fMRI和MEG眼动追踪出版物
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2022 |
Yih-Shiuan Lin; Chien-Chung Chen; Mark W. Greenlee Neural correlates of lateral modulation and perceptual filling-in in center-surround radial sinusoidal gratings: An fMRI study Journal Article In: Scientific Reports, vol. 12, pp. 1–14, 2022. @article{Lin2022, We investigated lateral modulation effects with functional magnetic resonance imaging. We presented radial sinusoidal gratings in random sequence: a scotoma grating with two arc-shaped blank regions (scotomata) in the periphery, one in the left and one in the right visual field, a center grating containing pattern only in the scotoma regions, and a full-field grating where the pattern occupied the whole screen. On each trial, one of the three gratings flickered in counterphase for 10 s, followed by a blank period. Observers were instructed to perform a fixation task and report whether filling-in was experienced during the scotoma condition. The results showed that the blood-oxygen-level-dependent signal was reduced in areas corresponding to the scotoma regions in the full-field compared to the center condition in V1 to V3 areas, indicating a lateral inhibition effect when the surround was added to the center pattern. The univariate analysis results showed no difference between the filling-in and no-filling-in trials. However, multivariate pattern analysis results showed that classifiers trained on activation pattern in V1 to V3 could differentiate between filling-in and no-filling-in trials, suggesting that the neural activation pattern in visual cortex correlated with the subjective percept. |
Christina Lubinus; Wolfgang Einhäuser; Florian Schiller; Tilo Kircher; Benjamin Straube; Bianca M. Kemenade Action-based predictions affect visual perception, neural processing, and pupil size, regardless of temporal predictability Journal Article In: NeuroImage, vol. 263, pp. 1–13, 2022. @article{Lubinus2022, Sensory consequences of one's own action are often perceived as less intense, and lead to reduced neural responses, compared to externally generated stimuli. Presumably, such sensory attenuation is due to predictive mechanisms based on the motor command (efference copy). However, sensory attenuation has also been observed outside the context of voluntary action, namely when stimuli are temporally predictable. Here, we aimed at disentangling the effects of motor and temporal predictability-based mechanisms on the attenuation of sensory action consequences. During fMRI data acquisition, participants (N = 25) judged which of two visual stimuli was brighter. In predictable blocks, the stimuli appeared temporally aligned with their button press (active) or aligned with an automatically generated cue (passive). In unpredictable blocks, stimuli were presented with a variable delay after button press/cue, respectively. Eye tracking was performed to investigate pupil-size changes and to ensure proper fixation. Self-generated stimuli were perceived as darker and led to less neural activation in visual areas than their passive counterparts, indicating sensory attenuation for self-generated stimuli independent of temporal predictability. Pupil size was larger during self-generated stimuli, which correlated negatively with the blood oxygenation level dependent (BOLD) response: the larger the pupil, the smaller the BOLD amplitude in visual areas. Our results suggest that sensory attenuation in visual cortex is driven by action-based predictive mechanisms rather than by temporal predictability. This effect may be related to changes in pupil diameter. Altogether, these results emphasize the role of the efference copy in the processing of sensory action consequences. |
Björn Machner; Lara Braun; Jonathan Imholz; Philipp J. Koch; Thomas F. Münte; Christoph Helmchen; Andreas Sprenger In: Frontiers in Human Neuroscience, vol. 15, pp. 1–12, 2022. @article{Machner2022, Between-subject variability in cognitive performance has been related to inter-individual differences in functional brain networks. Targeting the dorsal attention network (DAN) we questioned (i) whether resting-state functional connectivity (FC) within the DAN can predict individual performance in spatial attention tasks and (ii) whether there is short-term adaptation of DAN-FC in response to task engagement. Twenty-seven participants first underwent resting-state fMRI (PRE run), they subsequently performed different tasks of spatial attention [including visual search (VS)] and immediately afterwards received another rs-fMRI (POST run). Intra- and inter-hemispheric FC between core hubs of the DAN, bilateral intraparietal sulcus (IPS) and frontal eye field (FEF), was analyzed and compared between PRE and POST. Furthermore, we investigated rs-fMRI-behavior correlations between the DAN-FC in PRE/POST and task performance parameters. The absolute DAN-FC did not change from PRE to POST. However, different significant rs-fMRI-behavior correlations were revealed for intra-/inter-hemispheric connections in the PRE and POST run. The stronger the FC between left FEF and IPS before task engagement, the better was the learning effect (improvement of reaction times) in VS (r = 0.521 |
Paola Mengotti; Anne Sophie Käsbauer; Gereon R. Fink; Simone Vossel In: Cerebral Cortex, vol. 32, pp. 4698–4714, 2022. @article{Mengotti2022, Updating beliefs after unexpected events is fundamental for an optimal adaptation to the environment. Previous findings suggested a causal involvement of the right temporoparietal junction (rTPJ) in belief updating in an attention task. We combined offline continuous theta-burst stimulation (cTBS) over rTPJ with functional magnetic resonance imaging (fMRI) to investigate local and remote stimulation effects within the attention and salience networks. In a sham-controlled, within-subject crossover design, 25 participants performed an attentional cueing task during fMRI with true or false information about cue predictability. By estimating learning rates from response times, we characterized participants' belief updating. Model-derived cue predictability entered the fMRI analysis as a parametric regressor to identify the neural correlates of updating. rTPJ-cTBS effects showed high interindividual variability. The expected learning rate reduction with false cue predictability information by cTBS was only observed in participants showing higher updating in false than in true blocks after sham. cTBS modulated the neural signatures of belief updating, both in rTPJ and in nodes of the attention and salience networks. The interindividual variability of the behavioral cTBS effect was related to differential activity and rTPJ connectivity of the right anterior insula. These results demonstrate a crucial interaction between ventral attention and salience networks for belief updating. |
Camille Métais; Judith Nicolas; Moussa Diarra; Alexis Cheviet; Eric Koun; Denis Pélisson Neural substrates of saccadic adaptation: Plastic changes versus error processing and forward versus backward learning Journal Article In: NeuroImage, vol. 262, pp. 1–15, 2022. @article{Metais2022, Previous behavioral, clinical, and neuroimaging studies suggest that the neural substrates of adaptation of saccadic eye movements involve, beyond the central role of the cerebellum, several, still incompletely determined, cortical areas. Furthermore, no neuroimaging study has yet tackled the differences between saccade lengthening ("forward adaptation") and shortening ("backward adaptation") and neither between their two main components, i.e. error processing and oculomotor changes. The present fMRI study was designed to fill these gaps. Blood-oxygen-level-dependent (BOLD) signal and eye movements of 24 healthy volunteers were acquired while performing reactive saccades under 4 conditions repeated in short blocks of 16 trials: systematic target jump during the saccade and in the saccade direction (forward: FW) or in the opposite direction (backward: BW), randomly directed FW or BW target jump during the saccade (random: RND) and no intra-saccadic target jump (stationary: STA). BOLD signals were analyzed both through general linear model (GLM) approaches applied at the whole-brain level and through sensitive Multi-Variate Pattern Analyses (MVPA) applied to 34 regions of interest (ROIs) identified from independent 'Saccade Localizer' functional data. Oculomotor data were consistent with successful induction of forward and backward adaptation in FW and BW blocks, respectively. The different analyses of voxel activation patterns (MVPAs) disclosed the involvement of 1) a set of ROIs specifically related to adaptation in the right occipital cortex, right and left MT/MST, right FEF and right pallidum; 2) several ROIs specifically involved in error signal processing in the left occipital cortex, left PEF, left precuneus, Medial Cingulate cortex (MCC), left inferior and right superior cerebellum; 3) ROIs specific to the direction of adaptation in the occipital cortex and MT/MST (left and right hemispheres for FW and BW, respectively) and in the pallidum of the right hemisphere (FW). The involvement of the left PEF and of the (left and right) occipital cortex were further supported and qualified by the whole brain GLM analysis: clusters of increased activity were found in PEF for the RND versus STA contrast (related to error processing) and in the left (right) occipital cortex for the FW (BW) versus STA contrasts [related to the FW (BW) direction of error and/or adaptation]. The present study both adds complementary data to the growing literature supporting a role of the cerebral cortex in saccadic adaptation through feedback and feedforward relationships with the cerebellum and provides the basis for improving conceptual frameworks of oculomotor plasticity and of its link with spatial cognition. |
Viola Mocz; Maryam Vaziri-pashkam; Marvin Chun; Yaoda Xu Predicting identity-preserving object transformations in human posterior parietal cortex and convolutional neural networks Journal Article In: Journal of Cognitive Neuroscience, vol. 34, pp. 2406–2435, 2022. @article{Mocz2022, Previous research shows that, within human occipito- temporal cortex (OTC), we can use a general linear mapping function to link visual object responses across nonidentity feature changes, including Euclidean features (e.g., position and size) and non-Euclidean features (e.g., image statistics and spatial frequency). Although the learned mapping is capable of predicting responses of objects not included in training, these predictions are better for categories included than those not included in training. These findings demonstrate a near-orthogonal representation of object identity and nonidentity features throughout human OTC. Here, we extended these findings to examine the mapping across both Euclidean and non-Euclidean feature changes in human posterior parietal cortex (PPC), including functionally defined regions in inferior and superior intraparietal sulcus. We additionally examined responses in five convolutional neural networks (CNNs) pretrained with object classification, as CNNs are considered as the current best model of the primate ventral visual system. We separately compared results from PPC and CNNs with those of OTC. We found that a linear mapping function could successfully link object responses in different states of nonidentity transformations in human PPC and CNNs for both Euclidean and non-Euclidean features. Over-all, we found that object identity and nonidentity features are represented in a near-orthogonal, rather than complete-orthogonal, manner in PPC and CNNs, just like they do in OTC. Meanwhile, some differences existed among OTC, PPC, and CNNs. These results demonstrate the similarities and differences in how visual object information across an identity-preserving image transformation may be represented in OTC, PPC, and CNNs |
Robert M. Mok; Bradley C. Love Abstract neural representations of category membership beyond information coding stimulus or response Journal Article In: Journal of Cognitive Neuroscience, vol. 34, no. 10, pp. 1719–1735, 2022. @article{Mok2022, For decades, researchers have debated whether mental representations are symbolic or grounded in sensory inputs and motor programs. Certainly, aspects of mental representations are grounded. However, does the brain also contain abstract concept representations that mediate between perception and action in a flexible manner not tied to the details of sensory inputs and motor programs? Such conceptual pointers would be useful when concepts remain constant despite changes in appearance and associated actions. We evaluated whether human participants acquire such representations using fMRI. Participants completed a probabilistic concept learning task in which sensory, motor, and category variables were not perfectly coupled or entirely independent, making it possible to observe evidence for abstract representations or purely grounded representations. To assess how the learned concept structure is represented in the brain, we examined brain regions implicated in flexible cognition (e.g., pFC and parietal cortex) that are most likely to encode an abstract representation removed from sensory–motor details. We also examined sensory–motor regions that might encode grounded sensory–motor-based representations tuned for categorization. Using a cognitive model to estimate participants' category rule and multivariate pattern analysis of fMRI data, we found the left pFC and human middle temporal visual area (MT)/V5 coded for category in the absence of information coding for stimulus or response. Because category was based on the stimulus, finding an abstract representation of category was not inevitable. Our results suggest that certain brain areas support categorization behavior by constructing concept representations in a format akin to a symbol that differs from stimulus–motor codes. |
Roy Moyal; Hamid B. Turker; Wen Ming Luh; Khena M. Swallow Auditory target detection enhances visual processing and hippocampal functional connectivity Journal Article In: Frontiers in Psychology, vol. 13, pp. 1–18, 2022. @article{Moyal2022, Though dividing one's attention between two input streams typically impairs performance, detecting a behaviorally relevant stimulus can sometimes enhance the encoding of unrelated information presented at the same time. Previous research has shown that selection of this kind boosts visual cortical activity and memory for concurrent items. An important unanswered question is whether such effects are reflected in processing quality and functional connectivity in visual regions and in the hippocampus. In this fMRI study, participants were asked to memorize a stream of naturalistic images and press a button only when they heard a predefined target tone (400 or 1,200 Hz, counterbalanced). Images could be presented with a target tone, with a distractor tone, or without a tone. Auditory target detection increased activity throughout the ventral visual cortex but lowered it in the hippocampus. Enhancements in functional connectivity between the ventral visual cortex and the hippocampus were also observed following auditory targets. Multi-voxel pattern classification of image category was more accurate on target tone trials than on distractor and no tone trials in the fusiform gyrus and parahippocampal gyrus. This effect was stronger in visual cortical clusters whose activity was more correlated with the hippocampus on target tone than on distractor tone trials. In agreement with accounts suggesting that subcortical noradrenergic influences play a role in the attentional boost effect, auditory target detection also caused an increase in locus coeruleus activity and phasic pupil responses. These findings outline a network of cortical and subcortical regions that are involved in the selection and processing of information presented at behaviorally relevant moments. |
Laura Müller-Pinzler; Nora Czekalla; Annalina V. Mayer; Alexander Schröder; David S. Stolz; Frieder M. Paulus; Sören Krach Neurocomputational mechanisms of affected beliefs Journal Article In: Communications Biology, vol. 5, no. 1, pp. 1–16, 2022. @article{MuellerPinzler2022, The feedback people receive on their behavior shapes the process of belief formation and self-efficacy in mastering a particular task. However, the neural and computational mechanisms of how the subjective value of self-efficacy beliefs, and the corresponding affect, influence the learning process remain unclear. We investigated these mechanisms during self-efficacy belief formation using fMRI, pupillometry, and computational modeling, and by analyzing individual differences in affective experience. Biases in the formation of self-efficacy beliefs were associated with affect, pupil dilation, and neural activity within the anterior insula, amygdala, ventral tegmental area/ substantia nigra, and mPFC. Specifically, neural and pupil responses mapped the valence of the prediction errors in correspondence with individuals' experienced affective states and learning biases during self-efficacy belief formation. Together with the functional connectivity dynamics of the anterior insula within this network, our results provide evidence for neural and computational mechanisms of how we arrive at affected beliefs. |
Abigail L. Noyce; Ray W. Lefco; James A. Brissenden; Sean M. Tobyne; Barbara G. Shinn-Cunningham; David C. Somers Extended frontal networks for visual and auditory working memory Journal Article In: Cerebral Cortex, vol. 32, pp. 855–869, 2022. @article{Noyce2022, Working memory (WM) supports the persistent representation of transient sensory information. Visual and auditory stimuli place different demands on WM and recruit different brain networks. Separate auditory- and visual-biased WM networks extend into the frontal lobes, but several challenges confront attempts to parcellate human frontal cortex, including fine-grained organization and between-subject variability. Here, we use differential intrinsic functional connectivity from 2 visual-biased and 2 auditory-biased frontal structures to identify additional candidate sensory-biased regions in frontal cortex. We then examine direct contrasts of task functional magnetic resonance imaging during visual versus auditory 2-back WM to validate those candidate regions. Three visual-biased and 5 auditory-biased regions are robustly activated bilaterally in the frontal lobes of individual subjects (N = 14, 7 women). These regions exhibit a sensory preference during passive exposure to task stimuli, and that preference is stronger during WM. Hierarchical clustering analysis of intrinsic connectivity among novel and previously identified bilateral sensory-biased regions confirms that they functionally segregate into visual and auditory networks, even though the networks are anatomically interdigitated. We also observe that the frontotemporal auditory WM network is highly selective and exhibits strong functional connectivity to structures serving non-WM functions, while the frontoparietal visual WM network hierarchically merges into the multiple-demand cognitive system. |
Jefferson Ortega; Chelsea Reichert Plaska; Bernard A. Gomes; Timothy M. Ellmore Spontaneous eye blink rate during the working memory delay period predicts task accuracy Journal Article In: Frontiers in Psychology, vol. 13, pp. 1–11, 2022. @article{Ortega2022, Spontaneous eye blink rate (sEBR) has been linked to attention and memory, specifically working memory (WM). sEBR is also related to striatal dopamine (DA) activity with schizophrenia and Parkinson's disease showing increases and decreases, respectively, in sEBR. A weakness of past studies of sEBR and WM is that correlations have been reported using blink rates taken at baseline either before or after performance of the tasks used to assess WM. The goal of the present study was to understand how fluctuations in sEBR during different phases of a visual WM task predict task accuracy. In two experiments, with recordings of sEBR collected inside and outside of a magnetic resonance imaging bore, we observed sEBR to be positively correlated with WM task accuracy during the WM delay period. We also found task-related modulation of sEBR, including higher sEBR during the delay period compared to rest, and lower sEBR during task phases (e.g., stimulus encoding) that place demands on visual attention. These results provide further evidence that sEBR could be an important predictor of WM task performance with the changes during the delay period suggesting a role in WM maintenance. The relationship of sEBR to DA activity and WM maintenance is discussed. |
Soo Hyun Park; Kenji W. Koyano; Brian E. Russ; Elena N. Waidmann; David B. T. McMahon; David A. Leopold Parallel functional subnetworks embedded in the macaque face patch system Journal Article In: Science Advances, vol. 8, pp. 1–8, 2022. @article{Park2022, During normal vision, our eyes provide the brain with a continuous stream of useful information about the world. How visually specialized areas of the cortex, such as face-selective patches, operate under natural modes of behavior is poorly understood. Here we report that, during the free viewing of movies, cohorts of face-selective neurons in the macaque cortex fractionate into distributed and parallel subnetworks that carry distinct information. We classified neurons into functional groups on the basis of their movie-driven coupling with functional magnetic resonance imaging time courses across the brain. Neurons from each group were distributed across multiple face patches but intermixed locally with other groups at each recording site. These findings challenge prevailing views about functional segregation in the cortex and underscore the importance of naturalistic paradigms for cognitive neuroscience. |
Jordan E. Pierce; Elizabeth Clancy; Nathan M. Petro; Michael D. Dodd; Maital Neta Task-irrelevant emotional faces impact BOLD responses more for prosaccades than antisaccades in a mixed saccade fMRI task Journal Article In: Neuropsychologia, vol. 177, pp. 1–8, 2022. @article{Pierce2022, Cognitive control allows individuals to flexibly and efficiently perform tasks by attending to relevant stimuli while inhibiting distraction from irrelevant stimuli. The antisaccade task assesses cognitive control by requiring participants to inhibit a prepotent glance towards a peripheral stimulus and generate an eye movement to the mirror image location. This task can be administered with various contextual manipulations to investigate how factors such as trial timing or emotional content interact with cognitive control. In the current study, 26 healthy adults completed a mixed antisaccade and prosaccade fMRI task that included task irrelevant emotional faces and gap/overlap timing. The results showed typical antisaccade and gap behavioral effects with greater BOLD activation in frontal and parietal brain regions for antisaccade and overlap trials. Conversely, there were no differences in behavior based on the emotion of the task irrelevant face, but trials with neutral faces had greater activation in widespread visual regions than trials with angry faces, particularly for prosaccade and overlap trials. Together, these effects suggest that a high level of cognitive control and inhibition was required throughout the task, minimizing the impact of the face presentation on saccade behavior, but leading to increased attention to the neutral faces on overlap prosaccade trials when both the task cue (look towards) and emotion stimulus (neutral, non-threatening) facilitated disinhibition of visual processing. |
McKinney Pitts; Derek Evan Nee Generalizing the control architecture of the lateral prefrontal cortex Journal Article In: Neurobiology of Learning and Memory, vol. 195, pp. 1–14, 2022. @article{Pitts2022a, Cognitive control guides non-habitual, goal directed behaviors allowing us to flexibly adapt to ongoing demands. Previous work has suggested that multiple cognitive control processes exist that can be classed according to their action on present-oriented/external information versus future-oriented/internal information. These processes can be mapped onto the lateral prefrontal cortex (LPFC) such that increasingly rostral areas are involved in increasingly future-oriented/internal control processes. Whether and how such processes are organized to support goal-directed behavior remains unclear. On the one hand, the LPFC may flexibly adapt based upon demands. On the other hand, there may be a consistent control architecture such as a control hierarchy that generalizes across demands. Previous work using fMRI in humans during a comprehensive control task that engaged several control processes at once found that an area in mid-LPFC consistently exerted widespread influence throughout the LPFC. These data suggested that the mid-LPFC forms an apex of a putative control hierarchy. However, whether such an architecture generalizes across tasks remains to be tested. Here, we utilized a modified comprehensive control task designed to alter how control processes influence one another to test the generalizability of the LPFC control architecture. Univariate fMRI activations revealed distinct control-related activations relative to past work. Despite these changes, effective connectivity modeling revealed a directed architecture similar to previous findings with the mid-LPFC exerting the most widespread influences throughout LPFC. These results suggest that the fundamental control architecture of the LPFC is relatively fixed, and that different demands are accommodated through modulations of this fixed architecture. |
Ignacio Polti; Matthias Nau; Raphael Kaplan; Virginie Wassenhove; Christian F. Doeller Rapid encoding of task regularities in the human hippocampus guides sensorimotor timing Journal Article In: eLife, vol. 11, pp. 1–22, 2022. @article{Polti2022, The brain encodes the statistical regularities of the environment in a task-specific yet flexible and generalizable format. Here, we seek to understand this process by bridging two parallel lines of research, one centered on sensorimotor timing, and the other on cognitive mapping in the hippocampal system. By combining functional magnetic resonance imaging (fMRI) with a fast-paced time-to-contact (TTC) estimation task, we found that the hippocampus signaled behavioral feedback received in each trial as well as performance improvements across trials along with reward-processing regions. Critically, it signaled performance improvements independent from the tested intervals, and its activity accounted for the trial-wise regression-to-the-mean biases in TTC estimation. This is in line with the idea that the hippocampus supports the rapid encoding of temporal context even on short time scales in a behavior-dependent manner. Our results emphasize the central role of the hippocampus in statistical learning and position it at the core of a brain-wide network updating sensorimotor representations in real time for flexible behavior. |
R. T. Pramod; Michael A. Cohen; Joshua B. Tenenbaum; Nancy Kanwisher Invariant representation of physical stability in the human brain Journal Article In: eLife, vol. 11, pp. 1–19, 2022. @article{Pramod2022, Successful engagement with the world requires the ability to predict what will happen next. Here, we investigate how the brain makes a fundamental prediction about the physical world: whether the situation in front of us is stable, and hence likely to stay the same, or unstable, and hence likely to change in the immediate future. Specifically, we ask if judgments of stability can be supported by the kinds of representations that have proven to be highly effective at visual object recognition in both machines and brains, or instead if the ability to determine the physical stability of natural scenes may require generative algorithms that simulate the physics of the world. To find out, we measured responses in both convolutional neural networks (CNNs) and the brain (using fMRI) to natural images of physically stable versus unstable scenarios. We find no evidence for generalizable representations of physical stability in either standard CNNs trained on visual object and scene classification (ImageNet), or in the human ventral visual pathway, which has long been implicated in the same process. However, in frontoparietal regions previously implicated in intuitive physical reasoning we find both scenario-invariant representations of physical stability, and higher univariate responses to unstable than stable scenes. These results demonstrate abstract representations of physical stability in the dorsal but not ventral pathway, consistent with the hypothesis that the computations underlying stability entail not just pattern classification but forward physical simulation. |
Sophia Antonia Press; Stefanie C. Biehl; C. Carolyn Vatheuer; Gregor Domes; Jennifer Svaldi Neural correlates of body image processing in binge eating disorder Journal Article In: Journal of Psychopathology and Clinical Science, vol. 131, no. 4, pp. 350–364, 2022. @article{Press2022, Although body image disturbances play a central role in the development, maintenance and relapse of binge eating disorder (BED), studies investigating the neural basis underlying body processing in BED are still missing. To address this gap, we conducted a preregistered (German Clinical Trials Register [Deutsches Register Klinischer Studien; DRKS], Registration DRKS00008107) combined functional magnetic resonance (fMRI)/eye tracking study in which 38 women with BED and 22 healthy controls weight-matched for overall equivalence processed images of their own bodies, an unfamiliar weight- matched body, and visually matched nonbody control stimuli while performing a one-back task. Women with BED responded with higher left fusiform body area (FBA) activity than controls during body image processing. Despite higher levels of self-reported body dissatisfaction, women with BED did not show overactivation in emotion-processing areas in response to their own body. The eye-track- ing results indicated that visual attention toward the presented stimuli was associated with increased ac- tivity in the extrastriate body area (EBA) and FBA across groups. Our results thus provide evidence for an aberrant neural processing of body images in BED and highlight the importance of controlling for visual attention in future studies assessing neuronal body processing. |
Emily J. Allen; Ghislain St-Yves; Yihan Wu; Jesse L. Breedlove; Jacob S. Prince; Logan T. Dowdle; Matthias Nau; Brad Caron; Franco Pestilli; Ian Charest; J. Benjamin Hutchinson; Thomas Naselaris; Kendrick Kay A massive 7T fMRI dataset to bridge cognitive neuroscience and artificial intelligence Journal Article In: Nature Neuroscience, vol. 25, no. 1, pp. 116–126, 2022. @article{Allen2022, Extensive sampling of neural activity during rich cognitive phenomena is critical for robust understanding of brain function. Here we present the Natural Scenes Dataset (NSD), in which high-resolution functional magnetic resonance imaging responses to tens of thousands of richly annotated natural scenes were measured while participants performed a continuous recognition task. To optimize data quality, we developed and applied novel estimation and denoising techniques. Simple visual inspections of the NSD data reveal clear representational transformations along the ventral visual pathway. Further exemplifying the inferential power of the dataset, we used NSD to build and train deep neural network models that predict brain activity more accurately than state-of-the-art models from computer vision. NSD also includes substantial resting-state and diffusion data, enabling network neuroscience perspectives to constrain and enhance models of perception and memory. Given its unprecedented scale, quality and breadth, NSD opens new avenues of inquiry in cognitive neuroscience and artificial intelligence. |
Bertrand Beffara; Fadila Hadj-Bouziane; Suliann Ben Hamed; C. Nico Boehler; Leonardo Chelazzi; Elisa Santandrea; Emiliano Macaluso In: NeuroImage, vol. 255, pp. 1–18, 2022. @article{Beffara2022, Visuo-spatial attention prioritizes the processing of relevant inputs via different types of signals, including current goals and stimulus salience. Complex mixtures of these signals engage in everyday life situations, but little is known about how these signals jointly modulate distributed patterns of activity across the occipital regions that represent visual space. Here, we measured spatio-topic, quadrant-specific occipital activity during the processing of visual displays containing both task-relevant targets and salient color-singletons. We computed spatial bias vectors indexing the effect of attention in 2D space, as coded by distributed activity in the occipital cortex. We found that goal-directed spatial attention biased activity towards the target and that salience further modulated this endogenous effect: salient distractors decreased the spatial bias, while salient targets increased it. Analyses of effective connectivity revealed that the processing of salient distractors relied on the modulation of the bidirectional connectivity between the occipital and the posterior parietal cortex, as well as the modulation of the lateral interactions within the occipital cortex. These findings demonstrate that goal-directed attention and salience jointly contribute to shaping processing priorities in the occipital cortex and highlight that multiple functional paths determine how spatial information about these signals is distributed across occipital regions. |
Daniel K. Bjornn; Julie Van; C. Brock Kirwan The contributions of eye gaze fixations and target-lure similarity to behavioral and fMRI indices of pattern separation and pattern completion Journal Article In: Cognitive Neuroscience, vol. 13, no. 3-4, pp. 171–181, 2022. @article{Bjornn2022, Pattern separation and pattern completion are generally studied in humans using mnemonic discrimination tasks such as the Mnemonic Similarity Task (MST) where participants identify similar lures and repeated items from a series of images. Failures to correctly discriminate lures are thought to reflect a failure of pattern separation and a propensity toward pattern completion. Recent research has challenged this perspective, suggesting that poor encoding rather than pattern completion accounts for the occurrence of false alarm responses to similar lures. In two experiments, participants completed a continuous recognition task version of the MST while eye movement (Experiments 1 and 2) and fMRI data (Experiment 2) were collected. In Experiment 1, we replicated the result that fixation counts at study predicted accuracy on lure trials (consistent with poor encoding predicting mnemonic discrimination performance), but this effect was not observed in our fMRI task. In both experiments, we found that target-lure similarity was a strong predictor of accuracy on lure trials. Further, we found that fMRI activation changes in the hippocampus were significantly correlated with the number of fixations at study for correct but not incorrect mnemonic discrimination judgments when controlling for target-lure similarity. Our findings indicate that while eye movements during encoding predict subsequent hippocampal activation changes for correct mnemonic discriminations, the predictive power of eye movements for activation changes for incorrect mnemonic discrimination trials was modest at best. |
Charlie S. Burlingham; Minyoung Ryoo; Zvi N. Roth; Saghar Mirbagheri; David J. Heeger; Elisha P. Merriam Task-related hemodynamic responses in human early visual cortex are modulated by task difficulty and behavioral performance Journal Article In: eLife, vol. 11, pp. 1–24, 2022. @article{Burlingham2022a, Early visual cortex exhibits widespread hemodynamic responses in the absence of visual stimulation, which are entrained to the timing of a task and not predicted by local spiking or local field potential. Such task-related responses (TRRs) covary with reward magnitude and physiological signatures of arousal. It is unknown, however, if TRRs change on a trial-to-trial basis according to behavioral performance and task difficulty. If so, this would suggest that TRRs reflect arousal on a trial-to-trial timescale and covary with critical task and behavioral variables. We measured functional magnetic resonance imaging blood-oxygen-level-dependent (fMRI-BOLD) responses in the early visual cortex of human observers performing an orientation discrimination task consisting of separate easy and hard runs of trials. Stimuli were presented in a small portion of one hemifield, but the fMRI response was measured in the ipsilateral hemisphere, far from the stimulus representation and focus of spatial attention. TRRs scaled in amplitude with task difficulty, behavioral accuracy, reaction time, and lapses across trials. These modulations were not explained by the influence of respiration, cardiac activity, or head movement on the fMRI signal. Similar modulations with task difficulty and behavior were observed in pupil size. These results suggest that TRRs reflect arousal and behavior on the timescale of individual trials. |
Lisa Byrge; Dorit Kliemann; Ye He; Hu Cheng; Julian Michael Tyszka; Ralph Adolphs; Daniel P. Kennedy Video-evoked fMRI BOLD responses are highly consistent across different data acquisition sites Journal Article In: Human Brain Mapping, vol. 43, no. 9, pp. 2972–2991, 2022. @article{Byrge2022, Naturalistic imaging paradigms, in which participants view complex videos in the scanner, are increasingly used in human cognitive neuroscience. Videos evoke temporally synchronized brain responses that are similar across subjects as well as within subjects, but the reproducibility of these brain responses across different data acquisition sites has not yet been quantified. Here, we characterize the consistency of brain responses across independent samples of participants viewing the same videos in functional magnetic resonance imaging (fMRI) scanners at different sites (Indiana University and Caltech). We compared brain responses collected at these different sites for two carefully matched datasets with identical scanner models, acquisition, and preprocessing details, along with a third unmatched dataset in which these details varied. Our overall conclusion is that for matched and unmatched datasets alike, video-evoked brain responses have high consistency across these different sites, both when compared across groups and across pairs of individuals. As one might expect, differences between sites were larger for unmatched datasets than matched datasets. Residual differences between datasets could in part reflect participant-level variability rather than scanner- or data- related effects. Altogether our results indicate promise for the development and, critically, generalization of video fMRI studies of individual differences in healthy and clinical populations alike. |
Youngsun T. Cho; Flora Moujaes; Charles H. Schleifer; Martina Starc; Jie Lisa Ji; Nicole Santamauro; Brendan Adkinson; Antonija Kolobaric; Morgan Flynn; John H. Krystal; John D. Murray; Grega Repovs; Alan Anticevic Reward and loss incentives improve spatial working memory by shaping trial-by-trial posterior frontoparietal signals Journal Article In: NeuroImage, vol. 254, pp. 1–15, 2022. @article{Cho2022a, Integrating motivational signals with cognition is critical for goal-directed activities. The mechanisms that link neural changes with motivated working memory continue to be understood. Here, we tested how externally cued and non-cued (internally represented) reward and loss impact spatial working memory precision and neural circuits in human subjects using fMRI. We translated the classic delayed-response spatial working memory paradigm from non-human primate studies to take advantage of a continuous numeric measure of working memory precision, and the wealth of translational neuroscience yielded by these studies. Our results demonstrated that both cued and non-cued reward and loss improved spatial working memory precision. Visual association regions of the posterior prefrontal and parietal cortices, specifically the precentral sulcus (PCS) and intraparietal sulcus (IPS), had increased BOLD signal during incentivized spatial working memory. A subset of these regions had trial-by-trial increases in BOLD signal that were associated with better working memory precision, suggesting that these regions may be critical for linking neural signals with motivated working memory. In contrast, regions straddling executive networks, including areas in the dorsolateral prefrontal cortex, anterior parietal cortex and cerebellum displayed decreased BOLD signal during incentivized working memory. While reward and loss similarly impacted working memory processes, they dissociated during feedback when money won or avoided in loss was given based on working memory performance. During feedback, the trial-by-trial amount and valence of reward/loss received was dissociated amongst regions such as the ventral striatum, habenula and periaqueductal gray. Overall, this work suggests motivated spatial working memory is supported by complex sensory processes, and that the IPS and PCS in the posterior frontoparietal cortices may be key regions for integrating motivational signals with spatial working memory precision. |
Nicolas Clairis; Mathias Pessiglione Value, confidence, deliberation: A functional partition of the medial prefrontal cortex demonstrated across rating and choice tasks Journal Article In: Journal of Neuroscience, vol. 42, no. 28, pp. 1–41, 2022. @article{Clairis2022, Deciding about courses of action involves minimizing costs and maximizing benefits. Decision neuroscience studies have implicated both the ventral and dorsal medial PFC (vmPFC and dmPFC) in signaling goal value and action cost, but the precise functional role of these regions is still a matter of debate. Here, we suggest a more general functional partition that applies not only to decisions but also to judgments about goal value (expected reward) and action cost (expected effort). In this conceptual framework, cognitive representations related to options (reward value and effort cost) are dissociated from metacognitive representations (confidence and deliberation) related to solving the task (providing a judgment or making a choice). We used an original approach aimed at identifying consistencies across several preference tasks, from likeability ratings to binary decisions involving both attribute integration and option comparison. fMRI results in human male and female participants confirmed the vmPFC as a generic valuation system, its activity increasing with reward value and decreasing with effort cost. In contrast, more dorsal regions were not concerned with the valuation of options but with metacognitive variables, confidence being reflected in mPFC activity and deliberation time in dmPFC activity. Thus, there was a dissociation between the effort attached to choice options (represented in the vmPFC) and the effort invested in deliberation (represented in the dmPFC), the latter being expressed in pupil dilation. More generally, assessing commonalities across preference tasks might help in reaching a unified view of the neural mechanisms underlying the cost/benefit tradeoffs that drive human behavior. |
Xiaohui Cui; Fabio Richlan; Wei Zhou Fixation-related fMRI analysis reveals the neural basis of parafoveal processing in self-paced reading of Chinese words Journal Article In: Brain Structure and Function, vol. 227, no. 8, pp. 2609–2621, 2022. @article{Cui2022a, While parafoveal word processing plays an important role in natural reading, the underlying neural mechanism remains unclear. The present study investigated the neural basis of parafoveal processing during Chinese word reading with the co-registration of eye-tracking and functional magnetic resonance imaging (fMRI) using fixation-related fMRI analysis. In the gaze-contingent boundary paradigm, preview conditions (words that are identical, orthographically similar, and unrelated to target words), pre-target word frequency and target word frequency were manipulated. When fixating the pre-target word, the identical preview condition elicited lower brain activation in the left fusiform gyrus relative to unrelated and orthographically similar preview conditions and there were significant interactions of preview condition and pre-target word frequency on brain activation of the left middle frontal gyrus, left fusiform gyrus and supplementary motor area. When fixating the target word, there was a significant main effect of preview condition on brain activation of the right fusiform gyrus and a significant interaction of preview condition and pre-target word frequency on brain activation of the left middle frontal gyrus. These results suggest that fixation-related brain activation provides immediate measures and new perspectives to understand the mechanism of parafoveal processing in self-paced reading. |
Jasper H. Fabius; Katarina Moravkova; Alessio Fracasso Topographic organization of eye-position dependent gain fields in human visual cortex Journal Article In: Nature Communications, vol. 13, no. 1, pp. 1–16, 2022. @article{Fabius2022, The ability to move has introduced animals with the problem of sensory ambiguity: the position of an external stimulus could change over time because the stimulus moved, or because the animal moved its receptors. This ambiguity can be resolved with a change in neural response gain as a function of receptor orientation. Here, we developed an encoding model to capture gain modulation of visual responses in high field (7 T) fMRI data. We characterized population eye-position dependent gain fields (pEGF). The information contained in the pEGFs allowed us to reconstruct eye positions over time across the visual hierarchy. We discovered a systematic distribution of pEGF centers: pEGF centers shift from contra- to ipsilateral following pRF eccentricity. Such a topographical organization suggests that signals beyond pure retinotopy are accessible early in the visual hierarchy, providing the potential to solve sensory ambiguity and optimize sensory processing information for functionally relevant behavior. |
Farzad V. Farahani; Waldemar Karwowski; Mark D'Esposito; Richard F. Betzel; Pamela K. Douglas; Anna Maria Sobczak; Bartosz Bohaterewicz; Tadeusz Marek; Magdalena Fafrowicz Diurnal variations of resting-state fMRI data: A graph-based analysis Journal Article In: NeuroImage, vol. 256, pp. 1–25, 2022. @article{Farahani2022, Circadian rhythms (lasting approximately 24 h) control and entrain various physiological processes, ranging from neural activity and hormone secretion to sleep cycles and eating habits. Several studies have shown that time of day (TOD) is associated with human cognition and brain functions. In this study, utilizing a chronotype-based paradigm, we applied a graph theory approach on resting-state functional MRI (rs-fMRI) data to compare whole-brain functional network topology between morning and evening sessions and between morning-type (MT) and evening-type (ET) participants. Sixty-two individuals (31 MT and 31 ET) underwent two fMRI sessions, approximately 1 hour (morning) and 10 h (evening) after their wake-up time, according to their declared habitual sleep-wake pattern on a regular working day. In the global analysis, the findings revealed the effect of TOD on functional connectivity (FC) patterns, including increased small-worldness, assortativity, and synchronization across the day. However, we identified no significant differences based on chronotype categories. The study of the modular structure of the brain at mesoscale showed that functional networks tended to be more integrated with one another in the evening session than in the morning session. Local/regional changes were affected by both factors (i.e., TOD and chronotype), mostly in areas associated with somatomotor, attention, frontoparietal, and default networks. Furthermore, connectivity and hub analyses revealed that the somatomotor, ventral attention, and visual networks covered the most highly connected areas in the morning and evening sessions: the latter two were more active in the morning sessions, and the first was identified as being more active in the evening. Finally, we performed a correlation analysis to determine whether global and nodal measures were associated with subjective assessments across participants. Collectively, these findings contribute to an increased understanding of diurnal fluctuations in resting brain activity and highlight the role of TOD in future studies on brain function and the design of fMRI experiments. |
Mahtab Farahbakhsh; Elaine J. Anderson; Roni O. Maimon-Mor; Andy Rider; John A. Greenwood; Nashila Hirji; Serena Zaman; Pete R. Jones; D. Samuel Schwarzkopf; Geraint Rees; Michel Michaelides; Tessa M. Dekker A demonstration of cone function plasticity after gene therapy in achromatopsia Journal Article In: Brain, vol. 145, pp. 3803–3815, 2022. @article{Farahbakhsh2022, Recent advances in regenerative therapy have placed the treatment of previously incurable eye diseases within arms' reach. Achromatopsia is a severe monogenic heritable retinal disease that disrupts cone function from birth, leaving patients with complete colour blindness, low acuity, photosensitivity and nystagmus. While successful gene-replacement therapy in non-primate models of achromatopsia has raised widespread hopes for clinical treatment, it was yet to be determined if and how these therapies can induce new cone function in the human brain. Using a novel multimodal approach, we demonstrate for the first time that gene therapy can successfully activate dormant cone-mediated pathways in children with achromatopsia (CNGA3- and CNGB3-associated, 10–15 years). To test this, we combined functional MRI population receptive field mapping and psychophysics with stimuli that selectively measure cone photoreceptor signalling. We measured cortical and visual cone function before and after gene therapy in four paediatric patients, evaluating treatment-related change against benchmark data from untreated patients (n = 9) and normal-sighted participants (n = 28). After treatment, two of the four children displayed strong evidence for novel cone-mediated signals in visual cortex, with a retinotopic pattern that was not present in untreated achromatopsia and which is highly unlikely to emerge by chance. Importantly, this change was paired with a significant improvement in psychophysical measures of cone-mediated visual function. These improvements were specific to the treated eye, and provide strong evidence for successful read-out and use of new cone-mediated information. These data show for the first time that gene replacement therapy in achromatopsia within the plastic period of development can awaken dormant cone-signalling pathways after years of deprivation. This reveals unprecedented neural plasticity in the developing human nervous system and offers great promise for emerging regenerative therapies. |
Julia Fietz; Dorothee Pöhlchen; Florian P. Binder; Michael Czisch; Philipp G. Sämann; Victor I. Spoormaker Pupillometry tracks cognitive load and salience network activity in a working memory functional magnetic resonance imaging task Journal Article In: Human Brain Mapping, vol. 43, no. 2, pp. 665–680, 2022. @article{Fietz2022, The diameter of the human pupil tracks working memory processing and is associated with activity in the frontoparietal network. At the same time, recent neuroimaging research has linked human pupil fluctuations to activity in the salience network. In this combined functional magnetic resonance imaging (fMRI)/pupillometry study, we recorded the pupil size of healthy human participants while they performed a blockwise organized working memory task (N-back) inside an MRI scanner in order to monitor the pupil fluctuations associated neural activity during working memory processing. We first confirmed that mean pupil size closely followed working memory load. Combining this with fMRI data, we focused on blood oxygen level dependent (BOLD) correlates of mean pupil size modeled onto the task blocks as a parametric modulation. Interrogating this modulated task regressor, we were able to retrieve the frontoparietal network. Next, to fully exploit the within-block dynamics, we divided the blocks into 1 s time bins and filled these with corresponding pupil change values (first-order derivative of pupil size). We found that pupil change within N-back blocks was positively correlated with BOLD amplitudes in the areas of the salience network (namely bilateral insula, and anterior cingulate cortex). Taken together, fMRI with simultaneous measurement of pupil parameters constitutes a valuable tool to dissect working memory subprocesses related to both working memory load and salience of the presented stimuli. |
Joshua J. Foster; Sam Ling Feature-based attention multiplicatively scales the fMRI-BOLD contrast-response function Journal Article In: Journal of Neuroscience, vol. 42, no. 36, pp. 6894–6906, 2022. @article{Foster2022, fMRI plays a key role in the study of attention. However, there remains a puzzling discrepancy between attention effects measured with fMRI and with electrophysiological methods. While electrophysiological studies find that attention increases sensory gain, amplifying stimulus-evoked neural responses by multiplicatively scaling the contrast-response function (CRF), fMRI appears to be insensitive to these multiplicative effects. Instead, fMRI studies typically find that attention produces an additive baseline shift in the BOLD signal. These findings suggest that attentional effects measured with fMRI reflect top-down inputs to visual cortex, rather than the modulation of sensory gain. If true, this drastically limits what fMRI can tell us about how attention improves sensory coding. Here, we examined whether fMRI is sensitive to multiplicative effects of attention using a feature-based attention paradigm designed to preclude any possible additive effects. We measured BOLD activity evoked by a probe stimulus in one visual hemifield while participants (6 male, 6 female) attended to the probe orientation (attended condition), or to an orthogonal orientation (unattended condition), in the other hemifield. To measure CRFs in visual areas V1-V3, we parametrically varied the contrast of the probe stimulus. In all three areas, feature-based attention increased contrast gain, improving sensitivity by shifting CRFs toward lower contrasts. In V2 and V3, we also found an increase in response gain, an increase in the responsivity of the CRF, that was greatest at inner eccentricities. These results provide clear evidence that the fMRI-BOLD signal is sensitive to multiplicative effects of attention. |
Mathilda Froesel; Maëva Gacoin; Simon Clavagnier; Marc Hauser; Quentin Goudard; Suliann Ben Hamed Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain Journal Article In: Nature Communications, vol. 13, no. 1, pp. 1–17, 2022. @article{Froesel2022, Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality. |
Clément M. Garin; Yuki Hori; Stefan Everling; Christopher T. Whitlow; Finnegan J. Calabro; Beatriz Luna; Mathilda Froesel; Maëva Gacoin; Suliann Ben Hamed; Marc Dhenain; Christos Constantinidis An evolutionary gap in primate default mode network organization Journal Article In: Cell Reports, vol. 39, no. 2, pp. 1–17, 2022. @article{Garin2022, The human default mode network (DMN) is engaged at rest and in cognitive states such as self-directed thoughts. Interconnected homologous cortical areas in primates constitute a network considered as the equivalent. Here, based on a cross-species comparison of the DMN between humans and non-hominoid primates (macaques, marmosets, and mouse lemurs), we report major dissimilarities in connectivity profiles. Most importantly, the medial prefrontal cortex (mPFC) of non-hominoid primates is poorly engaged with the posterior cingulate cortex (PCC), though strong correlated activity between the human PCC and the mPFC is a key feature of the human DMN. Instead, a fronto-temporal resting-state network involving the mPFC was detected consistently across non-hominoid primate species. These common functional features shared between non-hominoid primates but not with humans suggest a substantial gap in the organization of the primate's DMN and its associated cognitive functions. |
Laura S. Geurts; James R. H. Cooke; Ruben S. Bergen; Janneke F. M. Jehee Subjective confidence reflects representation of Bayesian probability in cortex Journal Article In: Nature Human Behaviour, vol. 6, pp. 294–305, 2022. @article{Geurts2022, What gives rise to the human sense of confidence? Here we tested the Bayesian hypothesis that confidence is based on a probability distribution represented in neural population activity. We implemented several computational models of confidence and tested their predictions using psychophysics and functional magnetic resonance imaging. Using a generative model-based decoding technique, we extracted probability distributions from neural population activity in human visual cortex. We found that subjective confidence tracks the shape of the decoded distribution. That is, when sensory evidence was more precise, as indicated by the decoded distribution, observers reported higher levels of confidence. We furthermore found that neural activity in the insula, anterior cingulate and prefrontal cortex was linked to both the shape of the decoded distribution and reported confidence, in ways consistent with the Bayesian model. Altogether, our findings support recent statistical theories of confidence and suggest that probabilistic information guides the computation of one's sense of confidence. |
Camille Giacometti; Audrey Dureux; Delphine Autran-Clavagnier; Charles R. E. Wilson; Jérôme Sallet; Manon Dirheimer; Emmanuel Procyk; Fadila Hadj-Bouziane; Céline Amiez Frontal cortical functional connectivity is impacted by anaesthesia in macaques Journal Article In: Cerebral Cortex, vol. 32, pp. 4050–4067, 2022. @article{Giacometti2022, A critical aspect of neuroscience is to establish whether and how brain networks evolved across primates. To date, most comparative studies have used resting-state functional magnetic resonance imaging (rs-fMRI) in anaesthetized nonhuman primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investigated the impact of the awareness state (anaesthesia vs. awake) within the same group of macaque monkeys on the rs-fMRI functional connectivity organization of a well-characterized network in the human brain, the cingulo-frontal lateral network. Results in awake macaques show that rostral seeds in the cingulate sulcus exhibited stronger correlation strength with rostral compared to caudal lateral frontal cortical areas, while more caudal seeds displayed stronger correlation strength with caudal compared to anterior lateral frontal cortical areas. Critically, this inverse rostro-caudal functional gradient was abolished under anaesthesia. This study demonstrated a similar functional connectivity (FC) organization of the cingulo-frontal cortical network in awake macaque to that previously uncovered in the human brain pointing toward a preserved FC organization from macaque to human. However, it can only be observed in awake state suggesting that this network is sensitive to anaesthesia and warranting significant caution when comparing FC patterns across species under different states. |
Mengyuan Gong; Yilin Chen; Taosheng Liu Preparatory attention to visual features primarily relies on non-sensory representation Journal Article In: Scientific Reports, vol. 12, no. 1, pp. 1–12, 2022. @article{Gong2022, Prior knowledge of behaviorally relevant information promotes preparatory attention before the appearance of stimuli. A key question is how our brain represents the attended information during preparation. A sensory template hypothesis assumes that preparatory signals evoke neural activity patterns that resembled the perception of the attended stimuli, whereas a non-sensory, abstract template hypothesis assumes that preparatory signals reflect the abstraction of attended stimuli. To test these hypotheses, we used fMRI and multivariate analysis to characterize neural activity patterns when human participants were prepared to attend a feature and then select it from a compound stimulus. In an fMRI experiment using basic visual feature (motion direction), we observed reliable decoding of the to-be-attended feature from the preparatory activity in both visual and frontoparietal areas. However, while the neural patterns constructed by a single feature from a baseline task generalized to the activity patterns during stimulus selection, they could not generalize to the activity patterns during preparation. Our findings thus suggest that neural signals during attentional preparation are predominantly non-sensory in nature that may reflect an abstraction of the attended feature. Such a representation could provide efficient and stable guidance of attention. |
Evan M. Gordon; Timothy O. Laumann; Scott Marek; Dillan J. Newbold; Jacqueline M. Hampton; Nicole A. Seider; David F. Montez; Ashley M. Nielsen; Andrew N. Van; Annie Zheng; Ryland Miller; Joshua S. Siegel; Benjamin P. Kay; Abraham Z. Snyder; Deanna J. Greene; Bradley L. Schlaggar; Steven E. Petersen; Steven M. Nelson; Nico U. F. Dosenbach Individualized functional subnetworks connect human striatum and frontal cortex Journal Article In: Cerebral Cortex, vol. 32, no. 13, pp. 2868–2884, 2022. @article{Gordon2022, The striatum and cerebral cortex are interconnected via multiple recurrent loops that play a major role in many neuropsychiatric conditions. Primate corticostriatal connections can be precisely mapped using invasive tract-tracing. However, noninvasive human research has not mapped these connections with anatomical precision, limited in part by the practice of averaging neuroimaging data across individuals. Here we utilized highly sampled resting-state functional connectivity MRI for individual-specific precision functional mapping (PFM) of corticostriatal connections. We identified ten individual-specific subnetworks linking cortex—predominately frontal cortex—to striatum, most of which converged with nonhuman primate tract-tracing work. These included separable connections between nucleus accumbens core/shell and orbitofrontal/medial frontal gyrus; between anterior striatum and dorsomedial prefrontal cortex; between dorsal caudate and lateral prefrontal cortex; and between middle/posterior putamen and supplementary motor/primary motor cortex. Two subnetworks that did not converge with nonhuman primates were connected to cortical regions associated with human language function. Thus, precision subnetworks identify detailed, individual-specific, neurobiologically plausible corticostriatal connectivity that includes human-specific language networks. |
Marcus Grueschow; Birgit Kleim; Christian Carl Ruff Functional coupling of the locus coeruleus is linked to successful cognitive control Journal Article In: Brain Sciences, vol. 12, no. 3, pp. 1–15, 2022. @article{Grueschow2022, The locus coeruleus (LC) is a brainstem structure that sends widespread efferent projections throughout the mammalian brain. The LC constitutes the major source of noradrenaline (NE), a modulatory neurotransmitter that is crucial for fundamental brain functions such as arousal, attention, and cognitive control. This role of the LC-NE is traditionally not believed to reflect functional influences on the frontoparietal network or the striatum, but recent advances in chemogenetic manipulations of the rodent brain have challenged this notion. However, demonstrations of LCNE functional connectivity with these areas in the human brain are surprisingly sparse. Here, we close this gap. Using an established emotional stroop task, we directly compared trials requiring response conflict control with trials that did not require this, but were matched for visual stimulus properties, response modality, and controlled for pupil dilation differences across both trial types. We found that LC-NE functional coupling with the parietal cortex and regions of the striatum is substantially enhanced during trials requiring response conflict control. Crucially, the strength of this functional coupling was directly related to individual reaction time differences incurred by conflict resolution. Our data concur with recent rodent findings and highlight the importance of converging evidence between human and nonhuman neurophysiology to further understand the neural systems supporting adaptive and maladaptive behavior in health and disease. |
Hengda He; Nabil Ettehadi; Amir Shmuel; Qolamreza R. Razlighi Evidence suggesting common mechanisms underlie contralateral and ipsilateral negative BOLD responses in the human visual cortex Journal Article In: NeuroImage, vol. 262, pp. 1–13, 2022. @article{He2022a, The task-evoked positive BOLD response (PBR) to a unilateral visual hemi-field stimulation is often accompanied by robust and sustained contralateral as well as ipsilateral negative BOLD responses (NBRs) in the visual cortex. The signal characteristics and the neural and/or vascular mechanisms that underlie these two types of NBRs are not completely understood. In this paper, we investigated the properties of these two types of NBRs. We first demonstrated the linearity of both NBRs with respect to stimulus duration. Next, we showed that the hemodynamic response functions (HRFs) of the two NBRs were similar to each other, but significantly different from that of the PBR. Moreover, the subject-wise expressions of the two NBRs were tightly coupled to the degree that the correlation between the two NBRs was significantly higher than the correlation between each NBR and the PBR. However, the activation patterns of the two NBRs did not show a high level of interhemispheric spatial similarity, and the functional connectivity between them was not different than the interhemispheric functional connectivity between the NBRs and PBR. Finally, while attention did modulate both NBRs, the attention-related changes in their HRFs were similar. Our findings suggest that the two NBRs might be generated through common neural and/or vascular mechanisms involving distal/deep brain regions that project to the two hemispheres. |
Juyoen Hur; Manuel Kuhn; Shannon E. Grogans; Allegra S. Anderson; Samiha Islam; Hyung Cho Kim; Rachael M. Tillman; Andrew S. Fox; Jason F. Smith; Kathryn A. DeYoung; Alexander J. Shackman Anxiety-related frontocortical activity is associated with dampened stressor reactivity in the real world Journal Article In: Psychological Science, vol. 33, no. 6, pp. 906–924, 2022. @article{Hur2022, Negative affect is a fundamental dimension of human emotion. When extreme, it contributes to a variety of adverse outcomes, from physical and mental illness to divorce and premature death. Mechanistic work in animals and neuroimaging research in humans and monkeys have begun to reveal the broad contours of the neural circuits governing negative affect, but the relevance of these discoveries to everyday distress remains incompletely understood. Here, we used a combination of approaches—including neuroimaging assays of threat anticipation and emotional-face perception and more than 10,000 momentary assessments of emotional experience—to demonstrate that individuals who showed greater activation in a cingulo-opercular circuit during an anxiety-eliciting laboratory paradigm experienced lower levels of stressor-dependent distress in their daily lives (ns = 202–208 university students). Extended amygdala activation was not significantly related to momentary negative affect. These observations provide a framework for understanding the neurobiology of negative affect in the laboratory and in the real world. |
Tarik Jamoulle; Qian Ran; Karen Meersmans; Jolien Schaeverbeke; Patrick Dupont; Rik Vandenberghe Posterior intraparietal sulcus mediates detection of salient stimuli outside the endogenous focus of attention Journal Article In: Cerebral Cortex, vol. 32, pp. 1455–1469, 2022. @article{Jamoulle2022, Visual consciousness is shaped by the interplay between endogenous selection and exogenous capture. If stimulus saliency is aligned with a subject's attentional priorities, endogenous selection will be facilitated. In case of a misalignment, endogenous selection may be compromised as attentional capture is a strong and automatic process. We manipulated task-congruent versus -incongruent saliency in a functional magnetic resonance imaging change-detection task and analyzed brain activity patterns in the cortex surrounding the intraparietal sulcus (IPS) within the Julich-Brain probabilistic cytoarchitectonic mapping reference frame. We predicted that exogenous effects would be seen mainly in the posterior regions of the IPS (hIP4-hIP7-hIP8), whereas a conflict between endogenous and exogenous orienting would elicit activity from more anterior cytoarchitectonic areas (hIP1-hIP2-hIP3). Contrary to our hypothesis, a conflict between endogenous and exogenous orienting had an effect early in the IPS (mainly in hIP7 and hIP8). This is strong evidence for an endogenous component in hIP7/8 responses to salient stimuli beyond effects of attentional bottom-up sweep. Our results suggest that hIP7 and hIP8 are implicated in the individuation of attended locations based on saliency as well as endogenous instructions. |
Romuald A. Janik; Igor T. Podolak; Łukasz Struski; Anna Ceglarek; Koryna Lewandowska; Barbara Sikora-Wachowicz; Tadeusz Marek; Magdalena Fafrowicz Neural spatio-temporal patterns of information processing related to cognitive conflict and correct or false recognitions Journal Article In: Scientific Reports, vol. 12, no. 1, pp. 1–19, 2022. @article{Janik2022, Using a visual short-term memory task and employing a new methodological approach, we analyzed neural responses from the perspective of the conflict level and correctness/erroneous over a longer time window. Sixty-five participants performed the short-term memory task in the fMRI scanner. We explore neural spatio-temporal patterns of information processing in the context of correct or erroneous response and high or low level of cognitive conflict using classical fMRI analysis, surface-based cortical data, temporal analysis of interpolated mean activations, and machine learning classifiers. Our results provide evidence that information processing dynamics during the retrieval process vary depending on the correct or false recognition—for stimuli inducing a high level of cognitive conflict and erroneous response, information processing is prolonged. The observed phenomenon may be interpreted as the manifestation of the brain's preparation for future goal-directed action. |
Zhenlan Jin; Dong-gang Jin; Min Xiao; Aolin Ding; Jing Tian; Junjun Zhang; Ling Li In: Brain Structure and Function, vol. 227, no. 8, pp. 2623–2632, 2022. @article{Jin2022, Antisaccade task requires inhibition of a prepotent prosaccade to a peripheral target and initiation of a saccade to the opposite location, and, therefore, is used as a tool to investigate behavioral adjustment. The frontal and parietal cortices are both known for their activation during saccade generation, but it is unclear whether their neuroanatomical characteristics also contribute to antisaccades. Here, we took antisaccade cost (antisaccade latency minus prosaccade latency) as an index for additional time for generating antisaccades. Fifty-eight participants conducted pro and antisaccade tasks outside the magnetic resonance imaging (MRI) scanner and their structural MRI (sMRI) data were also collected to explore brain regions neuroanatomically related to antisaccade cost. Then, twelve participants performed saccade tasks in the scanner and their task-state functional MRI (fMRI) data were collected to verify the activation of structurally identified brain regions during the saccade generation. Voxel-based morphometry (VBM) results revealed that gray matter volume (GMV) of the left precentral gyrus and the left insula were positively correlated with the antisaccade cost, which was validated by the prediction analysis. Brain activation results showed the activation of the precentral during both pro and antisaccade execution period, but not the insula. Our results suggest that precentral gyrus and insula play vital roles to antisaccade cost, but possibly in different ways. The insula, a key node of the salience network, possibly regulates the saliency processing of the target, while the precentral gyrus possibly mediates the generation of saccades. Our study especially highlights an outstanding role of the precentral gyrus in flexible oculomotor control. |
Johannes Kirchner; Tamara Watson; Markus Lappe Real-time MRI reveals unique insight into the full eye kinematics of eye movements Journal Article In: eNeuro, vol. 9, no. 1, pp. 1–14, 2022. @article{Kirchner2022a, Our eyes are constantly in motion and the various kinds of eye movements are closely linked to many aspects of human cognitive processing. Measuring all possible eye movements unobtrusively is not achievable with current methods. Video-based eye-trackers only measure rotational but not translational motion of the eye, re- quire a calibration process relying on the participant's self-report of accurate fixation, and do not work if vision of the eyeball is blocked. Scleral search coils attach physical weight on the eyeball and also do not measure translation. Here, we describe a novel and fully automated method to use real-time magnetic resonance imaging (MRI) for eye tracking. We achieved a temporal resolution sufficient to measure eye rotations and transla- tions as short as those that occur within a blink and behind a closed eyelid. To demonstrate this method, we measured the full extent of the blink-related eye movement for two individuals, suggesting that the eye approaches a holding position during lid closure and can move by as much as 35° in rotation and 2 mm in translation. We also investigated the coordination of gaze shifts with blinks. We found that the gaze shift is tightly coupled in time to the translational blink movement and that blinks can induce significant temporal shifts of the gaze trajectory between left and right eye. Our MR-based Eye Tracking (MREyeTrack) method allows measurement of eye movements in terms of both translation and rotation and enables new opportunities for study- ing ocular motility and its disorders. |
Estelle Raffin; Adrien Witon; Roberto F. Salamanca-Giron; Krystel R. Huxlin; Friedhelm C. Hummel Functional segregation within the dorsal frontoparietal network: A multimodal dynamic causal modeling study Journal Article In: Cerebral Cortex, vol. 32, no. 15, pp. 3187–3205, 2022. @article{Raffin2022, Discrimination and integration of motion direction requires the interplay of multiple brain areas. Theoretical accounts of perception suggest that stimulus-related (i.e., exogenous) and decision-related (i.e., endogenous) factors affect distributed neuronal processing at different levels of the visual hierarchy. To test these predictions, we measured brain activity of healthy participants during a motion discrimination task, using electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). We independently modeled the impact of exogenous factors (task demand) and endogenous factors (perceptual decision-making) on the activity of the motion discrimination network and applied Dynamic Causal Modeling (DCM) to both modalities. DCM for event-related potentials (DCM-ERP) revealed that task demand impacted the reciprocal connections between the primary visual cortex (V1) and medial temporal areas (V5). With practice, higher visual areas were increasingly involved, as revealed by DCM-fMRI. Perceptual decision-making modulated higher levels (e.g., V5-to-Frontal Eye Fields, FEF), in a manner predictive of performance. Our data suggest that lower levels of the visual network support early, feature-based selection of responses, especially when learning strategies have not been implemented. In contrast, perceptual decision-making operates at higher levels of the visual hierarchy by integrating sensory information with the internal state of the subject. |
Johannes Rennig; Michael S. Beauchamp Intelligibility of audiovisual sentences drives multivoxel response patterns in human superior temporal cortex Journal Article In: NeuroImage, vol. 247, pp. 1–9, 2022. @article{Rennig2022, Regions of the human posterior superior temporal gyrus and sulcus (pSTG/S) respond to the visual mouth movements that constitute visual speech and the auditory vocalizations that constitute auditory speech, and neural responses in pSTG/S may underlie the perceptual benefit of visual speech for the comprehension of noisy auditory speech. We examined this possibility through the lens of multivoxel pattern responses in pSTG/S. BOLD fMRI data was collected from 22 participants presented with speech consisting of English sentences presented in five different formats: visual-only; auditory with and without added auditory noise; and audiovisual with and without auditory noise. Participants reported the intelligibility of each sentence with a button press and trials were sorted post-hoc into those that were more or less intelligible. Response patterns were measured in regions of the pSTG/S identified with an independent localizer. Noisy audiovisual sentences with very similar physical properties evoked very different response patterns depending on their intelligibility. When a noisy audiovisual sentence was reported as intelligible, the pattern was nearly identical to that elicited by clear audiovisual sentences. In contrast, an unintelligible noisy audiovisual sentence evoked a pattern like that of visual-only sentences. This effect was less pronounced for noisy auditory-only sentences, which evoked similar response patterns regardless of intelligibility. The successful integration of visual and auditory speech produces a characteristic neural signature in pSTG/S, highlighting the importance of this region in generating the perceptual benefit of visual speech. |
Noam Saadon-Grosman; Peter A. Angeli; Lauren M. DiNicola; Randy L. Buckner A third somatomotor representation in the human cerebellum Journal Article In: Journal of Neurophysiology, vol. 128, no. 5, pp. 1051–1073, 2022. @article{SaadonGrosman2022, Seminal neurophysiological studies in the 1940s discovered two somatomotor maps in the cerebellum-an inverted anterior lobe map and an upright posterior lobe map. Both maps have been confirmed in the human using noninvasive neuroimaging with additional hints of a third map within and near to the cerebellar vermis. Here, we sought direct evidence for the third somatomotor map by using intensive, repeated functional MRI (fMRI) scanning of individuals performing movements across multiple body parts (tongue, hands, glutes, and feet). An initial discovery sample (n = 4, 4 sessions per individual including 576 separate blocks of body movements) yielded evidence for the two established cerebellar somatomotor maps, as well as evidence for a third discontinuous foot representation within the vermis. When the left versus right foot movements were directly contrasted, the third representation could be clearly distinguished from the second representation in multiple individuals. Functional connectivity from seed regions in the third somatomotor representation confirmed anatomically specific connectivity with the cerebral cortex, paralleling the patterns observed for the two well-established maps. All results were prospectively replicated in an independent dataset with new individuals (n = 4). These collective findings provide direct support for a third somatomotor representation in the vermis of the cerebellum that may be part of a third map. We discuss the relations of this candidate third map to the broader topography of the cerebellum as well as its implications for understanding the specific organization of the human cerebellar vermis where distinct zones appear functionally specialized for somatomotor and visual domains. |
Patrick Sadil; Rosemary A. Cowell; David E. Huber A modeling framework for determining modulation of neural-level tuning from non-invasive human fMRI data Journal Article In: Communications Biology, vol. 5, no. 1, pp. 1–12, 2022. @article{Sadil2022, Many neuroscience theories assume that tuning modulation of individual neurons underlies changes in human cognition. However, non-invasive fMRI lacks sufficient resolution to visualize this modulation. To address this limitation, we developed an analysis framework called Inferring Neural Tuning Modulation (INTM) for “peering inside” voxels. Precise specification of neural tuning from the BOLD signal is not possible. Instead, INTM compares theoretical alternatives for the form of neural tuning modulation that might underlie changes in BOLD across experimental conditions. The most likely form is identified via formal model comparison, with assumed parametric Normal tuning functions, followed by a non-parametric check of conclusions. We validated the framework by successfully identifying a well-established form of modulation: visual contrast-induced multiplicative gain for orientation tuned neurons. INTM can be applied to any experimental paradigm testing several points along a continuous feature dimension (e.g., direction of motion, isoluminant hue) across two conditions (e.g., with/without attention, before/after learning). |
Arunava Samaddar; Brooke S. Jackson; Christopher J. Helms; Nicole A. Lazar; Jennifer E. McDowell; Cheolwoo Park A group comparison in fMRI data using a semiparametric model under shape invariance Journal Article In: Computational Statistics and Data Analysis, vol. 167, pp. 1–18, 2022. @article{Samaddar2022, In the analysis of functional magnetic resonance imaging (fMRI) data, a common type of analysis is to compare differences across scanning sessions. A challenge to direct comparisons of this type is the low signal-to-noise ratio in fMRI data. By using the property that brain signals from a task-related experiment may exhibit a similar pattern in regions of interest across participants, a semiparametric approach under shape invariance to quantify and test the differences in sessions and groups is developed. The common function is estimated with local polynomial regression and the shape invariance model parameters are estimated using evolutionary optimization methods. The efficacy of the semi-parametric approach is demonstrated on a study of brain activation changes across two sessions associated with practice-related cognitive control. The objective of the study is to evaluate neural circuitry supporting a cognitive control task, and associated practice-related changes via acquisition of blood oxygenation level dependent (BOLD) signal collected using fMRI. By using the proposed approach, BOLD signals in multiple regions of interest for control participants and participants with schizophrenia are compared as they perform a cognitive control task (known as the antisaccade task) at two sessions, and the effects of task practice in these groups are quantified. |
Takafumi Sasaoka; Tokiko Harada; Daichi Sato; Nanae Michida; Hironobu Yonezawa; Masatoshi Takayama; Takahide Nouzawa; Shigeto Yamawaki Neural basis for anxiety and anxiety-related physiological responses during a driving situation: An fMRI study Journal Article In: Cerebral Cortex, vol. 3, pp. 1–19, 2022. @article{Sasaoka2022, Although the exteroceptive and interoceptive prediction of a negative event increases a person's anxiety in daily life situations, the relationship between the brain mechanism of anxiety and the anxiety-related autonomic response has not been fully understood. In this functional magnetic resonance imaging (fMRI) study, we examined the neural basis of anxiety and anxiety-related autonomic responses in a daily driving situation. Participants viewed a driving video clip in the first-person perspective. During the video clip, participants were presented with a cue to indicate whether a subsequent crash could occur (attention condition) or not (safe condition). Enhanced activities in the anterior insula, bed nucleus of the stria terminalis, thalamus, and periaqueductal gray, and higher sympathetic nerve responses (pupil dilation and peripheral arterial stiffness) were triggered by the attention condition but not with the safe condition. Autonomic response-related functional connectivity was detected in the visual cortex, cerebellum, brainstem, and MCC/PCC with the right anterior insula and its adjacent regions as seed regions. Thus, the right anterior insula and adjacent regions, in collaboration with other regions play a role in eliciting anxiety based on the prediction of negative events, by mediating anxiety-related autonomic responses according to interoceptive information. |
Rebekka Schröder; Eliana Faiola; Maria Fernanda Urquijo; Katharina Bey; Inga Meyhöfer; Maria Steffens; Anna-Maria Kasparbauer; Anne Ruef; Hanna Högenauer; René Hurlemann; Joseph Kambeitz; Alexandra Philipsen; Michael Wagner; Nikolaos Koutsouleris; Ulrich Ettinger Neural correlates of smooth pursuit eye movements in schizotypy and recent onset psychosis: A multivariate pattern classification approach Journal Article In: Schizophrenia Bulletin Open, vol. 3, no. 1, pp. 1–13, 2022. @article{Schroeder2022, Schizotypy refers to a set of personality traits that bear resemblance, at subclinical level, to psychosis. Despite evidence of similarity at multiple levels of analysis, direct comparisons of schizotypy and clinical psychotic disorders are rare. Therefore, we used functional magnetic resonance imaging (fMRI) to examine the neural correlates and task-based functional connectivity (psychophysiological interactions; PPI) of smooth pursuit eye movements (SPEM) in patients with recent onset psychosis (ROP; n = 34), participants with high levels of negative (HNS; n = 46) or positive (HPS; n = 41) schizotypal traits, and low-schizotypy control participants (LS; n = 61) using machine-learning. Despite strong previous evidence that SPEM is a highly reliable marker of psychosis, patients and controls could not be significantly distinguished based on SPEM performance or blood oxygen level dependent (BOLD) signal during SPEM. Classification was, however, significant for the right frontal eye field (FEF) seed region in the PPI analyses but not for seed regions in other key areas of the SPEM network. Applying the right FEF classifier to the schizotypal samples yielded decision scores between the LS and ROP groups, suggesting similarities and dissimilarities of the HNS and HPS samples with the LS and ROP groups. The very small difference between groups is inconsistent with previous studies that showed significant differences between patients with ROP and controls in both SPEM performance and underlying neural mechanisms with large effect sizes. As the current study had sufficient power to detect such differences, other reasons are discussed. |
Raphael Vallat; Başak Türker; Alain Nicolas; Perrine Ruby High dream recall frequency is associated with increased creativity and default mode network connectivity Journal Article In: Nature and Science of Sleep, vol. 14, pp. 265–275, 2022. @article{Vallat2022, Introduction: Several results suggest that the frequency of dream recall is positively correlated with personality traits such as creativity and openness to experience. In addition, neuroimaging results have evidenced different neurophysiological profiles in high dream recallers (HR) and low dream recallers (LR) during both sleep and wakefulness, specifically within regions of the default mode network (DMN). These findings are consistent with the emerging view that dreaming and mind wandering pertain to the same family of spontaneous mental processes, subserved by the DMN. Methods: To further test this hypothesis, we measured the DMN functional connectivity during resting wakefulness, together with personality and cognitive abilities (including creativity) in 28 HR and 27 LR. Results: As expected, HR demonstrated a greater DMN connectivity than LR, higher scores of creativity, and no significant difference in memory abilities. However, there was no significant correlation between creativity scores and DMN connectivity. Discussion: These results further demonstrate that there are trait neurophysiological and psychological differences between individuals who frequently recall their dreams and those who do not. They support the forebrain and the DMN hypotheses of dreaming and leave open the possibility that increased activity in the DMN promotes creative-thinking during both wakefulness and sleep. Further work is needed to test whether activity in the DMN is causally associated with creative-thinking. |
Mirjam C. M. Wever; Lisanne A. E. M. Houtum; Loes H. C. Janssen; Wilma G. M. Wentholt; Iris M. Spruit; Marieke S. Tollenaar; Geert Jan Will; Bernet M. Elzinga Neural and affective responses to prolonged eye contact with one's own adolescent child and unfamiliar others Journal Article In: NeuroImage, vol. 260, pp. 1–12, 2022. @article{Wever2022, Eye contact is crucial for the formation and maintenance of social relationships, and plays a key role in facilitating a strong parent-child bond. However, the precise neural and affective mechanisms through which eye contact impacts on parent-child relationships remain elusive. We introduce a task to assess parents' neural and affective responses to prolonged direct and averted gaze coming from their own child, and an unfamiliar child and adult. While in the scanner, 79 parents (n = 44 mothers and n = 35 fathers) were presented with prolonged (16-38 s) videos of their own child, an unfamiliar child, an unfamiliar adult, and themselves (i.e., targets), facing the camera with a direct or an averted gaze. We measured BOLD-responses, tracked parents' eye movements during the videos, and asked them to report on their mood and feelings of connectedness with the targets after each video. Parents reported improved mood and increased feelings of connectedness after prolonged exposure to direct versus averted gaze and these effects were amplified for unfamiliar targets compared to their own child, due to high affect and connectedness ratings after videos of their own child. Neuroimaging results showed that the sight of one's own child was associated with increased activity in middle occipital gyrus, fusiform gyrus and inferior frontal gyrus relative to seeing an unfamiliar child or adult. While we found no robust evidence of specific neural correlates of eye contact (i.e., contrast direct > averted gaze), an exploratory parametric analysis showed that dorsomedial prefrontal cortex (dmPFC) activity increased linearly with duration of eye contact (collapsed across all “other” targets). Eye contact-related dmPFC activity correlated positively with increases in feelings of connectedness, suggesting that this region may drive feelings of connectedness during prolonged eye contact with others. These results underline the importance of prolonged eye contact for affiliative processes and provide first insights into its neural correlates. This may pave the way for new research in individuals or pairs in whom affiliative processes are disrupted. |
Antonius Wiehler; Francesca Branzoli; Isaac Adanyeguh; Fanny Mochel; Mathias Pessiglione A neuro-metabolic account of why daylong cognitive work alters the control of economic decisions Journal Article In: Current Biology, vol. 32, no. 16, pp. 3564–3575, 2022. @article{Wiehler2022, Behavioral activities that require control over automatic routines typically feel effortful and result in cognitive fatigue. Beyond subjective report, cognitive fatigue has been conceived as an inflated cost of cognitive control, objectified by more impulsive decisions. However, the origins of such control cost inflation with cognitive work are heavily debated. Here, we suggest a neuro-metabolic account: the cost would relate to the necessity of recycling potentially toxic substances accumulated during cognitive control exertion. We validated this account using magnetic resonance spectroscopy (MRS) to monitor brain metabolites throughout an approximate workday, during which two groups of participants performed either high-demand or low-demand cognitive control tasks, interleaved with economic decisions. Choice-related fatigue markers were only present in the high-demand group, with a reduction of pupil dilation during decision-making and a preference shift toward short-delay and little-effort options (a low-cost bias captured using computational modeling). At the end of the day, high-demand cognitive work resulted in higher glutamate concentration and glutamate/glutamine diffusion in a cognitive control brain region (lateral prefrontal cortex [lPFC]), relative to low-demand cognitive work and to a reference brain region (primary visual cortex [V1]). Taken together with previous fMRI data, these results support a neuro-metabolic model in which glutamate accumulation triggers a regulation mechanism that makes lPFC activation more costly, explaining why cognitive control is harder to mobilize after a strenuous workday. |
Marilena Wilding; Christof Körner; Anja Ischebeck; Natalia Zaretskaya Increased insula activity precedes the formation of subjective illusory Gestalt Journal Article In: NeuroImage, vol. 257, pp. 1–10, 2022. @article{Wilding2022, The constructive nature of human perception sometimes leads us to perceiving rather complex impressions from simple sensory input: for example, recognizing animal contours in cloud formations or seeing living creatures in shadows of objects. A special type of bistable stimuli gives us a rare opportunity to study the neural mechanisms behind this process. Such stimuli can be visually interpreted either as simple or as more complex illusory content on the basis of the same sensory input. Previous studies demonstrated increased activity in the superior parietal cortex during the perception of an illusory Gestalt impression compared to a simpler interpretation. Here, we examined the role of slow fluctuations of resting-state fMRI activity in shaping the subsequent illusory interpretation by investigating activity related to the illusory Gestalt not only during, but also prior to its perception. We presented 31 participants with a bistable motion stimulus, which can be perceived either as four moving dot pairs (local) or two moving illusory squares (global). fMRI was used to measure brain activity in a slow event-related design. We observed stronger IPS and putamen responses to the stimulus when participants perceived the global interpretation compared to the local, confirming the findings of previous studies. Most importantly, we also observed that the global stimulus interpretation was preceded by an increased activity of the bilateral dorsal insula, which is known to process saliency and gate information for conscious access. Our data suggest an important role of the dorsal insula in shaping complex illusory interpretations of the sensory input. |
2021 |
Abhijit Rajan; Sreenivasan Meyyappan; Yuelu Liu; Immanuel Babu Henry Samuel; Bijurika Nandi; George R. Mangun; Mingzhou Ding The microstructure of attentional control in the dorsal attention network Journal Article In: Journal of Cognitive Neuroscience, vol. 33, no. 6, pp. 965–983, 2021. @article{Rajan2021, The top–down control of attention involves command signals arising chiefly in the dorsal attention network (DAN) in frontal and parietal cortex and propagating to sensory cortex to enable the selective processing of incoming stimuli based on their behavioral relevance. Consistent with this view, the DAN is active during preparatory (anticipatory) attention for relevant events and objects, which, in vision, may be defined by different stimulus attributes including their spatial location, color, motion, or form. How this network is organized to support different forms of preparatory attention to different stimulus attributes remains unclear. We propose that, within the DAN, there exist functional microstructures (patterns of activity) specific for controlling attention based on the specific information to be attended. To test this, we contrasted preparatory attention to stimulus location (spatial attention) and to stimulus color (feature attention), and used multivoxel pattern analysis to characterize the corresponding patterns of activity within the DAN. We observed different multivoxel patterns of BOLD activation within the DAN for the control of spatial attention (attending left vs. right) and feature attention (attending red vs. green). These patterns of activity for spatial and feature attentional control showed limited overlap with each other within the DAN. Our findings thus support a model in which the DAN has different functional microstructures for distinctive forms of top–down control of visual attention. |
Ryan V. Raut; Abraham Z. Snyder; Anish Mitra; Dov Yellin; Naotaka Fujii; Rafael Malach; Marcus E. Raichle Global waves synchronize the brain's functional systems with fluctuating arousal Journal Article In: Science Advances, vol. 7, no. 30, pp. eabf2709, 2021. @article{Raut2021, We propose and empirically support a parsimonious account of intrinsic, brain-wide spatiotemporal organization arising from traveling waves linked to arousal. We hypothesize that these waves are the predominant physiological process reflected in spontaneous functional magnetic resonance imaging (fMRI) signal fluctuations. The correlation structure ("functional connectivity") of these fluctuations recapitulates the large-scale functional organization of the brain. However, a unifying physiological account of this structure has so far been lacking. Here, using fMRI in humans, we show that ongoing arousal fluctuations are associated with global waves of activity that slowly propagate in parallel throughout the neocortex, thalamus, striatum, and cerebellum. We show that these waves can parsimoniously account for many features of spontaneous fMRI signal fluctuations, including topographically organized functional connectivity. Last, we demonstrate similar, cortex-wide propagation of neural activity measured with electrocorticography in macaques. These findings suggest that traveling waves spatiotemporally pattern brain-wide excitability in relation to arousal. |
Mor Regev; Andrea R. Halpern; Adrian M. Owen; Aniruddh D. Patel; Robert J. Zatorre Mapping specific mental content during musical imagery Journal Article In: Cerebral Cortex, vol. 31, no. 8, pp. 3622–3640, 2021. @article{Regev2021, Humans can mentally represent auditory information without an external stimulus, but the specificity of these internal representations remains unclear. Here, we asked how similar the temporally unfolding neural representations of imagined music are compared to those during the original perceived experience. We also tested whether rhythmic motion can influence the neural representation of music during imagery as during perception. Participants first memorized six 1-min-long instrumental musical pieces with high accuracy. Functional MRI data were collected during: 1) silent imagery of melodies to the beat of a visual metronome; 2) same but while tapping to the beat; and 3) passive listening. During imagery, inter-subject correlation analysis showed that melody-specific temporal response patterns were reinstated in right associative auditory cortices. When tapping accompanied imagery, the melody-specific neural patterns were reinstated in more extensive temporal-lobe regions bilaterally. These results indicate that the specific contents of conscious experience are encoded similarly during imagery and perception in the dynamic activity of auditory cortices. Furthermore, rhythmic motion can enhance the reinstatement of neural patterns associated with the experience of complex sounds, in keeping with models of motor to sensory influences in auditory processing. |
Sarah Schuster; Nicole Alexandra; Florian Hutzler; Fabio Richlan; Martin Kronbichler; Stefan Hawelka Cloze enough? Hemodynamic effects of predictive processing during natural reading Journal Article In: NeuroImage, vol. 228, pp. 117687, 2021. @article{Schuster2021, Evidence accrues that readers form multiple hypotheses about upcoming words. The present study investigated the hemodynamic effects of predictive processing during natural reading by means of combining fMRI and eye movement recordings. In particular, we investigated the neural and behavioral correlates of precision-weighted prediction errors, which are thought to be indicative of subsequent belief updating. Participants silently read sentences in which we manipulated the cloze probability and the semantic congruency of the final word that served as an index for precision and prediction error respectively. With respect to the neural correlates, our findings indicate an enhanced activation within the left inferior frontal and middle temporal gyrus suggesting an effect of precision on prediction update in higher (lexico-)semantic levels. Despite being evident at the neural level, we did not observe any evidence that this mechanism resulted in disproportionate reading times on participants' eye movements. The results speak against discrete predictions, but favor the notion that multiple words are activated in parallel during reading. 1. |
Alyssa H. Sinclair; Grace M. Manalili; Iva K. Brunec; R. Alison Adcock; Morgan D. Barense Prediction errors disrupt hippocampal representations and update episodic memories Journal Article In: Proceedings of the National Academy of Sciences, vol. 118, no. 51, pp. 1–12, 2021. @article{Sinclair2021, The brain supports adaptive behavior by generating predictions, learning from errors, and updating memories to incorporate new information. Prediction error, or surprise, triggers learning when reality contradicts expectations. Prior studies have shown that the hippocampus signals prediction errors, but the hypothesized link to memory updating has not been demonstrated. In a human functional MRI study, we elicited mnemonic prediction errors by interrupting familiar narrative videos immediately before the expected endings. We found that prediction errors reversed the relationship between univariate hippocampal activation and memory: greater hippocampal activation predicted memory preservation after expected endings, but memory updating after surprising endings. In contrast to previous studies, we show that univariate activation was insufficient for understanding hippocampal prediction error signals. We explain this surprising finding by tracking both the evolution of hippocampal activation patterns and the connectivity between the hippocampus and neuromodulatory regions. We found that hippocampal activation patterns stabilized as each narrative episode unfolded, suggesting sustained episodic representations. Prediction errors disrupted these sustained representations and the degree of disruption predicted memory updating. The relationship between hippocampal activation and subsequent memory depended on concurrent basal forebrain activation, supporting the idea that cholinergic modulation regulates attention and memory. We conclude that prediction errors create conditions that favor memory updating, prompting the hippocampus to abandon ongoing predictions and make memories malleable. |
Nathan Tardiff; John D. Medaglia; Danielle S. Bassett; Sharon L. Thompson-Schill The modulation of brain network integration and arousal during exploration Journal Article In: NeuroImage, vol. 240, pp. 118369, 2021. @article{Tardiff2021, There is growing interest in how neuromodulators shape brain networks. Recent neuroimaging studies provide evidence that brainstem arousal systems, such as the locus coeruleus-norepinephrine system (LC-NE), influence functional connectivity and brain network topology, suggesting they have a role in flexibly reconfiguring brain networks in order to adapt behavior and cognition to environmental demands. To date, however, the relationship between brainstem arousal systems and functional connectivity has not been assessed within the context of a task with an established relationship between arousal and behavior, with most prior studies relying on incidental variations in arousal or pharmacological manipulation and static brain networks constructed over long periods of time. These factors have likely contributed to a heterogeneity of effects across studies. To address these issues, we took advantage of the association between LC-NE-linked arousal and exploration to probe the relationships between exploratory choice, arousal—as measured indirectly via pupil diameter—and brain network dynamics. Exploration in a bandit task was associated with a shift toward fewer, more weakly connected modules that were more segregated in terms of connectivity and topology but more integrated with respect to the diversity of cognitive systems represented in each module. Functional connectivity strength decreased, and changes in connectivity were correlated with changes in pupil diameter, in line with the hypothesis that brainstem arousal systems influence the dynamic reorganization of brain networks. More broadly, we argue that carefully aligning dynamic network analyses with task designs can increase the temporal resolution at which behaviorally- and cognitively-relevant modulations can be identified, and offer these results as a proof of concept of this approach. |
Hamid B. Turker; Elizabeth Riley; Wen Ming Luh; Stan J. Colcombe; Khena M. Swallow In: NeuroImage, vol. 236, pp. 1–17, 2021. @article{Turker2021, The locus coeruleus (LC) plays a central role in regulating human cognition, arousal, and autonomic states. Efforts to characterize the LC's function in humans using functional magnetic resonance imaging have been hampered by its small size and location near a large source of noise, the fourth ventricle. We tested whether the ability to characterize LC function is improved by employing neuromelanin-T1 weighted images (nmT1) for LC localization and multi-echo functional magnetic resonance imaging (ME-fMRI) for estimating intrinsic functional connectivity (iFC). Analyses indicated that, relative to a probabilistic atlas, utilizing nmT1 images to individually localize the LC increases the specificity of seed time series and clusters in the iFC maps. When combined with independent components analysis (ME-ICA), ME-fMRI data provided significant improvements in the temporal signal to noise ratio and DVARS relative to denoised single echo data (1E-fMRI). The effects of acquiring nmT1 images and ME-fMRI data did not appear to only reflect increases in power: iFC maps for each approach overlapped only moderately. This is consistent with findings that ME-fMRI offers substantial advantages over 1E-fMRI acquisition and denoising. It also suggests that individually identifying LC with nmT1 scans is likely to reduce the influence of other nearby brainstem regions on estimates of LC function. |
Renée M. Visser; Joe Bathelt; H. Steven Scholte; Merel Kindt Robust BOLD responses to faces but not to conditioned threat: Challenging the amygdala's reputation in human fear and extinction learning Journal Article In: Journal of Neuroscience, vol. 41, no. 50, pp. 10278–10292, 2021. @article{Visser2021, Most of our knowledge about human emotional memory comes from animal research. Based on this work, the amygdala is often labelled the brain's "fear center", but it is unclear to what degree neural circuitries underlying fear and extinction learning are conserved across species. Neuroimaging studies in humans yield conflicting findings, with many studies failing to show amygdala activation in response to learned threat. Such null-findings are often treated as resulting from MRI-specific problems related to measuring deep brain structures. Here we test this assumption in a mega-analysis of three studies on fear acquisition (n=98; 68 female) and extinction learning (n=79; 53 female). The conditioning procedure involved presentation of two pictures of faces and two pictures of houses: one of each pair was followed by an electric shock (CS+), the other one was never followed by a shock (CS-), and participants were instructed to learn these contingencies. Results revealed widespread responses to the CS+ compared to CS- in the fear network, including anterior insula, midcingulate cortex, thalamus and bed nucleus of the stria terminalis, but not the amygdala, which actually responded stronger to the CS-. Results were independent of spatial smoothing, and individual differences in trait anxiety and conditioned pupil responses. In contrast, robust amygdala activation distinguished faces from houses, refuting the idea that poor signal could account for the absence of effects. Moving forward, we suggest that apart from imaging larger samples at higher resolution, alternative statistical approaches may be employed to identify cross-species similarities in fear and extinction learning. |
Tianlu Wang; Lena M. Hofbauer; Dante Mantini; Céline R. Gillebert Behavioural and neural effects of eccentricity and visual field during covert visuospatial attention Journal Article In: Neuroimage: Reports, vol. 1, no. 3, pp. 1–11, 2021. @article{Wang2021g, The attentional priority map plays a key role in the distribution of attention, and is modulated by bottom-up sensory as well as top-down task-dependent factors. The intraparietal sulcus (IPS) is a key candidate to hold a neural representation of the attentional priority map. In the current study, we examined the role of the IPS during covert attention to spatial locations with high or low eccentricity in one or both visual hemifields. To this end, eighteen neurologically healthy participants performed a cued letter discrimination task in which they were endogenously cued to attend to a location at a 5 or 10◦ eccentricity in the left and/or right visual field. We briefly presented a four-letter target array and subsequently probed perceptual performance while acquiring event- related functional MRI data. While behavioural results showed greater letter discrimination performance at the low eccentricity compared to the high eccentricity location, no neural effect of eccentricity was observed. The results further showed that attending to one visual hemifield produced higher activation in the left parietal and occipital cortex compared to attending bilaterally. Future studies may consider increasing the involvement of top-down control of attention to the cued location to study the neural effect of eccentricity, e.g., through manipulating the task difficulty. |
Irma T. Kurniawan; Marcus Grueschow; Christian C. Ruff Anticipatory energization revealed by pupil and brain activity guides human effort-based decision making Journal Article In: Journal of Neuroscience, vol. 41, no. 29, pp. 6328–6342, 2021. @article{Kurniawan2021, An organism's fitness is determined by how it chooses to adapt to effort in response to challenges. Exertion of effort correlates with activity in dorsomedial prefrontal cortex (dmPFC) and noradrenergic pupil dilation, but little is known about the role of these neurophysiological processes for decisions about future efforts, they may provide anticipatory energization to help us accept the challenge or a cost representation that is weighted against the expected rewards. Here, we provide evidence for the former, by measuring pupil and functional magnetic resonance imaging (fMRI) brain responses while 52 human participants (29 females) chose whether to exert efforts to obtain rewards. Both pupil-dilation rate and dmPFC fMRI activity increased with anticipated effort level, and these increases differ depending on the choice outcome: they were stronger when participants chose to accept the challenge compared with when the challenge was declined. Crucially, the choice-dependent modulation of pupil and brain-activity effort representations were stronger in participants whose behavioral choices were more sensitive to effort. Our results identify a process involving the peripheral and central human nervous system that simulates the required energization before overt response, suggesting a role in guiding effort-based decisions. |
Hsin-Hung Li; Thomas C. Sprague; Aspen H. Yoo; Wei Ji Ma; Clayton E. Curtis Joint representation of working memory and uncertainty in human cortex Journal Article In: Neuron, vol. 109, no. 22, pp. 3699–3712, 2021. @article{Li2021c, Neural representations of visual working memory (VWM) are noisy, and thus, decisions based on VWM are inevitably subject to uncertainty. However, the mechanisms by which the brain simultaneously represents the content and uncertainty of memory remain largely unknown. Here, inspired by the theory of probabilistic population codes, we test the hypothesis that the human brain represents an item maintained in VWM as a probability distribution over stimulus feature space, thereby capturing both its content and uncertainty. We used a neural generative model to decode probability distributions over memorized locations from fMRI activation patterns. We found that the mean of the probability distribution decoded from retinotopic cortical areas predicted memory reports on a trial-by-trial basis. Moreover, in several of the same mid-dorsal stream areas, the spread of the distribution predicted subjective trial-by-trial uncertainty judgments. These results provide evidence that VWM content and uncertainty are jointly represented by probabilistic neural codes. |
Björn Machner; Jonathan Imholz; Lara Braun; Philipp J. Koch; Tobias Bäumer; Thomas F. Münte; Christoph Helmchen; Andreas Sprenger In: Neuroimage: Reports, vol. 1, no. 2, pp. 100013, 2021. @article{Machner2021, Disruption of resting-state functional connectivity (RSFC) between core regions of the dorsal attention network (DAN), including the bilateral superior parietal lobule (SPL), and structural damage of the right-lateralized ventral attention network (VAN), including the temporo-parietal junction (TPJ), have been described as neural basis for hemispatial neglect. Pursuing a virtual lesion model, we aimed to perturbate the attention networks of 22 healthy subjects by applying continuous theta burst stimulation (cTBS) to the right SPL or TPJ. We first created network masks of the DAN and VAN based on RSFC analyses from a RS-fMRI baseline session and determined the SPL and TPJ stimulation site within the respective mask. We then performed RS-fMRI immediately after cTBS of the SPL, TPJ (active sites) or vertex (control site). RSFC between SPL/TPJ and whole brain as well as between predefined regions of interest (ROI) in the attention networks was analyzed in a within-subject design. Contrary to our hypothesis, seed-based RSFC did not differ between the four experimental conditions. The individual change in ROI-to-ROI RSFC from baseline to post-stimulation did also not differ between active (SPL, TPJ) and control (vertex) cTBS. In our study, a single session offline cTBS over the right SPL or TPJ could not alter RSFC in the attention networks as compared to a control stimulation, maybe because effects wore off too early. Future studies should consider a modified cTBS protocol, concurrent TMS-fMRI or transcranial direct current stimulation. |
Jennifer E. Mack; Colleen Ward; Sofia Stratford Impact of the fMRI environment on eye-tracking measures in a linguistic prediction task Journal Article In: Language, Cognition and Neuroscience, vol. 36, no. 6, pp. 675–693, 2021. @article{Mack2021, The present study investigated the impact of the MRI environment on eye-movement measures in the visual-world paradigm. 24 neurotypical young adults performed a linguistic prediction task in a typical lab setting (Lab) and 22 did so during MRI scanning (Scanner). Data analyses focused on eye-tracking data quality and the time course and magnitude of prediction effects. Data quality was reduced in the Scanner as compared to the Lab, as indicated by a higher rate of track loss and saccades/fixations of atypical duration. Predictive eye movement patterns were generally similar in timing and magnitude between the Lab and Scanner, although there was modest evidence for increased prediction effects in the Scanner. In the Scanner environment only, predictive eye movements were linked to better task performance. Evidently, the MRI environment can enhance prediction effects and their relationship to task performance, possibly due to increased deployment of cognitive control mechanisms. |
Verónica Mäki-Marttunen Pupil-based states of brain integration across cognitive states Journal Article In: Neuroscience, vol. 471, pp. 61–71, 2021. @article{MaekiMarttunen2021, Arousal is a potent mechanism that provides the brain with functional flexibility and adaptability to external conditions. Within the wake state, arousal levels driven by activity in the neuromodulatory systems are related to specific signatures of neural activation and brain synchrony. However, direct evidence is still lacking on the varying effects of arousal on macroscopic brain characteristics and across a variety of cognitive states in humans. Using a concurrent fMRI-pupillometry approach, we used pupil size as a proxy for arousal and obtained patterns of brain integration associated with increasing arousal levels. We carried out this analysis on resting-state data and data from two attentional tasks implicating different cognitive processes. We found that an increasing level of arousal was related to a state of increased brain integration. This effect was prominent in the salience, visual and default-mode networks in all conditions, while other regions showed task-specificity. Increased integration in the salience network was also related to faster pupil dilation in the two attentional tasks. Furthermore, task performance was related to arousal level, with lower accuracy at higher level of arousal. Taken together, our study provides evidence in humans for pupil size as an index of brain network state, and supports the role of arousal as a switch that drives brain coordination in specific brain regions according to the cognitive state. |
Cornelia McCormick; Marshall A. Dalton; Peter Zeidman; Eleanor A. Maguire Characterising the hippocampal response to perception, construction and complexity Journal Article In: Cortex, vol. 137, pp. 1–17, 2021. @article{McCormick2021, The precise role played by the hippocampus in supporting cognitive functions such as episodic memory and future thinking is debated, but there is general agreement that it involves constructing representations comprised of numerous elements. Visual scenes have been deployed extensively in cognitive neuroscience because they are paradigmatic multi-element stimuli. However, questions remain about the specificity and nature of the hippocampal response to scenes. Here, we devised a paradigm in which we had participants search pairs of images for either colour or layout differences, thought to be associated with perceptual or spatial constructive processes respectively. Importantly, images depicted either naturalistic scenes or phase-scrambled versions of the same scenes, and were either simple or complex. Using this paradigm during functional MRI scanning, we addressed three questions: 1. Is the hippocampus recruited specifically during scene processing? 2. If the hippocampus is more active in response to scenes, does searching for colour or layout differences influence its activation? 3. Does the complexity of the scenes affect its response? We found that, compared to phase-scrambled versions of the scenes, the hippocampus was more responsive to scene stimuli. Moreover, a clear anatomical distinction was evident, with colour detection in scenes engaging the posterior hippocampus whereas layout detection in scenes recruited the anterior hippocampus. The complexity of the scenes did not influence hippocampal activity. These findings seem to align with perspectives that propose the hippocampus is especially attuned to scenes, and its involvement occurs irrespective of the cognitive process or the complexity of the scenes. |
Cornelia McCormick; Eleanor A. Maguire The distinct and overlapping brain networks supporting semantic and spatial constructive scene processing Journal Article In: Neuropsychologia, vol. 158, pp. 107912, 2021. @article{McCormick2021a, Scene imagery features prominently when we recall autobiographical memories, imagine the future and navigate around in the world. Consequently, in this study we sought to better understand how scene representations are supported by the brain. Processing scenes involves a variety of cognitive processes that in the real world are highly interactive. Here, however, our goal was to separate semantic and spatial constructive scene processes in order to identify the brain areas that were distinct to each process, those they had in common, and the connectivity between regions. To this end, participants searched for either semantic or spatial constructive impossibilities in scenes during functional MRI. We focussed our analyses on only those scenes that were possible, thus removing any error detection that would evoke reactions such as surprise or novelty. Importantly, we also counterbalanced possible scenes across participants, enabling us to examine brain activity and connectivity for the same possible scene images under two different conditions. We found that participants adopted different cognitive strategies, which were reflected in distinct oculomotor behaviour, for each condition. These were in turn associated with increased engagement of lateral temporal and parietal cortices for semantic scene processing, the hippocampus for spatial constructive scene processing, and increased activation of the ventromedial prefrontal cortex (vmPFC) that was common to both. Connectivity analyses showed that the vmPFC switched between semantic and spatial constructive brain networks depending on the task at hand. These findings further highlight the well-known semantic functions of lateral temporal areas, while providing additional support for the previously-asserted contribution of the hippocampus to scene construction, and recent suggestions that the vmPFC may play a key role in orchestrating scene processing. |
Sreenivasan Meyyappan; Abhijit Rajan; George R. Mangun; Mingzhou Ding Role of inferior frontal junction (IFJ) in the control of feature versus spatial attention Journal Article In: Journal of Neuroscience, vol. 41, no. 38, pp. 8065–8074, 2021. @article{Meyyappan2021, Feature-based visual attention refers to preferential selection and processing of visual stimuli based on their nonspatial attributes, such as color or shape. Recent studies have highlighted the inferior frontal junction (IFJ) as a control region for feature but not spatial attention. However, the extent to which IFJ contributes to spatial versus feature attention control remains a topic of debate. We investigated in humans of both sexes the role of IFJ in the control of feature versus spatial attention in a cued visual spatial (attend-left or attend-right) and feature (attend-red or attend-green) attention task using fMRI. Analyzing cue-related fMRI using both univariate activation and multivoxel pattern analysis, we found the following results in IFJ. First, in line with some prior studies, the univariate activations were not different between feature and spatial attentional control. Second, in contrast, the multivoxel pattern analysis decoding accuracy was above chance level for feature attention (attend-red vs attend-green) but not for spatial attention (attend-left vs attend-right). Third, while the decoding accuracy for feature attention was above chance level during attentional control in the cue-to-target interval, it was not during target processing. Fourth, the right IFJ and visual cortex (V4) were observed to be functionally connected during feature but not during spatial attention control, and this functional connectivity was positively associated with subsequent attentional selection of targets in V4, as well as with behavioral performance. These results support a model in which IFJ plays a crucial role in topdown control of visual feature but not visual spatial attention. |
Kentaro Miyamoto; Nadescha Trudel; Kevin Kamermans; Michele C. Lim; Alberto Lazari; Lennart Verhagen; Marco K. Wittmann; Matthew F. S. Rushworth Identification and disruption of a neural mechanism for accumulating prospective metacognitive information prior to decision-making Journal Article In: Neuron, vol. 109, no. 8, pp. 1396–1408, 2021. @article{Miyamoto2021, More than one type of probability must be considered when making decisions. It is as necessary to know one's chance of performing choices correctly as it is to know the chances that desired outcomes will follow choices. We refer to these two choice contingencies as internal and external probability. Neural activity across many frontal and parietal areas reflected internal and external probabilities in a similar manner during decision-making. However, neural recording and manipulation approaches suggest that one area, the anterior lateral prefrontal cortex (alPFC), is highly specialized for making prospective, metacognitive judgments on the basis of internal probability; it is essential for knowing which decisions to tackle, given its assessment of how well they will be performed. Its activity predicted prospective metacognitive judgments, and individual variation in activity predicted individual variation in metacognitive judgments. Its disruption altered metacognitive judgments, leading participants to tackle perceptual decisions they were likely to fail. |
Viola Mocz; Maryam Vaziri-Pashkam; Marvin Chun; Yaoda Xu Predicting identity-preserving object transformations across the human ventral visual stream Journal Article In: Journal of Neuroscience, vol. 41, no. 35, pp. 7403–7419, 2021. @article{Mocz2021, In everyday life, we have no trouble categorizing objects varying in position, size, and orientation. Previous fMRI research shows that higher-level object processing regions in the human lateral occipital cortex may link object responses from different affine states (i.e. size and viewpoint) through a general linear mapping function capable of predicting responses to novel objects. In this study, we extended this approach to examine the mapping for both Euclidean (e.g. position and size) and non-Euclidean (e.g. image statistics and spatial frequency) transformations across the human ventral visual processing hierarchy, including areas V1, V2, V3, V4, ventral occipitotemporal cortex (VOT), and lateral occipitotemporal cortex (LOT). The predicted pattern generated from a linear mapping function could capture a significant amount of the changes associated with the transformations throughout the ventral visual stream. The derived linear mapping functions were not category independent, as performance was better for the categories included than those not included in training and better between two similar versus two dissimilar categories in both lower and higher visual regions. Consistent with object representations being stronger in higher than lower visual regions, pattern selectivity and object category representational structure were somewhat better preserved in the predicted patterns in higher than lower visual regions. There were no notable differences between Euclidean and non-Euclidean transformations. These findings demonstrate a near-orthogonal representation of object identity and these non-identity features throughout the human ventral visual processing pathway, with these non-identity features largely untangled from the identity features early in visual processing. |
Sophia Nestmann; Daniel Wiesen; Hans-Otto Karnath; Johannes Rennig Temporo-parietal brain regions are involved in higher order object perception Journal Article In: NeuroImage, vol. 234, pp. 117982, 2021. @article{Nestmann2021, Lesions to posterior temporo-parietal brain regions are associated with deficits in perception of global, hierarchical shapes, but also with impairments in the processing of objects presented under demanding viewing conditions. Evidence from neuroimaging studies and lesion patterns observed in patients with simultanagnosia and agnosia for object orientation suggest similar brain regions to be involved in perception of global shapes and processing of objects in atypical (‘non-canonical') orientation. In a localizer experiment, we identified individual temporo-parietal brain areas involved in global shape perception and found significantly higher BOLD signals during the processing of non-canonical compared to canonical objects. In a multivariate approach, we demonstrated that posterior temporo-parietal brain areas show distinct voxel patterns for non-canonical and canonical objects and that voxel patterns of global shapes are more similar to those of objects in non-canonical compared to canonical viewing conditions. These results suggest that temporo-parietal brain areas are not only involved in global shape perception but might serve a more general mechanism of complex object perception. Our results challenge a strict attribution of object processing to the ventral visual stream by suggesting specific dorsal contributions in more demanding viewing conditions. |
Bao N. Nguyen; Scott C. Kolbe; Ashika Verghese; Christine Nearchou; Allison M. McKendrick; Gary F. Egan; Trichur R. Vidyasagar Visual search efficiency and functional visual cortical size in children with and without dyslexia Journal Article In: Neuropsychologia, vol. 155, pp. 107819, 2021. @article{Nguyen2021, Dyslexia is characterised by poor reading ability. Its aetiology is probably multifactorial, with abnormal visual processing playing an important role. Among adults with normal reading ability, there is a larger representation of central visual field in the primary visual cortex (V1) in those with more efficient visuospatial attention. In this study, we tested the hypothesis that poor reading ability in school-aged children (17 children with dyslexia, 14 control children with normal reading ability) is associated with deficits in visuospatial attention using a visual search task. We corroborated the psychophysical findings with neuroimaging, by measuring the functional size of V1 in response to a central 12° visual stimulus. Consistent with other literature, visual search was impaired and less efficient in the dyslexic children, particularly with more distractor elements in the search array (p = 0.04). We also found atypical interhemispheric asymmetry in functional V1 size in the dyslexia group (p = 0.02). Reading impaired children showed poorer visual search efficiency (p = 0.01), needing more time per unit distractor (higher ms/item). Reading ability was also correlated with V1 size asymmetry (p = 0.03), such that poorer readers showed less left hemisphere bias relative to the right hemisphere. Our findings support the view that dyslexic children have abnormal visuospatial attention and interhemispheric V1 asymmetry, relative to chronological age-matched peers, and that these factors may contribute to inter-individual variation in reading performance in children. |
Katya Olmos-Solis; Anouk Mariette Loon; Christian N. L. Olivers Content or status: Frontal and posterior cortical representations of object category and upcoming task goals in working memory Journal Article In: Cortex, vol. 135, pp. 61–77, 2021. @article{OlmosSolis2021, To optimize task sequences, the brain must differentiate between current and prospective goals. We previously showed that currently and prospectively relevant object representations in working memory can be dissociated within object-selective cortex. Based on other recent studies indicating that a range of brain areas may be involved in distinguishing between currently relevant and prospectively relevant information in working memory, here we conducted multivoxel pattern analyses of fMRI activity in additional posterior areas (specifically early visual cortex and the intraparietal sulcus) as well as frontal areas (specifically the frontal eye fields and lateral prefrontal cortex). We assessed whether these areas represent the memory content, the current versus prospective status of the memory, or both. On each trial, participants memorized an object drawn from three different categories. The object was the target for either a first task (currently relevant), a second task (prospectively relevant), or for neither task (irrelevant). The results revealed a division of labor across brain regions: While posterior areas preferentially coded for content (i.e., the category), frontal areas carried information about the current versus prospective relevance status of the memory, irrespective of the category. Intraparietal sulcus revealed both strong category- and status-sensitivity, consistent with its hub function of combining stimulus and priority signals. Furthermore, cross-decoding analyses revealed that while current and prospective representations were similar prior to search, they became dissimilar during search, in posterior as well as frontal areas. The findings provide further evidence for a dissociation between content and control networks in working memory. |
Heath R. Pardoe; Samantha P. Martin; Yijun Zhao; Allan George; Hui Yuan; Jingjie Zhou; Wei Liu; Orrin Devinsky Estimation of in-scanner head pose changes during structural MRI using a convolutional neural network trained on eye tracker video Journal Article In: Magnetic Resonance Imaging, vol. 81, pp. 101–108, 2021. @article{Pardoe2021, Introduction: In-scanner head motion is a common cause of reduced image quality in neuroimaging, and causes systematic brain-wide changes in cortical thickness and volumetric estimates derived from structural MRI scans. There are few widely available methods for measuring head motion during structural MRI. Here, we train a deep learning predictive model to estimate changes in head pose using video obtained from an in-scanner eye tracker during an EPI-BOLD acquisition with participants undertaking deliberate in-scanner head movements. The predictive model was used to estimate head pose changes during structural MRI scans, and correlated with cortical thickness and subcortical volume estimates. Methods: 21 healthy controls (age 32 ± 13 years, 11 female) were studied. Participants carried out a series of stereotyped prompted in-scanner head motions during acquisition of an EPI-BOLD sequence with simultaneous recording of eye tracker video. Motion-affected and motion-free whole brain T1-weighted MRI were also obtained. Image coregistration was used to estimate changes in head pose over the duration of the EPI-BOLD scan, and used to train a predictive model to estimate head pose changes from the video data. Model performance was quantified by assessing the coefficient of determination (R2). We evaluated the utility of our technique by assessing the relationship between video-based head pose changes during structural MRI and (i) vertex-wise cortical thickness and (ii) subcortical volume estimates. Results: Video-based head pose estimates were significantly correlated with ground truth head pose changes estimated from EPI-BOLD imaging in a hold-out dataset. We observed a general brain-wide overall reduction in cortical thickness with increased head motion, with some isolated regions showing increased cortical thickness estimates with increased motion. Subcortical volumes were generally reduced in motion affected scans. Conclusions: We trained a predictive model to estimate changes in head pose during structural MRI scans using in-scanner eye tracker video. The method is independent of individual image acquisition parameters and does not require markers to be to be fixed to the patient, suggesting it may be well suited to clinical imaging and research environments. Head pose changes estimated using our approach can be used as covariates for morphometric image analyses to improve the neurobiological validity of structural imaging studies of brain development and disease. |
Gabriel Pelletier; Nadav Aridan; Lesley K. Fellows; Tom Schonberg A preferential role for ventromedial prefrontal cortex in assessing "the value of the whole" in multiattribute object evaluation Journal Article In: Journal of Neuroscience, vol. 41, no. 23, pp. 5056–5068, 2021. @article{Pelletier2021, Everyday decision-making commonly involves assigning values to complex objects with multiple value-relevant attributes. Drawing on object recognition theories, we hypothesized two routes to multiattribute evaluation: Assessing the value of the whole object based on holistic attribute configuration or summing individual attribute values. In two samples of healthy human male and female participants undergoing eye tracking and functional magnetic resonance imaging (fMRI) while evaluating novel pseudo objects, we found evidence for both forms of evaluation. Fixations to and transitions between attributes differed systematically when the value of pseudo objects was associated with individual attributes or attribute configurations. Ventromedial prefrontal cortex (vmPFC) and perirhinal cortex were engaged when configural processing was required. These results converge with our recent findings that individuals with vmPFC lesions were impaired in decisions requiring configural evaluation but not when evaluating the sum of the parts. This suggests that multiattribute decision-making engages distinct evaluation mechanisms relying on partially dissociable neural substrates, depending on the relationship between attributes and value. |
Samuel Planton; Stanislas Dehaene Cerebral representation of sequence patterns across multiple presentation formats Journal Article In: Cortex, vol. 145, pp. 13–36, 2021. @article{Planton2021, The ability to detect the abstract pattern underlying a temporal sequence of events is crucial to many human activities, including language and mathematics, but its cortical correlates remain poorly understood. It is also unclear whether repeated exposure to the same sequence of sensory stimuli is sufficient to induce the encoding of an abstract amodal representation of the pattern. Using functional MRI, we probed the existence of such abstract codes for sequential patterns, their localization in the human brain, and their relation to existing language and math-responsive networks. We used a passive sequence violation paradigm, in which a given sequence is repeatedly presented before rare deviant sequences are introduced. We presented two binary patterns, AABB and ABAB, in four presentation formats, either visual or auditory, and either cued by the identity of the stimuli or by their spatial location. Regardless of the presentation format, a habituation to the repeated pattern and a response to pattern violations were seen in a set of inferior frontal, intraparietal and temporal areas. Within language areas, such pattern-violation responses were only found in the inferior frontal gyrus (IFG), whereas all math-responsive regions responded to pattern changes. Most of these regions also responded whenever the modality or the cue changed, suggesting a general sensitivity to violation detection. Thus, the representation of sequence patterns appears to be distributed, yet to include a core set of abstract amodal regions, particularly the IFG. |
Sonia Poltoratski; Kendrick Kay; Dawn Finzi; Kalanit Grill-Spector Holistic face recognition is an emergent phenomenon of spatial processing in face-selective regions Journal Article In: Nature Communications, vol. 12, pp. 4745, 2021. @article{Poltoratski2021, Spatial processing by receptive fields is a core property of the visual system. However, it is unknown how spatial processing in high-level regions contributes to recognition behavior. As face inversion is thought to disrupt typical holistic processing of information in faces, we mapped population receptive fields (pRFs) with upright and inverted faces in the human visual system. Here we show that in face-selective regions, but not primary visual cortex, pRFs and overall visual field coverage are smaller and shifted downward in response to face inversion. From these measurements, we successfully predict the relative behavioral detriment of face inversion at different positions in the visual field. This correspondence between neural measurements and behavior demonstrates how spatial processing in face-selective regions may enable holistic perception. These results not only show that spatial processing in high-level visual regions is dynamically used towards recognition, but also suggest a powerful approach for bridging neural computations by receptive fields to behavior. |
John R. Purcell; Andrew Jahn; Justin M. Fine; Joshua W. Brown Neural correlates of visual attention during risky decision evidence integration Journal Article In: NeuroImage, vol. 234, pp. 117979, 2021. @article{Purcell2021, Value-based decision-making is presumed to involve a dynamic integration process that supports assessing the potential outcomes of different choice options. Decision frameworks assume the value of a decision rests on both the desirability and risk surrounding an outcome. Previous work has highlighted neural representations of risk in the human brain, and their relation to decision choice. Key neural regions including the insula and anterior cingulate cortex (ACC) have been implicated in encoding the effects of risk on decision outcomes, including approach and avoidance. Yet, it remains unknown whether these regions are involved in the dynamic integration processes that precede and drive choice, and their relationship with ongoing attention. Here, we used concurrent fMRI and eye-tracking to discern neural activation related to visual attention preceding choice between sure-thing (i.e. safe) and risky gamble options. We found activation in both dorsal ACC (dACC) and posterior insula (PI) scaled in opposite directions with the difference in attention to risky rewards relative to risky losses. PI activation also differentiated foveations on both risky options (rewards and losses) relative to a sure-thing option. These findings point to ACC involvement in ongoing evaluation of risky but higher value options. The role of PI in risky outcomes points to a more general evaluative role in the decision-making that compares both safe and risky outcomes, irrespective of potential for gains or losses. |
Yali Pan; Steven Frisson; Ole Jensen Neural evidence for lexical parafoveal processing Journal Article In: Nature Communications, vol. 12, pp. 5234, 2021. @article{Pan2021a, In spite of the reduced visual acuity, parafoveal information plays an important role in natural reading. However, competing models on reading disagree on whether words are previewed parafoveally at the lexical level. We find neural evidence for lexical parafoveal processing by combining a rapid invisible frequency tagging (RIFT) approach with magnetoencephalography (MEG) and eye-tracking. In a silent reading task, target words are tagged (flickered) subliminally at 60 Hz. The tagging responses measured when fixating on the pre-target word reflect parafoveal processing of the target word. We observe stronger tagging responses during pre-target fixations when followed by low compared with high lexical frequency targets. Moreover, this lexical parafoveal processing is associated with individual reading speed. Our findings suggest that reading unfolds in the fovea and parafovea simultaneously to support fluent reading. |
J. A. Nij Bijvank; E. M. M. Strijbis; I. M. Nauta; S. D. Kulik; L. J. Balk; C. J. Stam; A. Hillebrand; J. J. G. Geurts; B. M. J. Uitdehaag; L. J. Rijn; A. Petzold; M. M. Schoonheim Impaired saccadic eye movements in multiple sclerosis are related to altered functional connectivity of the oculomotor brain network Journal Article In: NeuroImage: Clinical, vol. 32, pp. 102848, 2021. @article{NijBijvank2021, Background: Impaired eye movements in multiple sclerosis (MS) are common and could represent a non-invasive and accurate measure of (dys)functioning of interconnected areas within the complex brain network. The aim of this study was to test whether altered saccadic eye movements are related to changes in functional connectivity (FC) in patients with MS. Methods: Cross-sectional eye movement (pro-saccades and anti-saccades) and magnetoencephalography (MEG) data from the Amsterdam MS cohort were included from 176 MS patients and 33 healthy controls. FC was calculated between all regions of the Brainnetome atlas in six conventional frequency bands. Cognitive function and disability were evaluated by previously validated measures. The relationships between saccadic parameters and both FC and clinical scores in MS patients were analysed using multivariate linear regression models. Results: In MS pro- and anti-saccades were abnormal compared to healthy controls A relationship of saccadic eye movements was found with FC of the oculomotor network, which was stronger for regional than global FC. In general, abnormal eye movements were related to higher delta and theta FC but lower beta FC. Strongest associations were found for pro-saccadic latency and FC of the precuneus (beta band β = -0.23 |
Rodolfo Solís-Vivanco; Ole Jensen; Mathilde Bonnefond New insights on the ventral attention network: Active suppression and involuntary recruitment during a bimodal task Journal Article In: Human Brain Mapping, vol. 42, no. 6, pp. 1699–1713, 2021. @article{SolisVivanco2021, Detection of unexpected, yet relevant events is essential in daily life. fMRI studies have revealed the involvement of the ventral attention network (VAN), including the temporo-parietal junction (TPJ), in such process. In this MEG study with 34 participants (17 women), we used a bimodal (visual/auditory) attention task to determine the neuronal dynamics associated with suppression of the activity of the VAN during top-down attention and its recruitment when information from the unattended sensory modality is involuntarily integrated. We observed an anticipatory power increase of alpha/beta oscillations (12–20 Hz, previously associated with functional inhibition) in the VAN following a cue indicating the modality to attend. Stronger VAN power increases were associated with better task performance, suggesting that the VAN suppression prevents shifting attention to distractors. Moreover, the TPJ was synchronized with the frontal eye field in that frequency band, indicating that the dorsal attention network (DAN) might participate in such suppression. Furthermore, we found a 12–20 Hz power decrease and enhanced synchronization, in both the VAN and DAN, when information between sensory modalities was congruent, suggesting an involvement of these networks when attention is involuntarily enhanced due to multisensory integration. Our results show that effective multimodal attentional allocation includes the modulation of the VAN and DAN through upper-alpha/beta oscillations. Altogether these results indicate that the suppressing role of alpha/beta oscillations might operate beyond sensory regions. |
Isabelle A. Rosenthal; Shridhar R. Singh; Katherine L. Hermann; Dimitrios Pantazis; Bevil R. Conway Color space geometry uncovered with magnetoencephalography Journal Article In: Current Biology, vol. 31, no. 3, pp. 515–526, 2021. @article{Rosenthal2021, The geometry that describes the relationship among colors, and the neural mechanisms that support color vision, are unsettled. Here, we use multivariate analyses of measurements of brain activity obtained with magnetoencephalography to reverse-engineer a geometry of the neural representation of color space. The analyses depend upon determining similarity relationships among the spatial patterns of neural responses to different colors and assessing how these relationships change in time. We evaluate the approach by relating the results to universal patterns in color naming. Two prominent patterns of color naming could be accounted for by the decoding results: the greater precision in naming warm colors compared to cool colors evident by an interaction of hue and lightness, and the preeminence among colors of reddish hues. Additional experiments showed that classifiers trained on responses to color words could decode color from data obtained using colored stimuli, but only at relatively long delays after stimulus onset. These results provide evidence that perceptual representations can give rise to semantic representations, but not the reverse. Taken together, the results uncover a dynamic geometry that provides neural correlates for color appearance and generates new hypotheses about the structure of color space. |
Anastasia O. Ovchinnikova; Anatoly N. Vasilyev; Ivan P. Zubarev; Bogdan L. Kozyrskiy; Sergei L. Shishkin MEG-based detection of voluntary eye fixations used to control a computer Journal Article In: Frontiers in Neuroscience, vol. 15, pp. 619591, 2021. @article{Ovchinnikova2021, Gaze-based input is an efficient way of hand-free human-computer interaction. However, it suffers from the inability of gaze-based interfaces to discriminate voluntary and spontaneous gaze behaviors, which are overtly similar. Here, we demonstrate that voluntary eye fixations can be discriminated from spontaneous ones using short segments of magnetoencephalography (MEG) data measured immediately after the fixation onset. Recently proposed convolutional neural networks (CNNs), linear finite impulse response filters CNN (LF-CNN) and vector autoregressive CNN (VAR-CNN), were applied for binary classification of the MEG signals related to spontaneous and voluntary eye fixations collected in healthy participants (n = 25) who performed a game-like task by fixating on targets voluntarily for 500 ms or longer. Voluntary fixations were identified as those followed by a fixation in a special confirmatory area. Spontaneous vs. voluntary fixation-related single-trial 700 ms MEG segments were non-randomly classified in the majority of participants, with the group average cross-validated ROC AUC of 0.66 ± 0.07 for LF-CNN and 0.67 ± 0.07 for VAR-CNN (M ± SD). When the time interval, from which the MEG data were taken, was extended beyond the onset of the visual feedback, the group average classification performance increased up to 0.91. Analysis of spatial patterns contributing to classification did not reveal signs of significant eye movement impact on the classification results. We conclude that the classification of MEG signals has a certain potential to support gaze-based interfaces by avoiding false responses to spontaneous eye fixations on a single-trial basis. Current results for intention detection prior to gaze-based interface's feedback, however, are not sufficient for online single-trial eye fixation classification using MEG data alone, and further work is needed to find out if it could be used in practical applications. |
Thomas Pfeffer; Adrian Ponce-Alvarez; Konstantinos Tsetsos; Thomas Meindertsma; Christoffer Julius Gahnström; Ruud Lucas Brink; Guido Nolte; Andreas Karl Engel; Gustavo Deco; Tobias Hinrich Donner Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability Journal Article In: Science Advances, vol. 7, no. 29, pp. eabf5620, 2021. @article{Pfeffer2021, Influential theories postulate distinct roles of catecholamines and acetylcholine in cognition and behavior. However, previous physiological work reported similar effects of these neuromodulators on the response properties (specifically, the gain) of individual cortical neurons. Here, we show a double dissociation between the effects of catecholamines and acetylcholine at the level of large-scale interactions between cortical areas in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. An acetylcholine boost decreased interactions during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: The local excitation-inhibition balance (more strongly increased by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted noisier decision-making, which we confirmed for both perceptual and value-based choice behavior. Our work highlights specific circuit mechanisms for shaping cortical network interactions and behavioral variability by key neuromodulatory systems. |
Aurélien Weiss; Valérian Chambon; Junseok K. Lee; Jan Drugowitsch; Valentin Wyart Interacting with volatile environments stabilizes hidden-state inference and its brain signatures Journal Article In: Nature Communications, vol. 12, pp. 2228, 2021. @article{Weiss2021, Making accurate decisions in uncertain environments requires identifying the generative cause of sensory cues, but also the expected outcomes of possible actions. Although both cognitive processes can be formalized as Bayesian inference, they are commonly studied using different experimental frameworks, making their formal comparison difficult. Here, by framing a reversal learning task either as cue-based or outcome-based inference, we found that humans perceive the same volatile environment as more stable when inferring its hidden state by interaction with uncertain outcomes than by observation of equally uncertain cues. Multivariate patterns of magnetoencephalographic (MEG) activity reflected this behavioral difference in the neural interaction between inferred beliefs and incoming evidence, an effect originating from associative regions in the temporal lobe. Together, these findings indicate that the degree of control over the sampling of volatile environments shapes human learning and decision-making under uncertainty. |
Benjamin J. Stauch; Alina Peter; Heike Schuler; Pascal Fries Stimulus-specific plasticity in human visual gamma-band activity and functional connectivity Journal Article In: eLife, vol. 10, pp. e68240, 2021. @article{Stauch2021, Under natural conditions, the visual system often sees a given input repeatedly. This provides an opportunity to optimize processing of the repeated stimuli. Stimulus repetition has been shown to strongly modulate neuronal-gamma band synchronization, yet crucial questions remained open. Here we used magnetoencephalography in 30 human subjects and find that gamma decreases across ≈10 repetitions and then increases across further repetitions, revealing plastic changes of the activated neuronal circuits. Crucially, increases induced by one stimulus did not affect responses to other stimuli, demonstrating stimulus specificity. Changes partially persisted when the inducing stimulus was repeated after 25 minutes of intervening stimuli. They were strongest in early visual cortex and increased interareal feedforward influences. Our results suggest that early visual cortex gamma synchronization enables adaptive neuronal processing of recurring stimuli. These and previously reported changes might be due to an interaction of oscillatory dynamics with established synaptic plasticity mechanisms. |
Yu Takagi; Laurence Tudor Hunt; Mark W. Woolrich; Timothy E. J. Behrens; Miriam C. Klein-Flügge Adapting non-invasive human recordings along multiple task-axes shows unfolding of spontaneous and over-trained choice Journal Article In: eLife, vol. 10, pp. 1–27, 2021. @article{Takagi2021, Choices rely on a transformation of sensory inputs into motor responses. Using invasive single neuron recordings, the evolution of a choice process has been tracked by projecting population neural responses into state spaces. Here, we develop an approach that allows us to recover similar trajectories on a millisecond timescale in non-invasive human recordings. We selectively suppress activity related to three task-axes, relevant and irrelevant sensory inputs and response direction, in magnetoencephalography data acquired during context-dependent choices. Recordings from premotor cortex show a progression from processing sensory input to processing the response. In contrast to previous macaque recordings, information related to choice-irrelevant features is represented more weakly than choice-relevant sensory information. To test whether this mechanistic difference between species is caused by extensive over-training common in non-human primate studies, we trained humans on >20,000 trials of the task. Choice-irrelevant features were still weaker than relevant features in premotor cortex after over-training. |
Ella Podvalny; Leana E. King; Biyu J. He Spectral signature and behavioral consequence of spontaneous shifts of pupil-linked arousal in human Journal Article In: eLife, vol. 10, pp. e68265, 2021. @article{Podvalny2021, Arousal levels perpetually rise and fall spontaneously. How markers of arousal—pupil size and frequency content of brain activity—relate to each other and influence behavior in humans is poorly understood. We simultaneously monitored magnetoencephalography and pupil in healthy volunteers at rest and during a visual perceptual decision-making task. Spontaneously varying pupil size correlates with power of brain activity in most frequency bands across large-scale resting-state cortical networks. Pupil size recorded at prestimulus baseline correlates with subsequent shifts in detection bias (c) and sensitivity (d'). When dissociated from pupil-linked state, prestimulus spectral power of resting state networks still predicts perceptual behavior. Fast spontaneous pupil constriction and dilation correlate with large-scale brain activity as well but not perceptual behavior. Our results illuminate the relation between central and peripheral arousal markers and their respective roles in human perceptual decision-making. |
Bo Yao; Jason R. Taylor; Briony Banks; Sonja A. Kotz Reading direct speech quotes increases theta phase-locking: Evidence for cortical tracking of inner speech? Journal Article In: NeuroImage, vol. 239, pp. 118313, 2021. @article{Yao2021a, Growing evidence shows that theta-band (4–7 Hz) activity in the auditory cortex phase-locks to rhythms of overt speech. Does theta activity also encode the rhythmic dynamics of inner speech? Previous research established that silent reading of direct speech quotes (e.g., Mary said: “This dress is lovely!”) elicits more vivid inner speech than indirect speech quotes (e.g., Mary said that the dress was lovely). As we cannot directly track the phase alignment between theta activity and inner speech over time, we used EEG to measure the brain's phase-locked responses to the onset of speech quote reading. We found that direct (vs. indirect) quote reading was associated with increased theta phase synchrony over trials at 250–500 ms post-reading onset, with sources of the evoked activity estimated in the speech processing network. An eye-tracking control experiment confirmed that increased theta phase synchrony in direct quote reading was not driven by eye movement patterns, and more likely reflects synchronous phase resetting at the onset of inner speech. These findings suggest a functional role of theta phase modulation in reading-induced inner speech. |
Nicole H. Yuen; Fred Tam; Nathan W. Churchill; Tom A. Schweizer; Simon J. Graham Driving with distraction: Measuring brain activity and oculomotor behavior using fMRI and eye-tracking Journal Article In: Frontiers in Human Neuroscience, vol. 15, pp. 1–20, 2021. @article{Yuen2021, Introduction: Driving motor vehicles is a complex task that depends heavily on how visual stimuli are received and subsequently processed by the brain. The potential impact of distraction on driving performance is well known and poses a safety concern – especially for individuals with cognitive impairments who may be clinically unfit to drive. The present study is the first to combine functional magnetic resonance imaging (fMRI) and eye-tracking during simulated driving with distraction, providing oculomotor metrics to enhance scientific understanding of the brain activity that supports driving performance. Materials and Methods: As initial work, twelve healthy young, right-handed participants performed turns ranging in complexity, including simple right and left turns without oncoming traffic, and left turns with oncoming traffic. Distraction was introduced as an auditory task during straight driving, and during left turns with oncoming traffic. Eye-tracking data were recorded during fMRI to characterize fixations, saccades, pupil diameter and blink rate. Results: Brain activation maps for right turns, left turns without oncoming traffic, left turns with oncoming traffic, and the distraction conditions were largely consistent with previous literature reporting the neural correlates of simulated driving. When the effects of distraction were evaluated for left turns with oncoming traffic, increased activation was observed in areas involved in executive function (e.g., middle and inferior frontal gyri) as well as decreased activation in the posterior brain (e.g., middle and superior occipital gyri). Whereas driving performance remained mostly unchanged (e.g., turn speed, time to turn, collisions), the oculomotor measures showed that distraction resulted in more consistent gaze at oncoming traffic in a small area of the visual scene; less time spent gazing at off-road targets (e.g., speedometer, rear-view mirror); more time spent performing saccadic eye movements; and decreased blink rate. Conclusion: Oculomotor behavior modulated with driving task complexity and distraction in a manner consistent with the brain activation features revealed by fMRI. The results suggest that eye-tracking technology should be included in future fMRI studies of simulated driving behavior in targeted populations, such as the elderly and individuals with cognitive complaints – ultimately toward developing better technology to assess and enhance fitness to drive. |
Shengnan Zhu; Yang Zhang; Junli Dong; Lihong Chen; Wenbo Luo Low-spatial-frequency information facilitates threat detection in a response-specific manner Journal Article In: Journal of Vision, vol. 21, no. 4, pp. 1–9, 2021. @article{Zhu2021a, The role of different spatial frequency bands in threat detection has been explored extensively. However, most studies use manual responses and the results are mixed. Here, we aimed to investigate the contribution of spatial frequency information to threat detection by using three response types, including manual responses, eye movements, and reaching movements, together with a priming paradigm. The results showed that both saccade and reaching responses were significantly faster to threatening stimuli than to nonthreatening stimuli when primed by low-spatial-frequency gratings rather than by high-spatial-frequency gratings. However, the manual response times to threatening stimuli were comparable to nonthreatening stimuli, irrespective of the spatial frequency content of the primes. The findings provide clear evidence that low-spatial-frequency information can facilitate threat detection in a response-specific manner, possibly through the subcortical magnocellular pathway dedicated to processing threat-related signals, which is automatically prioritized in the oculomotor system and biases behavior. |
Kristin Marie Zimmermann; Kirsten Daniela Schmidt; Franziska Gronow; Jens Sommer; Frank Leweke; Andreas Jansen Seeing things differently: Gaze shapes neural signal during mentalizing according to emotional awareness Journal Article In: NeuroImage, vol. 238, pp. 1–14, 2021. @article{Zimmermann2021, Studies on social cognition often use complex visual stimuli to asses neural processes attributed to abilities like “mentalizing” or “Theory of Mind” (ToM). During the processing of these stimuli, eye gaze, however, shapes neural signal patterns. Individual differences in neural operations on social cognition may therefore be obscured if individuals' gaze behavior differs systematically. These obstacles can be overcome by the combined analysis of neural signal and natural viewing behavior. Here, we combined functional magnetic resonance imaging (fMRI) with eye-tracking to examine effects of unconstrained gaze on neural ToM processes in healthy individuals with differing levels of emotional awareness, i.e. alexithymia. First, as previously described for emotional tasks, people with higher alexithymia levels look less at eyes in both ToM and task-free viewing contexts. Further, we find that neural ToM processes are not affected by individual differences in alexithymia per se. Instead, depending on alexithymia levels, gaze on critical stimulus aspects reversely shapes the signal in medial prefrontal cortex (MPFC) and anterior temporoparietal junction (TPJ) as distinct nodes of the ToM system. These results emphasize that natural selective attention affects fMRI patterns well beyond the visual system. Our study implies that, whenever using a task with multiple degrees of freedom in scan paths, ignoring the latter might obscure important conclusions. |
Fosca Al Roumi; Sébastien Marti; Liping Wang; Marie Amalric; Stanislas Dehaene Mental compression of spatial sequences in human working memory using numerical and geometrical primitives Journal Article In: Neuron, vol. 109, no. 16, pp. 2627–2639, 2021. @article{AlRoumi2021, How does the human brain store sequences of spatial locations? We propose that each sequence is internally compressed using an abstract, language-like code that captures its numerical and geometrical regularities. We exposed participants to spatial sequences of fixed length but variable regularity while their brain activity was recorded using magneto-encephalography. Using multivariate decoders, each successive location could be decoded from brain signals, and upcoming locations were anticipated prior to their actual onset. Crucially, sequences with lower complexity, defined as the minimal description length provided by the formal language, led to lower error rates and to increased anticipations. Furthermore, neural codes specific to the numerical and geometrical primitives of the postulated language could be detected, both in isolation and within the sequences. These results suggest that the human brain detects sequence regularities at multiple nested levels and uses them to compress long sequences in working memory. |
Damiano Azzalini; Anne Buot; Stefano Palminteri; Catherine Tallon-Baudry Responses to heartbeats in ventromedial prefrontal cortex contribute to subjective preference-based decisions Journal Article In: Journal of Neuroscience, vol. 41, no. 23, pp. 5102–5114, 2021. @article{Azzalini2021, Forrest Gump or The Matrix? Preference-based decisions are subjective and entail self-reflection. However, these self-related features are unaccounted for by known neural mechanisms of valuation and choice. Self-related processes have been linked to a basic interoceptive biological mechanism, the neural monitoring of heartbeats, in particular in ventromedial prefrontal cortex (vmPFC), a region also involved in value encoding. We thus hypothesized a functional coupling between the neural monitoring of heartbeats and the precision of value encoding in vmPFC. Human participants of both sexes were presented with pairs of movie titles. They indicated either which movie they preferred or performed a control objective visual discrimination that did not require self-reflection. Using magnetoencephalography, we measured heartbeat-evoked responses (HERs) before option presentation and confirmed that HERs in vmPFC were larger when preparing for the subjective, self-related task. We retrieved the expected cortical value network during choice with time-resolved statistical modeling. Crucially, we show that larger HERs before option presentation are followed by stronger value encoding during choice in vmPFC. This effect is independent of overall vmPFC baseline activity. The neural interaction between HERs and value encoding predicted preference-based choice consistency over time, accounting for both interindividual differences and trial-to-trial fluctuations within individuals. Neither cardiac activity nor arousal fluctuations could account for any of the effects. HERs did not interact with the encoding of perceptual evidence in the discrimination task. Our results show that the self-reflection underlying preference-based decisions involves HERs, and that HER integration to subjective value encoding in vmPFC contributes to preference stability. |
Anne Buot; Damiano Azzalini; Maximilien Chaumon; Catherine Tallon-Baudry Does stroke volume influence heartbeat evoked responses? Journal Article In: Biological Psychology, vol. 165, pp. 108165, 2021. @article{Buot2021, We know surprisingly little on how heartbeat-evoked responses (HERs) vary with cardiac parameters. Here, we measured both stroke volume, or volume of blood ejected at each heartbeat, with impedance cardiography, and HER amplitude with magneto-encephalography, in 21 male and female participants at rest with eyes open. We observed that HER co-fluctuates with stroke volume on a beat-to-beat basis, but only when no correction for cardiac artifact was performed. This highlights the importance of an ICA correction tailored to the cardiac artifact. We also observed that easy-to-measure cardiac parameters (interbeat intervals, ECG amplitude) are sensitive to stroke volume fluctuations and can be used as proxies when stroke volume measurements are not available. Finally, interindividual differences in stroke volume were reflected in MEG data, but whether this effect is locked to heartbeats is unclear. Altogether, our results question assumptions on the link between stroke volume and HERs. |
Jonathan Daume; Peng Wang; Alexander Maye; Dan Zhang; Andreas K. Engel Non-rhythmic temporal prediction involves phase resets of low-frequency delta oscillations Journal Article In: NeuroImage, vol. 224, pp. 117376, 2021. @article{Daume2021, The phase of neural oscillatory signals aligns to the predicted onset of upcoming stimulation. Whether such phase alignments represent phase resets of underlying neural oscillations or just rhythmically evoked activity, and whether they can be observed in a rhythm-free visual context, however, remains unclear. Here, we recorded the magnetoencephalogram while participants were engaged in a temporal prediction task, judging the visual or tactile reappearance of a uniformly moving stimulus. The prediction conditions were contrasted with a control condition to dissociate phase adjustments of neural oscillations from stimulus-driven activity. We observed stronger delta band inter-trial phase consistency (ITPC) in a network of sensory, parietal and frontal brain areas, but no power increase reflecting stimulus-driven or prediction-related evoked activity. Delta ITPC further correlated with prediction performance in the cerebellum and visual cortex. Our results provide evidence that phase alignments of low-frequency neural oscillations underlie temporal predictions in a non-rhythmic visual and crossmodal context. |
Linda Drijvers; Ole Jensen; Eelke Spaak Rapid invisible frequency tagging reveals nonlinear integration of auditory and visual information Journal Article In: Human Brain Mapping, vol. 42, no. 4, pp. 1138–1152, 2021. @article{Drijvers2021, During communication in real-life settings, the brain integrates information from auditory and visual modalities to form a unified percept of our environment. In the current magnetoencephalography (MEG) study, we used rapid invisible frequency tagging (RIFT) to generate steady-state evoked fields and investigated the integration of audiovisual information in a semantic context. We presented participants with videos of an actress uttering action verbs (auditory; tagged at 61 Hz) accompanied by a gesture (visual; tagged at 68 Hz, using a projector with a 1,440 Hz refresh rate). Integration difficulty was manipulated by lower-order auditory factors (clear/degraded speech) and higher-order visual factors (congruent/incongruent gesture). We identified MEG spectral peaks at the individual (61/68 Hz) tagging frequencies. We furthermore observed a peak at the intermodulation frequency of the auditory and visually tagged signals (fvisual − fauditory = 7 Hz), specifically when lower-order integration was easiest because signal quality was optimal. This intermodulation peak is a signature of nonlinear audiovisual integration, and was strongest in left inferior frontal gyrus and left temporal regions; areas known to be involved in speech-gesture integration. The enhanced power at the intermodulation frequency thus reflects the ease of lower-order audiovisual integration and demonstrates that speech-gesture information interacts in higher-order language areas. Furthermore, we provide a proof-of-principle of the use of RIFT to study the integration of audiovisual stimuli, in relation to, for instance, semantic context. |