes in the working brain, and disentangling components of emotion processing that include sensory decoding, emotion categorization and emotional contagion. We addressed this using functional MRI of naturalistic, dynamic facial emotion processing with concurrent indices of autonomic arousal, in a cohort of patients representing all major frontotemporal dementia syndromes relative to healthy age-matched individuals. Seventeen patients with behavioural variant frontotemporal dementia [four female; mean (standard deviation) age 64.8 (6.8) years], 12 with semantic variant primary progressive aphasia [four female; 66.9 (7.0) years], nine with non-fluent variant primary progressive aphasia [five female; 67.4 (8.1) years] and 22 healthy controls [12 female; 68.6 (6.8) years] passively viewed videos of universal facial expressions during functional MRI acquisition, with simultaneous heart rate and pupillometric recordings; emotion identification accuracy was assessed in a post-scan behavioural task. Relative to healthy controls, patient groups showed significant impairments (analysis of variance models, all P 5 0.05) of facial emotion identification (all syndromes) and cardiac (all syndromes) and pupillary (non-fluent variant only) reactivity. Group-level functional neuroanatomical changes were assessed using statistical parametric mapping, thresholded at P 5 0.05 after correction for multiple comparisons over the whole brain or within pre-specified regions of interest. In response to viewing facial expressions, all participant groups showed comparable activation of primary visual cortex while patient groups showed differential hypo-activation of fusiform and posterior temporo-occipital junctional cortices. Bi-hemispheric, syndrome-specific activations predicting facial emotion identification performance were identified (behavioural variant, anterior insula and caudate; semantic variant, anterior temporal cortex; non-fluent variant, frontal operculum). The semantic and non-fluent variant groups additionally showed complex profiles of central parasympathetic and sympathetic autonomic involvement that overlapped signatures of emotional visual and categorization processing and extended (in the non-fluent group) to brainstem effector pathways. These findings open a window on the functional cerebral mechanisms underpinning complex socio-emotional phenotypes of frontotemporal dementia, with implications for novel physiological biomarker development.
Rasmus M. Birn; Alexander K. Converse; Abigail Z. Rajala; Andrew L. Alexander; Walter F. Block; Alan B. McMillan; Bradley T. Christian; Caitlynn N. Filla; Dhanabalan Murali; Samuel A. Hurley; Rick L. Jenison; Luis C. Populin
Changes in endogenous dopamine induced by methylphenidate predict functional connectivity in nonhuman primates Journal Article
In: Journal of Neuroscience, vol. 39, no. 8, pp. 1436–1444, 2019.
Dopamine (DA) levels in the striatum are increased by many therapeutic drugs, such as methylphenidate (MPH), which also alters behavioral and cognitive functions thought to be controlled by the PFC dose-dependently. We linked DA changes and functional connectivity (FC) using simultaneous [18F]fallypride PET and resting-state fMRI in awake male rhesus monkeys after oral administration of various doses of MPH. We found a negative correlation between [18F]fallypride nondisplaceable binding potential (BPND) and MPH dose in the head of the caudate (hCd), demonstrating increased extracellular DA resulting from MPH administration. The decreased BPND was negatively correlated with FC between the hCd and the PFC. Subsequent voxelwise analyses revealed negative correlations with FC between the hCd and the dorsolateral PFC, hippocampus, and precuneus. These results, showing that MPH-induced changes in DA levels in the hCd predict resting-state FC, shed light on a mechanism by which changes in striatal DA could influence function in the PFC.
Ilona M. Bloem; Sam Ling
Normalization governs attentional modulation within human visual cortex Journal Article
In: Nature Communications, vol. 10, pp. 5660, 2019.
Although attention is known to increase the gain of visuocortical responses, its underlying neural computations remain unclear. Here, we use fMRI to test the hypothesis that a neural population's ability to be modulated by attention is dependent on divisive normalization. To do so, we leverage the feature-tuned properties of normalization and find that visuocortical responses to stimuli sharing features normalize each other more strongly. Comparing these normalization measures to measures of attentional modulation, we demonstrate that subpopulations which exhibit stronger normalization also exhibit larger attentional benefits. In a converging experiment, we reveal that attentional benefits are greatest when a subpopulation is forced into a state of stronger normalization. Taken together, these results suggest that the degree to which a subpopulation exhibits normalization plays a role in dictating its potential for attentional benefits.
Rodrigo M. Braga; Koene R. A. Van Dijk; Jonathan R. Polimeni; Mark C. Eldaief; Randy L. Buckner
Parallel distributed networks resolved at high resolution reveal close juxtaposition of distinct regions Journal Article
In: Journal of Neurophysiology, vol. 121, no. 4, pp. 1513–1534, 2019.
Examination of large-scale distributed networks within the individual reveals details of cortical network organization that are absent in group-averaged studies. One recent discovery is that a distributed transmodal network, often referred to as the “default network,” comprises two closely interdigitated networks, only one of which is coupled to posterior parahippocampal cortex. Not all studies of individuals have identified the same networks, and questions remain about the degree to which the two networks are separate, particularly within regions hypothesized to be interconnected hubs. In this study we replicate the observation of network separation across analytical (seed-based connectivity and parcellation) and data projection (volume and surface) methods in two individuals each scanned 31 times. Additionally, three individuals were examined with highresolution (7T; 1.35 mm) functional magnetic resonance imaging to gain further insight into the anatomical details. The two networks were identified with separate regions localized to adjacent portions of the cortical ribbon, sometimes inside the same sulcus. Midline regions previously implicated as hubs revealed near complete spatial separation of the two networks, displaying a complex spatial topography in the posterior cingulate and precuneus. The network coupled to parahippocampal cortex also revealed a separate region directly within the hippocampus, at or near the subiculum. These collective results support that the default network is composed of at least two spatially juxtaposed networks. Fine spatial details and juxtapositions of the two networks can be identified within individuals at high resolution, providing insight into the network organization of association cortex and placing further constraints on interpretation of group-averaged neuroimaging data.
Benjamin T. Carter; Brent Foster; Nathan M. Muncy; Steven G. Luke
Linguistic networks associated with lexical, semantic and syntactic predictability in reading: A fixation-related fMRI study Journal Article
In: NeuroImage, vol. 189, pp. 224–240, 2019.
The ability to make predictions is thought to facilitate language processing. During language comprehension such predictions appear to occur at multiple levels of linguistic representations (i.e. semantic, syntactic and lexical). The neural mechanisms that define the network sensitive to linguistic predictability have yet to be adequately defined. The purpose of the present study was to explore the neural network underlying predictability during the normal reading of connected text. Predictability values for different linguistic information were obtained from a pre-existing text corpus. Forty-one subjects underwent simultaneous eye-tracking and fMRI scans while reading these select paragraphs. Lexical, semantic, and syntactic predictability measures were then correlated with functional activation associated with fixation onset on the individual words. Activation patterns showed both positive and negative correlations to lexical, semantic, and syntactic predictabilities. Conjunction analysis revealed regions specific to or shared between each type of predictability. The regions associated with the different predictability measures were largely separate. Results suggest that most linguistic predictions are graded in nature, activating components of the existing language system. A number of regions were also found to be uniquely associated with full lexical predictability, most notably the anterior temporal lobe and the inferior posterior temporal cortex.
Joao Castelhano; Isabel C. Duarte; Carlos Ferreira; Joao Duraes; Henrique Madeira; Miguel Castelo-Branco
The role of the insula in intuitive expert bug detection in computer code: an fMRI study Journal Article
In: Brain Imaging and Behavior, vol. 13, no. 3, pp. 623–637, 2019.
Software programming is a complex and relatively recent human activity, involving the integration of mathematical, recursive thinking and language processing. The neural correlates of this recent human activity are still poorly understood. Error monitoring during this type of task, requiring the integration of language, logical symbol manipulation and other mathematical skills, is particularly challenging. We therefore aimed to investigate the neural correlates of decision-making during source code understanding and mental manipulation in professional participants with high expertise. The present fMRI study directly addressed error monitoring during source code comprehension, expert bug detection and decision-making. We used C code, which triggers the same sort of processing irrespective of the native language of the programmer. We discovered a distinct role for the insula in bug monitoring and detection and a novel connectivity pattern that goes beyond the expected activation pattern evoked by source code understanding in semantic language and mathematical processing regions. Importantly, insula activity levels were critically related to the quality of error detection, involving intuition, as signalled by reported initial bug suspicion, prior to final decision and bug detection. Activity in this salience network (SN) region evoked by bug suspicion was predictive of bug detection precision, suggesting that it encodes the quality of the behavioral evidence. Connectivity analysis provided evidence for top-down circuit “reutilization” stemming from anterior cingulate cortex (BA32), a core region in the SN that evolved for complex error monitoring such as required for this type of recent human activity. Cingulate (BA32) and anterolateral (BA10) frontal regions causally modulated decision processes in the insula, which in turn was related to activity of math processing regions in early parietal cortex. In other words, earlier brain regions used during evolution for other functions seem to be reutilized in a top-down manner for a new complex function, in an analogous manner as described for other cultural creations such as reading and literacy.
Alexandra E. D'Agostino; David Kattan; Turhan Canli
An fMRI study of loneliness in younger and older adults Journal Article
In: Social Neuroscience, vol. 14, no. 2, pp. 136–148, 2019.
Loneliness, the subjective experience of social isolation, may reflect, in part, underlying neural processing of social signals. Aging may exacerbate loneliness due to decreased social networks and increased social isolation, or it may reduce loneliness due to preferential attentional processing of positive information and increased interactions with emotionally close partners. Here, we conducted a functional magnetic resonance imaging (fMRI) study of loneliness in younger (N = 50, 26 female, M age = 20.4) and older (N = 49, 30 female, M age = 62.9) adults. Compared to younger adults, older adults were less lonely and dwelled longer on faces, regardless of valence. Previous studies in younger adults found that loneliness was negatively correlated with ventral striatal (VS) activation to pleasant social pictures of strangers yet positively correlated with VS activation to faces of close others. In the present study, we observed no association between loneliness and VS activation to social pictures of strangers in either age group. Further, unlike previous studies, we observed no association between social network size and amygdala activation to social stimuli. Additional research is needed to examine the effect of loneliness and social network size on neural processing of different dimensions of social stimuli.
Abdurahman S. Elkhetali; Leland L. Fleming; Ryan J. Vaden; Rodolphe Nenert; Jane E. Mendle; Kristina M. Visscher
Background connectivity between frontal and sensory cortex depends on task state, independent of stimulus modality Journal Article
In: NeuroImage, vol. 184, pp. 790–800, 2019.
The human brain has the ability to process identical information differently depending on the task. In order to perform a given task, the brain must select and react to the appropriate stimuli while ignoring other irrelevant stimuli. The dynamic nature of environmental stimuli and behavioral intentions requires an equally dynamic set of responses within the brain. Collectively, these responses act to set up and maintain states needed to perform a given task. However, the mechanisms that allow for setting up and maintaining a task state are not fully understood. Prior evidence suggests that one possible mechanism for maintaining a task state may be through altering 'background connectivity,' connectivity that exists independently of the trials of a task. Although previous studies have suggested that background connectivity contributes to a task state, these studies have typically not controlled for stimulus characteristics, or have focused primarily on relationships among areas involved with visual sensory processing. In the present study we examined background connectivity during tasks involving both visual and auditory stimuli. We examined the connectivity profiles of both visual and auditory sensory cortex that allow for selection of task-relevant stimuli, demonstrating the existence of a potentially universal pattern of background connectivity underlying attention to a stimulus. Participants were presented with simultaneous auditory and visual stimuli and were instructed to respond to only one, while ignoring the other. Using functional MRI, we observed task-based modulation of the background connectivity profile for both the auditory and visual cortex to certain brain regions. There was an increase in background connectivity between the task-relevant sensory cortex and control areas in the frontal cortex. This increase in synchrony when receiving the task-relevant stimulus as compared to the task irrelevant stimulus may be maintaining paths for passing information within the cortex. These task-based modulations of connectivity occur independently of stimuli and could be one way the brain sets up and maintains a task state.
Magdalena Fafrowicz; Bartosz Bohaterewicz; Anna Ceglarek; Monika Cichocka; Koryna Lewandowska; Barbara Sikora-Wachowicz; Halszka Oginska; Anna Beres; Justyna Olszewska; Tadeusz Marek
Beyond the low frequency fluctuations: Morning and evening differences in human brain Journal Article
In: Frontiers in Human Neuroscience, vol. 13, pp. 288, 2019.
Human performance, alertness, and most biological functions express rhythmic fluctuations across a 24-h-period. This phenomenon is believed to originate from differences in both circadian and homeostatic sleep-wake regulatory processes. Interactions between these processes result in time-of-day modulations of behavioral performance as well as brain activity patterns. Although the basic mechanism of the 24-h clock is conserved across evolution, there are interindividual differences in the timing of sleep-wake cycles, subjective alertness and functioning throughout the day. The study of circadian typology differences has increased during the last few years, especially research on extreme chronotypes, which provide a unique way to investigate the effects of sleep-wake regulation on cerebral mechanisms. Using functional magnetic resonance imaging (fMRI), we assessed the influence of chronotype and time-of-day on resting-state functional connectivity. Twenty-nine extreme morning- and 34 evening-type participants underwent two fMRI sessions: about 1 h after wake-up time (morning) and about 10 h after wake-up time (evening), scheduled according to their declared habitual sleep-wake pattern on a regular working day. Analysis of obtained neuroimaging data disclosed only an effect of time of day on resting-state functional connectivity; there were different patterns of functional connectivity between morning (MS) and evening (ES) sessions. The results of our study showed no differences between extreme morning-type and evening-type individuals. We demonstrate that circadian and homeostatic influences on the resting-state functional connectivity have a universal character, unaffected by circadian typology.
Jesse Gomez; Alexis Drain; Brianna Jeska; Vaidehi S. Natu; Michael Barnett; Kalanit Grill-Spector
Development of population receptive fields in the lateral visual stream improves spatial coding amid stable structural-functional coupling Journal Article
In: NeuroImage, vol. 188, pp. 59–69, 2019.
Human visual cortex encompasses more than a dozen visual field maps across three major processing streams. One of these streams is the lateral visual stream, which extends from V1 to lateral-occipital (LO) and temporal-occipital (TO) visual field maps and plays a prominent role in shape as well as motion perception. However, it is unknown if and how population receptive fields (pRFs) in the lateral visual stream develop from childhood to adulthood, and what impact this development may have on spatial coding. Here, we used functional magnetic resonance imaging and pRF modeling in school-age children and adults to investigate the development of the lateral visual stream. Our data reveal four main findings: 1) The topographic organization of eccentricity and polar angle maps of the lateral stream is stable after age five. 2) In both age groups there is a reliable relationship between eccentricity map transitions and cortical folding: the middle occipital gyrus predicts the transition between the peripheral representation of LO and TO maps. 3) pRFs in LO and TO maps undergo differential development from childhood to adulthood, resulting in increasing coverage of the central visual field in LO and of the peripheral visual field in TO. 4) Model-based decoding shows that the consequence of pRF and visual field coverage development is improved spatial decoding from LO and TO distributed responses in adults vs. children. Together, these results explicate both the development and topography of the lateral visual stream. Our data show that the general structural-functional organization is laid out early in development, but fine-scale properties, such as pRF distribution across the visual field and consequently, spatial precision, become fine-tuned across childhood development. These findings advance understanding of the development of the human visual system from childhood to adulthood and provide an essential foundation for understanding developmental deficits.
Noriya Watanabe; Jamil P. Bhanji; Hideki Ohira; Mauricio R. Delgado
Reward-driven arousal impacts preparation to perform a task via amygdala-caudate mechanisms Journal Article
In: Cerebral Cortex, vol. 29, no. 7, pp. 3010–3022, 2019.
Preparing for a challenging task can increase physiological arousal, in particular when potential incentives are large (e.g., a solo musical performance in front of an audience). Here, we examine how potential reward and its influence on arousal, measured by pupil dynamics, are represented in the brain while preparing for a challenging task. We further ask how neural representations during preparation relate to actual performance. Trials resulting in performance failure were characterized by increased pupil dilation as a function of increasing reward magnitude during preparation. Such failure trials were also associated with activation of the right amygdala representing pupil dilation, and the left caudate representing reward magnitude. Notably, increases in functional connectivity between amygdala and caudate preceded performance failure. These findings highlight increased connectivity between neural regions representing reward and arousal in circumstances where reward-driven arousal impairs performance.
Noriya Watanabe; Jamil P. Bhanji; Hiroki C. Tanabe; Mauricio R. Delgado
Ventromedial prefrontal cortex contributes to performance success by controlling reward-driven arousal representation in amygdala Journal Article
In: NeuroImage, vol. 202, pp. 116136, 2019.
When preparing for a challenging task, potential rewards can cause physiological arousal that may impair performance. In this case, it is important to control reward-driven arousal while preparing for task execution. We recently examined neural representations of physiological arousal and potential reward magnitude during preparation, and found that performance failure was explained by relatively increased reward representation in the left caudate nucleus and arousal representation in the right amygdala (Watanabe, et al., 2019). Here we examine how prefrontal cortex influences the amygdala and caudate to control reward-driven arousal. Ventromedial prefrontal cortex (VMPFC) exhibited activity that was negatively correlated with trial-wise physiological arousal change, which identified this region as a potential modulator of amygdala and caudate. Next we tested the VMPFC - amygdala - caudate effective network using dynamic causal modeling (Friston et al., 2003). Post-hoc Bayesian model selection (Friston and Penny, 2011) identified a model that best fit data, in which amygdala activation was suppressively controlled by the VMPFC only in success trials. Furthermore, fixed connectivity strength from VMPFC to amygdala explained individual task performance. These findings highlight the role of effective connectivity from VMPFC to amygdala in order to control arousal during preparation for successful performance.
Yuan-hao Wu; Lisa A. Velenosi; Pia Schröder; Simon Ludwig; Felix Blankenburg
Decoding vibrotactile choice independent of stimulus order and saccade selection during sequential comparisons Journal Article
In: Human Brain Mapping, vol. 40, no. 6, pp. 1898–1907, 2019.
Decision-making in the somatosensory domain has been intensively studied using vibrotactile frequency discrimination tasks. Results from human and monkey electrophysiological studies from this line of research suggest that perceptual choices are encoded within a sensorimotor network. These findings, however, rely on experimental settings in which perceptual choices are inextricably linked to sensory and motor components of the task. Here, we devised a novel version of the vibrotactile frequency discrimination task with saccade responses which has the crucial advantage of decoupling perceptual choices from sensory and motor processes. We recorded human fMRI data from 32 participants while they performed the task. Using a whole-brain searchlight multivariate classification technique, we identify the left lateral prefrontal cortex and the oculomotor system, including the bilateral frontal eye fields (FEF) and intraparietal sulci, as representing vibrotactile choices. Moreover, we show that the decoding accuracy of choice information in the right FEF correlates with behavioral performance. Not only are these findings in remarkable agreement with previous work, they also provide novel fMRI evidence for choice coding in human oculomotor regions, which is not limited to saccadic decisions, but pertains to contexts where choices are made in a more abstract form.
Yaoda Xu; Maryam Vaziri-Pashkam
Task modulation of the 2-pathway characterization of occipitotemporal and posterior parietal visual object representations Journal Article
In: Neuropsychologia, vol. 132, pp. 107140, 2019.
Recent studies have reported the existence of rich non-spatial visual object representations in both human and monkey posterior parietal cortex (PPC), similar to those found in occipito-temporal cortex (OTC). Despite this similarity, we recently showed that visual object representation still differ between OTC and PPC in two aspects. In one study, by manipulating whether object shape or color was task relevant, we showed that visual object representations were under greater top-down attention and task control in PPC than in OTC (Vaziri-Pashkam & Xu, 2017, J Neurosci). In another study, using a bottom-up data driven approach, we showed that there exists a large separation between PPC and OTC regions in the representational space, with OTC regions lining up hierarchically along an OTC pathway and PPC regions lining up hierarchically along an orthogonal PPC pathway (Vaziri-Pashkam & Xu, 2019, Cereb Cortex). To understand the interaction of goal-driven visual processing and the two-pathway structure in the representational space, here we performed a set of new analyses of the data from the three experiments of Vaziri-Pashkam and Xu (2017) and directly compared the two-pathway separation of OTC and PPC regions when object shapes were attended and task relevant and when they were not. We found that in all three experiments the correlation of visual object representational structure between superior IPS (a key PPC visual region) and lateral and ventral occipito-temporal regions (higher OTC visual regions) became greater when object shapes were attended than when they were not. This modified the two-pathway structure, with PPC regions moving closer to higher OTC regions and a compression of the PPC pathway towards the OTC pathway in the representational space when shapes were attended. Consistent with this observation, the correlation between neural and behavioral measures of visual representational structure was also higher in superior IPS when shapes were attended than when they were not. By comparing representational structures across experiments and tasks, we further showed that attention to object shape resulted in the formation of more similar object representations in superior IPS across experiments than between the two tasks within the same experiment despite noise and stimulus differences across the experiments. Overall, these results demonstrated that, despite the separation of the OTC and PPC pathways in the representational space, the visual representational structure of PPC is flexible and can be modulated by the task demand. This reaffirms the adaptive nature of visual processing in PPC and further distinguishes it from the more invariant nature of visual processing in OTC.
Imme C. Zillekens; Marie Luise Brandi; Juha M. Lahnakoski; Atesh Koul; Valeria Manera; Cristina Becchio; Leonhard Schilbach
Increased functional coupling of the left amygdala and medial prefrontal cortex during the perception of communicative point-light stimuli Journal Article
In: Social Cognitive and Affective Neuroscience, vol. 14, no. 1, pp. 97–107, 2019.
Interpersonal predictive coding (IPPC) describes the behavioral phenomenon whereby seeing a communicative rather than an individual action helps to discern a masked second agent. As little is known, yet, about the neural correlates of IPPC, we conducted a functional magnetic resonance imaging study in a group of 27 healthy participants using point-light displays of moving agents embedded in distractors. We discovered that seeing communicative compared to individual actions was associated with higher activation of right superior frontal gyrus, whereas the reversed contrast elicited increased neural activation in an action observation network that was activated during all trials. Our findings, therefore, potentially indicate the formation of action predictions and a reduced demand for executive control in response to communicative actions. Further, in a regression analysis, we revealed that increased perceptual sensitivity was associated with a deactivation of the left amygdala during the perceptual task. A consecutive psychophysiological interaction analysis showed increased connectivity of the amygdala with medial prefrontal cortex in the context of communicative compared to individual actions. Thus, whereas increased amygdala signaling might interfere with task-relevant processes, increased co-activation of the amygdala and the medial prefrontal cortex in a communicative context might represent the integration of mentalizing computations.
Sonya Bells; Jérémie Lefebvre; Giulia Longoni; Sridar Narayanan; Douglas L. Arnold; Eleun Ann Yeh; Donald J. Mabbott
White matter plasticity and maturation in human cognition Journal Article
In: Glia, vol. 67, no. 11, pp. 2020–2037, 2019.
White matter plasticity likely plays a critical role in supporting cognitive development. However, few studies have used the imaging methods specific to white matter tissue structure or experimental designs sensitive to change in white matter necessary to elucidate these relations. Here we briefly review novel imaging approaches that provide more specific information regarding white matter microstructure. Furthermore, we highlight recent studies that provide greater clarity regarding the relations between changes in white matter and cognition maturation in both healthy children and adolescents and those with white matter insult. Finally, we examine the hypothesis that white matter is linked to cognitive function via its impact on neural synchro- nization. We test this hypothesis in a population of children and adolescents with recurrent demyelinating syndromes. Specifically, we evaluate group differences in white matter microstructure within the optic radiation; and neural phase synchrony in visual cortex during a visual task between 25 patients and 28 typically developing age-matched controls. Children and adolescents with demyelinating syndromes show evidence of myelin and axonal compromise and this compromise predicts reduced phase synchrony during a visual task compared to typically developing controls. We investigate one plausible mechanism at play in this relationship using a computational model of gamma generation in early visual cortical areas. Overall, our findings show a fundamental connection between white matter microstructure and neural synchronization that may be critical for cognitive processing. In the future, longitudinal or interventional studies can build upon our knowledge of these exciting relations between white matter, neural communication, and cognition.
Antea D'Andrea; Federico Chella; Tom R. Marshall; Vittorio Pizzella; Gian Luca Romani; Ole Jensen; Laura Marzetti
Alpha and alpha-beta phase synchronization mediate the recruitment of the visuospatial attention network through the Superior Longitudinal Fasciculus Journal Article
In: NeuroImage, vol. 188, pp. 722–732, 2019.
It is well known that attentional selection of relevant information relies on local synchronization of alpha band neuronal oscillations in visual cortices for inhibition of distracting inputs. Additionally, evidence for long-range coupling of neuronal oscillations between visual cortices and regions engaged in the anticipation of upcoming stimuli has been more recently provided. Nevertheless, on the one hand the relation between long-range functional coupling and anatomical connections is still to be assessed, and, on the other hand, the specific role of the alpha and beta frequency bands in the different processes underlying visuo-spatial attention still needs further clarification. We address these questions using measures of linear (frequency-specific) and nonlinear (cross-frequency) phase-synchronization in a cohort of 28 healthy subjects using magnetoencephalography. We show that alpha band phase-synchronization is modulated by the orienting of attention according to a parieto-occipital top-down mechanism reflecting behavior, and its hemispheric asymmetry is predicted by volume's asymmetry of specific tracts of the Superior-Longitudinal-Fasciculus. We also show that a network comprising parietal regions and the right putative Frontal-Eye-Field, but not the left, is recruited in the deployment of spatial attention through an alpha-beta cross-frequency coupling. Overall, we demonstrate that the visuospatial attention network features subsystems indexed by characteristic spectral fingerprints, playing different functional roles in the anticipation of upcoming stimuli and with diverse relation to fiber tracts.
Linda Drijvers; Mircea Plas; Asli Özyürek; Ole Jensen
Native and non-native listeners show similar yet distinct oscillatory dynamics when using gestures to access speech in noise Journal Article
In: NeuroImage, vol. 194, pp. 55–67, 2019.
Listeners are often challenged by adverse listening conditions during language comprehension induced by external factors, such as noise, but also internal factors, such as being a non-native listener. Visible cues, such as semantic information conveyed by iconic gestures, can enhance language comprehension in such situations. Using magnetoencephalography (MEG) we investigated whether spatiotemporal oscillatory dynamics can predict a listener's benefit of iconic gestures during language comprehension in both internally (non-native versus native listeners) and externally (clear/degraded speech) induced adverse listening conditions. Proficient non-native speakers of Dutch were presented with videos in which an actress uttered a degraded or clear verb, accompanied by a gesture or not, and completed a cued-recall task after every video. The behavioral and oscillatory results obtained from non-native listeners were compared to an MEG study where we presented the same stimuli to native listeners (Drijvers et al., 2018a). Non-native listeners demonstrated a similar gestural enhancement effect as native listeners, but overall scored significantly slower on the cued-recall task. In both native and non-native listeners, an alpha/beta power suppression revealed engagement of the extended language network, motor and visual regions during gestural enhancement of degraded speech comprehension, suggesting similar core processes that support unification and lexical access processes. An individual's alpha/beta power modulation predicted the gestural benefit a listener experienced during degraded speech comprehension. Importantly, however, non-native listeners showed less engagement of the mouth area of the primary somatosensory cortex, left insula (beta), LIFG and ATL (alpha) than native listeners, which suggests that non-native listeners might be hindered in processing the degraded phonological cues and coupling them to the semantic information conveyed by the gesture. Native and non-native listeners thus demonstrated similar yet distinct spatiotemporal oscillatory dynamics when recruiting visual cues to disambiguate degraded speech.
Susanne Eisenhauer; Christian J. Fiebach; Benjamin Gagl
Context-based facilitation in visual word recognition: Evidence for visual and lexical but not pre-lexical contributions Journal Article
In: eNeuro, vol. 6, no. 2, pp. 1–25, 2019.
Word familiarity and predictive context facilitate visual word processing, leading to faster recognition times and reduced neuronal responses. Previously, models with and without top-down connections, including lexical-semantic, pre-lexical (e.g., orthographic/phonological), and visual processing levels were successful in accounting for these facilitation effects. Here we systematically assessed context-based facilitation with a repetition priming task and explicitly dissociated pre-lexical and lexical processing levels using a pseudoword (PW) familiarization procedure. Experiment 1 investigated the temporal dynamics of neuronal facilitation effects with magnetoencephalography (MEG; N = 38 human participants), while experiment 2 assessed behavioral facilitation effects (N = 24 human participants). Across all stimulus conditions, MEG demonstrated context-based facilitation across multiple time windows starting at 100 ms, in occipital brain areas. This finding indicates context-based facilitation at an early visual processing level. In both experiments, we furthermore found an interaction of context and lexical familiarity, such that stimuli with associated meaning showed the strongest context-dependent facilitation in brain activation and behavior. Using MEG, this facilitation effect could be localized to the left anterior temporal lobe at around 400 ms, indicating within-level (i.e., exclusively lexical-semantic) facilitation but no top-down effects on earlier processing stages. Increased pre-lexical familiarity (in PWs familiarized utilizing training) did not enhance or reduce context effects significantly. We conclude that context-based facilitation is achieved within visual and lexical processing levels. Finally, by testing alternative hypotheses derived from mechanistic accounts of repetition suppression, we suggest that the facilitatory context effects found here are implemented using a predictive coding mechanism.
Matthew W. Flounders; Carlos González-García; Richard Hardstone; Biyu J. He
Neural dynamics of visual ambiguity resolution by perceptual prior Journal Article
In: eLife, vol. 8, pp. 1–25, 2019.
Past experiences have enormous power in shaping our daily perception. Currently, dynamical neural mechanisms underlying this process remain mysterious. Exploiting a dramatic visual phenomenon, where a single experience of viewing a clear image allows instant recognition of a related degraded image, we investigated this question using MEG and 7 Tesla fMRI in humans. We observed that following the acquisition of perceptual priors, different degraded images are represented much more distinctly in neural dynamics starting from $sim$500 ms after stimulus onset. Content-specific neural activity related to stimulus-feature processing dominated within 300 ms after stimulus onset, while content-specific neural activity related to recognition processing dominated from 500 ms onward. Model-driven MEG-fMRI data fusion revealed the spatiotemporal evolution of neural activities involved in stimulus, attentional, and recognition processing. Together, these findings shed light on how experience shapes perceptual processing across space and time in the brain.
Jim D. Herring; Sophie Esterer; Tom R. Marshall; Ole Jensen; Til O. Bergmann
Low-frequency alternating current stimulation rhythmically suppresses gamma-band oscillations and impairs perceptual performance Journal Article
In: NeuroImage, vol. 184, pp. 440–449, 2019.
Low frequency oscillations such as alpha (8–12 Hz) are hypothesized to rhythmically gate sensory processing, reflected by 40–100 Hz gamma band activity, via the mechanism of pulsed inhibition. We applied transcranial alternating current stimulation (TACS) at individual alpha frequency (IAF) and flanking frequencies (IAF-4 Hz, IAF+4 Hz) to the occipital cortex of healthy human volunteers during concurrent magnetoencephalography (MEG), while participants performed a visual detection task inducing strong gamma-band responses. Occipital (but not retinal) TACS phasically suppressed stimulus-induced gamma oscillations in the visual cortex and impaired target detection, with stronger phase-to-amplitude coupling predicting behavioral impairments. Retinal control TACS ruled out retino-thalamo-cortical entrainment resulting from (subthreshold) retinal stimulation. All TACS frequencies tested were effective, suggesting that visual gamma-band responses can be modulated by a range of low frequency oscillations. We propose that TACS-induced membrane potential modulations mimic the rhythmic change in cortical excitability by which spontaneous low frequency oscillations may eventually exert their impact when gating sensory processing via pulsed inhibition.
Erik L Meijs; Pim Mostert; Heleen A. Slagter; Floris P. Lange; Simon Gaal
Exploring the role of expectations and stimulus relevance on stimulus-specific neural representations and conscious report Journal Article
In: Neuroscience of Consciousness, vol. 5, no. 1, pp. 1–12, 2019.
Subjective experience can be influenced by top-down factors, such as expectations and stimulus relevance. Recently, it has been shown that expectations can enhance the likelihood that a stimulus is consciously reported, but the neural mechanisms supporting this enhancement are still unclear. We manipulated stimulus expectations within the attentional blink (AB) paradigm using letters and combined visual psychophysics with magnetoencephalographic (MEG) recordings to investigate whether prior expectations may enhance conscious access by sharpening stimulus-specific neural representations. We further explored how stimulus-specific neural activity patterns are affected by the factors expectation, stimulus relevance and conscious report. First, we show that valid expectations about the identity of an upcoming stimulus increase the likelihood that it is consciously reported. Second, using a series of multivariate decoding analyses, we show that the identity of letters presented in and out of the AB can be reliably decoded from MEG data. Third, we show that early sensory stimulus-specific neural representations are similar for reported and missed target letters in the AB task (active report required) and an oddball task in which the letter was clearly presented but its identity was task-irrelevant. However, later sustained and stable stimulus-specific representations were uniquely observed when target letters were consciously reported (decision-dependent signal). Fourth, we show that global pre-stimulus neural activity biased perceptual decisions for a ‘seen' response. Fifth and last, no evidence was obtained for the sharpening of sensory representations by top-down expectations. We discuss these findings in light of emerging models of perception and conscious report highlighting the role of expectations and stimulus relevance.
Sebastian Michelmann; Bernhard P. Staresina; Howard Bowman; Simon Hanslmayr
Speed of time-compressed forward replay flexibly changes in human episodic memory Journal Article
In: Nature Human Behaviour, vol. 3, no. 2, pp. 143–154, 2019.
Remembering information from continuous past episodes is a complex task 1 . On the one hand, we must be able to recall events in a highly accurate way, often including exact timings. On the other hand, we can ignore irrelevant details and skip to events of interest. Here, we track continuous episodes consisting of different subevents as they are recalled from memory. In behavioural and magnetoencephalography data, we show that memory replay is temporally compressed and proceeds in a forward direction. Neural replay is characterized by the reinstatement of temporal patterns from encoding 2,3 . These fragments of activity reappear on a compressed timescale. Herein, the replay of subevents takes longer than the transition from one subevent to another. This identifies episodic memory replay as a dynamic process in which participants replay fragments of fine-grained temporal patterns and are able to skip flexibly across subevents.
Judith Nicolas; Aline Bompas; Romain Bouet; Olivier Sillan; Eric Koun; Christian Urquizar; Aurélie Bidet-Caulet; Denis Pélisson
Saccadic adaptation boosts ongoing gamma activity in a subsequent visuoattentional task Journal Article
In: Cerebral Cortex, vol. 29, no. 9, pp. 3606–3617, 2019.
Attention and saccadic adaptation (SA) are critical components of visual perception, the former enhancing sensory processing of selected objects, the latter maintaining the eye movements accuracy toward them. Recent studies propelled the hypothesis of a tight functional coupling between these mechanisms, possibly due to shared neural substrates. Here, we used magnetoencephalography to investigate for the first time the neurophysiological bases of this coupling and of SA per se. We compared visual discrimination performance of 12 healthy subjects before and after SA. Eye movements and magnetic signals were recorded continuously. Analyses focused on gamma band activity (GBA) during the pretarget period of the discrimination and the saccadic tasks. We found that GBA increases after SA. This increase was found in the right hemisphere for both postadaptation saccadic and discrimination tasks. For the latter, GBA also increased in the left hemisphere. We conclude that oculomotor plasticity involves GBA modulation within an extended neural network which persists after SA, suggesting a possible role of gamma oscillations in the coupling between SA and attention.
Elena V. Orekhova; Tatiana A. Stroganova; Justin F. Schneiderman; Sebastian Lundström; Bushra Riaz; Darko Sarovic; Olga V. Sysoeva; Georg Brant; Christopher Gillberg; Nouchine Hadjikhani
Neural gain control measured through cortical gamma oscillations is associated with sensory sensitivity Journal Article
In: Human Brain Mapping, vol. 40, no. 5, pp. 1583–1593, 2019.
Gamma oscillations facilitate information processing by shaping the excitatory input/output of neuronal populations. Recent studies in humans and nonhuman primates have shown that strong excitatory drive to the visual cortex leads to suppression of induced gamma oscillations, which may reflect inhibitory-based gain control of network excitation. The efficiency of the gain control measured through gamma oscillations may in turn affect sensory sensitivity in everyday life. To test this prediction, we assessed the link between self-reported sensitivity and changes in magneto-encephalographic gamma oscillations as a function of motion velocity of high-contrast visual gratings. The induced gamma oscillations increased in frequency and decreased in power with increasing stimulation intensity. As expected, weaker suppression of the gamma response correlated with sensory hypersensitivity. Robustness of this result was confirmed by its replication in the two samples: neurotypical subjects and people with autism, who had generally elevated sensory sensitivity. We conclude that intensity-related suppression of gamma response is a promising biomarker of homeostatic control of the excitation–inhibition balance in the visual cortex.
Davide Paoletti; Christoph Braun; Elisabeth Julie Vargo; Wieske Zoest
Spontaneous pre-stimulus oscillatory activity shapes the way we look: A concurrent imaging and eye-movement study Journal Article
In: European Journal of Neuroscience, vol. 49, pp. 137–149, 2019.
Previous behavioural studies have accrued evidence that response time plays a critical role in determining whether selection is influenced by stimulus saliency or target template. In the present work, we investigated to what extent the variations in timing and consequent oculomotor controls are influenced by spontaneous variations in pre-stimulus alpha oscillations. We recorded simultaneously brain activity using magnetoencephalography (MEG) and eye movements while participants performed a visual search task. Our results show that slower saccadic reaction times were predicted by an overall stronger alpha power in the 500 ms time window preceding the stimulus onset, while weaker alpha power was a signature of faster responses. When looking separately at performance for fast and slow responses, we found evidence for two specific sources of alpha activity predicting correct versus incorrect responses. When saccades were quickly elicited, errors were predicted by stronger alpha activity in posterior areas, comprising the angular gyrus in the temporal-parietal junction (TPJ) and possibly the lateral intraparietal area (LIP). Instead, when participants were slower in responding, an increase of alpha power in frontal eye fields (FEF), supplementary eye fields (SEF) and dorsolateral pre-frontal cortex (DLPFC) predicted erroneous saccades. In other words, oculomotor accuracy in fast responses was predicted by alpha power differences in more posterior areas, while the accuracy in slow responses was predicted by alpha power differences in frontal areas, in line with the idea that these areas may be differentially related to stimulus-driven and goal-driven control of selection.
Thomas Parr; M. Berk Mirza; Hayriye Cagnan; Karl J. Friston
Dynamic causal modelling of active vision Journal Article
In: Journal of Neuroscience, vol. 39, no. 32, pp. 6265–6275, 2019.
In this paper, we draw from recent theoretical work on active perception, which suggests that the brain makes use of an internal (i.e., generative) model to make inferences about the causes of sensations. This view treats visual sensations as consequent on action (i.e., saccades) and implies that visual percepts must be actively constructed via a sequence ofeye movements. Oculomotor control calls on a distributed set ofbrain sources that includes the dorsal and ventral frontoparietal (attention) networks.Weargue that connections from the frontal eye fields to ventral parietal sources represent the mapping from “where”, fixation location to information derived from “what” representations in the ventral visual stream. During scene construction, this mapping must be learned, putatively through changes in the effective connectivityofthese synapses. Here,wetest the hypothesis that the couplingbetweenthe dorsal frontal cortexand the right temporoparietal cortex is modulated during saccadic interrogation ofa simple visual scene. Using dynamic causal modeling for magnetoencephalography with (male and female) human participants, we assess the evidence for changes in effective connectivity by comparing models that allow for this modulation with models that do not. We find strong evidence for modulation of connections between the two attention networks; namely, a disinhibition ofthe ventral network by its dorsal counterpart.
Ella Podvalny; Matthew W. Flounders; Leana E. King; Tom Holroyd; Biyu J. He
A dual role of prestimulus spontaneous neural activity in visual object recognition Journal Article
In: Nature Communications, vol. 10, pp. 3910, 2019.
Vision relies on both specific knowledge of visual attributes, such as object categories, and general brain states, such as those reflecting arousal. We hypothesized that these phenomena independently influence recognition of forthcoming stimuli through distinct processes reflected in spontaneous neural activity. Here, we recorded magnetoencephalographic (MEG) activity in participants (N = 24) who viewed images of objects presented at recognition threshold. Using multivariate analysis applied to sensor-level activity patterns recorded before stimulus presentation, we identified two neural processes influencing subsequent subjective recognition: a general process, which disregards stimulus category and correlates with pupil size, and a specific process, which facilitates category-specific recognition. The two processes are doubly-dissociable: the general process correlates with changes in criterion but not in sensitivity, whereas the specific process correlates with changes in sensitivity but not in criterion. Our findings reveal distinct mechanisms of how spontaneous neural activity influences perception and provide a framework to integrate previous findings.
Tzvetan Popov; Bart Gips; Sabine Kastner; Ole Jensen
Spatial specificity of alpha oscillations in the human visual system Journal Article
In: Human Brain Mapping, vol. 40, no. 15, pp. 4432–4440, 2019.
Alpha oscillations are strongly modulated by spatial attention. To what extent, the generators of cortical alpha oscillations are spatially distributed and have selectivity that can be related to retinotopic organization is a matter of continuous scientific debate. In the present report, neuromagnetic activity was quantified by means of spatial location tuning functions from 30 participants engaged in a visuospatial attention task. A cue presented briefly in one of 16 locations directing covert spatial attention resulted in a robust modulation of posterior alpha oscillations. The distribution of the alpha sources approximated the retinotopic organization of the human visual system known from hemodynamic studies. Better performance in terms of target identification was associated with a more spatially constrained alpha modulation. The present findings demonstrate that the generators of posterior alpha oscillations are retinotopically organized when modulated by spatial attention.
Silvan C. Quax; Nadine Dijkstra; Mariel J. Staveren; Sander E. Bosch; Marcel A. J. Gerven
Eye movements explain decodability during perception and cued attention in MEG Journal Article
In: NeuroImage, vol. 195, pp. 444–453, 2019.
Eye movements are an integral part of human perception, but can induce artifacts in many magneto-encephalography (MEG) and electroencephalography (EEG) studies. For this reason, investigators try to minimize eye movements and remove these artifacts from their data using different techniques. When these artifacts are not purely random, but consistent regarding certain stimuli or conditions, the possibility arises that eye movements are actually inducing effects in the MEG signal. It remains unclear how much of an influence eye movements can have on observed effects in MEG, since most MEG studies lack a control analysis to verify whether an effect found in the MEG signal is induced by eye movements. Here, we find that we can decode stimulus location from eye movements in two different stages of a working memory match-to-sample task that encompass different areas of research typically done with MEG. This means that the observed MEG effect might be (partly) due to eye movements instead of any true neural correlate. We suggest how to check for eye movement effects in the data and make suggestions on how to minimize eye movement artifacts from occurring in the first place.
Romain Quentin; Jean Rémi King; Etienne Sallard; Nathan Fishman; Ryan Thompson; Ethan R. Buch; Leonardo G. Cohen
Differential brain mechanisms of selection and maintenance of information during working memory Journal Article
In: Journal of Neuroscience, vol. 39, no. 19, pp. 3728–3740, 2019.
Working memory is our ability to select and temporarily hold information as needed for complex cognitive operations. The temporal dynamics of sustained and transient neural activity supporting the selection and holding of memory content is not known. To address this problem, we recorded magnetoencephalography in healthy participants performing a retro-cue working memory task in which the selection rule and the memory content varied independently. Multivariate decoding and source analyses showed that selecting the memory content relies on prefrontal and parieto-occipital persistent oscillatory neural activity. By contrast, the memory content was reactivated in a distributed occipitotemporal posterior network, preceding the working memory decision and in a different format than during the visual encoding. These results identify a neural signature of content selection and characterize differentiated spatiotemporal constraints for subprocesses of working memory.
Mats W. J. Es; Jan-Mathijs Schoffelen
Stimulus-induced gamma power predicts the amplitude of the subsequent visual evoked response Journal Article
In: NeuroImage, vol. 186, pp. 703–712, 2019.
The efficiency of neuronal information transfer in activated brain networks may affect behavioral performance. Gamma-band synchronization has been proposed to be a mechanism that facilitates neuronal processing of behaviorally relevant stimuli. In line with this, it has been shown that strong gamma-band activity in visual cortical areas leads to faster responses to a visual go cue. We investigated whether there are directly observable consequences of trial-by-trial fluctuations in non-invasively observed gamma-band activity on the neuronal response. Specifically, we hypothesized that the amplitude of the visual evoked response to a go cue can be predicted by gamma power in the visual system, in the window preceding the evoked response. Thirty-three human subjects (22 female) performed a visual speeded response task while their magnetoencephalogram (MEG) was recorded. The participants had to respond to a pattern reversal of a concentric moving grating. We estimated single trial stimulus-induced visual cortical gamma power, and correlated this with the estimated single trial amplitude of the most prominent event-related field (ERF) peak within the first 100 ms after the pattern reversal. In parieto-occipital cortical areas, the amplitude of the ERF correlated positively with gamma power, and correlated negatively with reaction times. No effects were observed for the alpha and beta frequency bands, despite clear stimulus onset induced modulation at those frequencies. These results support a mechanistic model, in which gamma-band synchronization enhances the neuronal gain to relevant visual input, thus leading to more efficient downstream processing and to faster responses.
Rodolfo Solís-Vivanco; Ole Jensen; Mathilde Bonnefond
Top–down control of alpha phase adjustment in anticipation of temporally predictable visual stimuli Journal Article
In: Journal of Cognitive Neuroscience, vol. 30, no. 8, pp. 1157–1169, 2018.
Alpha oscillations (8–14 Hz) are proposed to represent an active mechanism of functional inhibition of neuronal processing. Specifically, alpha oscillations are associated with pulses of inhibition repeating every ∼100 msec. Whether alpha phase, similar to alpha power, is under top–down control remains unclear. Moreover, the sources of such putative top–down phase control are unknown. We designed a cross-modal (visual/auditory) attention study in which we used magnetoencephalography to record the brain activity from 34 healthy participants. In each trial, a somatosensory cue indicated whether to attend to either the visual or auditory domain. The timing of the stimulus onset was predictable across trials. We found that, when visual information was attended, anticipatory alpha power was reduced in visual areas, whereas the phase adjusted just before the stimulus onset. Performance in each modality was predicted by the phase of the alpha oscillations previous to stimulus onset. Alpha oscillations in the left pFC appeared to lead the adjustment of alpha phase in visual areas. Finally, alpha phase modulated stimulus-induced gamma activity. Our results confirm that alpha phase can be top–down adjusted in anticipation of predictable stimuli and improve performance. Phase adjustment of the alpha rhythm might serve as a neurophysiological resource for optimizing visual processing when temporal predictions are possible and there is considerable competition between target and distracting stimuli.
Tobias Staudigl; Marcin Leszczynski; Joshua Jacobs; Sameer A. Sheth; Charles E. Schroeder; Ole Jensen; Christian F. Doeller
Hexadirectional modulation of high-frequency electrophysiological activity in the human anterior medial temporal lobe maps visual space Journal Article
In: Current Biology, vol. 28, pp. 1–5, 2018.
Grid cells are one of the core building blocks of spatial navigation . Single-cell recordings of grid cells in the rodent entorhinal cortex revealed hexagonal coding of the local environment during spatial navigation . Grid-like activity has also been identified in human single-cell recordings during virtual navigation . Human fMRI studies further provide evidence that grid-like signals are also accessible on a macroscopic level [3–7]. Studies in both nonhuman primates  and humans [9, 10] suggest that grid-like coding in the entorhinal cortex generalizes beyond spatial navigation during locomotion, providing evidence for grid-like mapping of visual space during visual exploration—akin to the grid cell positional code in rodents during spatial navigation. However, electrophysiological correlates of the grid code in humans remain unknown. Here, we provide evidence for grid-like, hexadirectional coding of visual space by human high-frequency activity, based on two independent datasets: non-invasive magnetoencephalography (MEG) in healthy subjects and entorhinal intracranial electroencephalography (EEG) recordings in an epileptic patient. Both datasets consistently show a hexadirectional modulation of broadband high-frequency activity (60–120 Hz). Our findings provide first evidence for a grid-like MEG signal, indicating that the human entorhinal cortex codes visual space in a grid-like manner [8–10], and support the view that grid coding generalizes beyond environmental mapping during locomotion [4–6, 11]. Due to their millisecond accuracy, MEG recordings allow linking of grid-like activity to epochs during relevant behavior, thereby opening up the possibility for new MEG-based investigations of grid coding at high temporal resolution.
K. Seeliger; Matthias Fritsche; U. Güçlü; S. Schoenmakers; J. M. Schoffelen; S. E. Bosch; Marcel A. J. Gerven
Convolutional neural network-based encoding and decoding of visual object recognition in space and time Journal Article
In: NeuroImage, vol. 180, pp. 253–266, 2018.
Representations learned by deep convolutional neural networks (CNNs) for object recognition are a widely investigated model of the processing hierarchy in the human visual system. Using functional magnetic resonance imaging, CNN representations of visual stimuli have previously been shown to correspond to processing stages in the ventral and dorsal streams of the visual system. Whether this correspondence between models and brain signals also holds for activity acquired at high temporal resolution has been explored less exhaustively. Here, we addressed this question by combining CNN-based encoding models with magnetoencephalography (MEG). Human participants passively viewed 1,000 images of objects while MEG signals were acquired. We modelled their high temporal resolution source-reconstructed cortical activity with CNNs, and observed a feed-forward sweep across the visual hierarchy between 75 and 200 ms after stimulus onset. This spatiotemporal cascade was captured by the network layer representations, where the increasingly abstract stimulus representation in the hierarchical network model was reflected in different parts of the visual cortex, following the visual ventral stream. We further validated the accuracy of our encoding model by decoding stimulus identity in a left-out validation set of viewed objects, achieving state-of-the-art decoding accuracy.
E. A. Allen; E. Damaraju; T. Eichele; L. Wu; V. D. Calhoun
EEG signatures of dynamic functional network connectivity states Journal Article
In: Brain Topography, vol. 31, no. 1, pp. 101–116, 2018.
The human brain operates by dynamically mod- ulating different neural populations to enable goal directed behavior. The synchrony or lack thereof between different brain regions is thought to correspond to observed functional connectivity dynamics in resting state brain imaging data. In a large sample of healthy human adult subjects and utilizing a sliding windowed correlation method on functional imaging data, earlier we demonstrated the presence of seven distinct functional connectivity states/patterns between different brain networks that reliably occur across time and subjects. Whether these connectivity states correspond to meaningful electrophysiological signatures was not clear. In this study, using a dataset with concurrent EEG and resting state functional imaging data acquired during eyes open and eyes closed states, we demonstrate the replicability of previous findings in an independent sample, and identify EEG spectral signatures associated with these functional network connectivity changes. Eyes open and eyes closed conditions show common and different connectivity patterns that are associated with distinct EEG spectral signatures. Certain connectivity states are more prevalent in the eyes open case and some occur only in eyes closed state. Both conditions exhibit a state of increased thalamo-cortical anticorrelation associated with reduced EEG spec- tral alpha power and increased delta and theta power possi- bly reflecting drowsiness. This state occurs more frequently in the eyes closed state. In summary, we find a link between dynamic connectivity in fMRI data and concurrently collected EEG data, including a large effect of vigilance on functional connectivity. As demonstrated with EEG and fMRI, the stationarity of connectivity cannot be assumed, even for relatively short periods.
Noah C. Benson; Keith W. Jamison; Michael J. Arcaro; An T. Vu; Matthew F. Glasser; Timothy S. Coalson; David C. Van Essen; Essa Yacoub; Kamil Ugurbil; Jonathan Winawer; Kendrick N. Kay
The Human Connectome Project 7 Tesla retinotopy dataset: Description and population receptive field analysis Journal Article
In: Journal of Vision, vol. 18, no. 13, pp. 1–22, 2018.
About a quarter of human cerebral cortex is dedicated mainly to visual processing. The large-scale spatial organization of visual cortex can be measured with functional magnetic resonance imaging (fMRI) while subjects view spatially modulated visual stimuli, also known as ‘‘retinotopic mapping.'' One of the datasets collected by the Human Connectome Project involved ultra high-field (7 Tesla) fMRI retinotopic mapping in 181 healthy young adults (1.6-mm resolution), yielding the largest freely available collection of retinotopy data. Here, we describe the experimental paradigm and the results of model-based analysis of the fMRI data. These results provide estimates of population receptive field position and size. Our analyses include both results from individual subjects as well as results obtained by averaging fMRI time series across subjects at each cortical and subcortical location and then fitting models. Both the group-average and individual-subject results reveal robust signals across much of the brain, including occipital, temporal, parietal, and frontal cortex as well as subcortical areas. The group-average results agree well with previously published parcellations of visual areas. In addition, split-half analyses show strong within-subject reliability, further demonstrating the high quality of the data. We make publicly available the analysis results for individual subjects and the group avera ge, as well as associated stimuli and analysis code. These resources provide an opportunity for studying fine-scale individual variability in cortical and subcortical organization and the properties of high-resolution fMRI. In addition, they provide a set of observations that can be compared with other Human Connectome Project measures acquired in these same participants.
Daniel K. Bjornn; Bonnie Brinton Anderson; Anthony Vance; Jeffrey L. Jenkins; C. Brock Kirwan
Tuning out security warnings: A longitudinal examination of habituation through fMRI, eye tracking, and field experiments Journal Article
In: MIS Quarterly, vol. 42, no. 2, pp. 355–380, 2018.
Research in the fields of information systems and human-computer interaction has shown that habituation— decreased response to repeated stimulation—is a serious threat to the effectiveness of security warnings. Although habituation is a neurobiological phenomenon that develops over time, past studies have only examined this problem cross-sectionally. Further, past studies have not examined how habituation influences actual security warning adherence in the field. For these reasons, the full extent of the problem of habituation is unknown. We address these gaps by conducting two complementary longitudinal experiments. First, we performed an experiment collecting fMRI and eye-tracking data simultaneously to directly measure habituation to security warnings as it develops in the brain over a five-day workweek. Our results show not only a general decline of participants' attention to warnings over time but also that attention recovers at least partially between workdays without exposure to the warnings. Further, we found that updating the appearance of a warning— that is, a polymorphic design—substantially reduced habituation of attention. Second, we performed a three-week field experiment in which users were naturally exposed to privacy permis-sion warnings as they installed apps on their mobile devices. Consistent with our fMRI results, users' warning adherence substantially decreased over the three weeks. However, for users who received polymorphic permis-sion warnings, adherence dropped at a substantially lower rate and remained high after three weeks, compared to users who received standard warnings. Together, these findings provide the most complete view yet of the problem of habituation to security warnings and demonstrate that polymorphic warnings can substantially improve adherence.
Johannes Bloechle; Stefan Huber; Elise Klein; Julia Bahnmueller; Korbinian Moeller; Johannes Rennig
Neuro-cognitive mechanisms of global Gestalt perception in visual quantification Journal Article
In: NeuroImage, vol. 181, pp. 359–369, 2018.
Recent neuroimaging studies identified posterior regions in the temporal and parietal lobes as neuro-functional correlates of subitizing and global Gestalt perception. Beyond notable overlap on a neuronal level both mechanisms are remarkably similar on a behavioral level representing both a specific form of visual top-down processing where single elements are integrated into a superordinate entity. In the present study, we investigated whether subitizing draws on principles of global Gestalt perception enabling rapid top-down processes of visual quantification. We designed two functional neuroimaging experiments: a task identifying voxels responding to global Gestalt stimuli in posterior temporo-parietal brain regions and a visual quantification task on dot patterns with magnitudes within and outside the subitizing range. We hypothesized that voxels activated in global Gestalt perception should respond stronger to dot patterns within than those outside the subitizing range. The results confirmed this prediction for left-hemispheric posterior temporo-parietal brain areas. Additionally, we trained a classifier with response patterns from global Gestalt perception to predict neural responses of visual quantification. With this approach we were able to classify from TPJ Gestalt ROIs of both hemispheres whether a trial requiring subitizing was processed. The present study demonstrates that mechanisms of subitizing seem to build on processes of high-level visual perception.