A characterization of the neural representation of confidence during probabilistic learning.

Learning in a stochastic and changing environment is a difficult task. Models of learning typically postulate that observations that deviate from the learned predictions are surprising and used to update those predictions. Bayesian accounts further posit the existence of a confidence-weighting mechanism: learning should be modulated by the confidence level that accompanies those predictions. However, the neural bases of this confidence are much less known than the ones of surprise. Here, we used a dynamic probability learning task and high-field MRI to identify putative cortical regions involved in the representation of confidence about predictions during human learning. We devised a stringent test based on the conjunction of four criteria. We localized several regions in parietal and frontal cortices whose activity is sensitive to the confidence of an ideal observer, specifically so with respect to potential confounds (surprise and predictability), and in a way that is invariant to which item is predicted. We also tested for functionality in two ways. First, we localized regions whose activity patterns at the subject level showed an effect of both confidence and surprise in qualitative agreement with the confidence-weighting principle. Second, we found neural representations of ideal confidence that also accounted for subjective confidence. Taken together, those results identify a set of cortical regions potentially implicated in the confidence-weighting of learning.

Subject-specific segregation of functional territories based on deep phenotyping.

Functional magnetic resonance imaging (fMRI) has opened the possibility to investigate how brain activity is modulated by behavior. Most studies so far are bound to one single task, in which functional responses to a handful of contrasts are analyzed and reported as a group average brain map. Contrariwise, recent data-collection efforts have started to target a systematic spatial representation of multiple mental functions. In this paper, we leverage the Individual Brain Charting (IBC) dataset-a high-resolution task-fMRI dataset acquired in a fixed environment-in order to study the feasibility of individual mapping. First, we verify that the IBC brain maps reproduce those obtained from previous, large-scale datasets using the same tasks. Second, we confirm that the elementary spatial components, inferred across all tasks, are consistently mapped within and, to a lesser extent, across participants. Third, we demonstrate the relevance of the topographic information of the individual contrast maps, showing that contrasts from one task can be predicted by contrasts from other tasks. At last, we showcase the benefit of contrast accumulation for the fine functional characterization of brain regions within a prespecified network. To this end, we analyze the cognitive profile of functional territories pertaining to the language network and prove that these profiles generalize across participants.

Mapping subcomponents of numerical cognition in relation to functional and anatomical landmarks of human parietal cortex.

Human functional imaging has identified the middle part of the intraparietal sulcus (IPS) as an important brain substrate for different types of numerical tasks. This area is often equated with the macaque ventral intraparietal area (VIP) where neuronal selectivity for non-symbolic numerical stimuli (sets of items) is found. However, the low spatial resolution and whole-brain averaging analysis performed in most fMRI studies limit the extent to which an exact correspondence of activations in different numerical tasks with specific sub-regions of the IPS can be established. Here we acquired high-resolution 7T fMRI data in a group of human adults and related the activations in several numerical contrasts (implying different numerical stimuli and tasks) to anatomical and functional landmarks on the cortical surface. Our results reveal a functional heterogeneity within human intraparietal cortex where the retinotopic visual field maps in superior/medial parts of the IPS and superior parietal gyrus respond preferentially to the visual processing of concrete sets of items (over single Arabic numerals), whereas lateral/inferior parts of the IPS are predominantly recruited during numerical operations such as calculation and quantitative comparison. Since calculation and comparison-related activity fell mainly outside the retinotopic visual field maps considered the human functional equivalent of the monkey VIP/LIP complex, the areas most activated during such numerical operations in humans are likely different from VIP.

Excessive visual crowding effects in developmental dyscalculia.

Visual crowding refers to the inability to identify objects when surrounded by other similar items. Crowding-like mechanisms are thought to play a key role in numerical perception by determining the sensory mechanisms through which ensembles are perceived. Enhanced visual crowding might hence prevent the normal development of a system involved in segregating and perceiving discrete numbers of items and ultimately the acquisition of more abstract numerical skills. Here, we investigated whether excessive crowding occurs in developmental dyscalculia (DD), a neurodevelopmental disorder characterized by difficulty in learning the most basic numerical and arithmetical concepts, and whether it is found independently of associated major reading and attentional difficulties. We measured spatial crowding in two groups of adult individuals with DD and control subjects. In separate experiments, participants were asked to discriminate the orientation of a Gabor patch either in isolation or under spatial crowding. Orientation discrimination thresholds were comparable across groups when stimuli were shown in isolation, yet they were much higher for the DD group with respect to the control group when the target was crowded by closely neighbouring flanking gratings. The difficulty in discriminating orientation (as reflected by the combination of accuracy and reaction times) in the DD compared to the control group persisted over several larger target flanker distances. Finally, we found that the degree of such spatial crowding correlated with impairments in mathematical abilities even when controlling for visual attention and reading skills. These results suggest that excessive crowding effects might be a characteristic of DD, independent of other associated neurodevelopmental disorders.

Conceptual and Perceptual Dimensions of Word Meaning Are Recovered Rapidly and in Parallel during Reading.

A single word (the noun "elephant") encapsulates a complex multidimensional meaning, including both perceptual ("big", "gray", "trumpeting") and conceptual ("mammal", "can be found in India") features. Opposing theories make different predictions as to whether different features (also conceivable as dimensions of the semantic space) are stored in similar neural regions and recovered with similar temporal dynamics during word reading. In this magnetoencephalography study, we tracked the brain activity of healthy human participants while reading single words varying orthogonally across three semantic dimensions: two perceptual ones (i.e., the average implied real-world size and the average strength of association with a prototypical sound) and a conceptual one (i.e., the semantic category). The results indicate that perceptual and conceptual representations are supported by partially segregated neural networks: Whereas visual and auditory dimensions are encoded in the phase coherence of low-frequency oscillations of occipital and superior temporal regions, respectively, semantic features are encoded in the power of low-frequency oscillations of anterior temporal and inferior parietal areas. However, despite the differences, these representations appear to emerge at the same latency: around 200 msec after stimulus onset. Taken together, these findings suggest that perceptual and conceptual dimensions of the semantic space are recovered automatically, rapidly, and in parallel during word reading.

Perceiving numerosity from birth.

Leibovich et al. opened up an important discussion on the nature and origins of numerosity perception. The authors rightly point out that non-numerical features of stimuli influence this ability. Despite these biases, there is evidence that from birth, humans perceive and represent numerosities, and not just non-numerical quantitative features such as item size, density, and convex hull.

Word meaning in the ventral visual path: a perceptual to conceptual gradient of semantic coding.

The meaning of words referring to concrete items is thought of as a multidimensional representation that includes both perceptual (e.g., average size, prototypical color) and conceptual (e.g., taxonomic class) dimensions. Are these different dimensions coded in different brain regions? In healthy human subjects, we tested the presence of a mapping between the implied real object size (a perceptual dimension) and the taxonomic categories at different levels of specificity (conceptual dimensions) of a series of words, and the patterns of brain activity recorded with functional magnetic resonance imaging in six areas along the ventral occipito-temporal cortical path. Combining multivariate pattern classification and representational similarity analysis, we found that the real object size implied by a word appears to be primarily encoded in early visual regions, while the taxonomic category and sub-categorical cluster in more anterior temporal regions. This anteroposterior gradient of information content indicates that different areas along the ventral stream encode complementary dimensions of the semantic space.

A shared, flexible neural map architecture reflects capacity limits in both visual short-term memory and enumeration.

Human cognition is characterized by severe capacity limits: we can accurately track, enumerate, or hold in mind only a small number of items at a time. It remains debated whether capacity limitations across tasks are determined by a common system. Here we measure brain activation of adult subjects performing either a visual short-term memory (vSTM) task consisting of holding in mind precise information about the orientation and position of a variable number of items, or an enumeration task consisting of assessing the number of items in those sets. We show that task-specific capacity limits (three to four items in enumeration and two to three in vSTM) are neurally reflected in the activity of the posterior parietal cortex (PPC): an identical set of voxels in this region, commonly activated during the two tasks, changed its overall response profile reflecting task-specific capacity limitations. These results, replicated in a second experiment, were further supported by multivariate pattern analysis in which we could decode the number of items presented over a larger range during enumeration than during vSTM. Finally, we simulated our results with a computational model of PPC using a saliency map architecture in which the level of mutual inhibition between nodes gives rise to capacity limitations and reflects the task-dependent precision with which objects need to be encoded (high precision for vSTM, lower precision for enumeration). Together, our work supports the existence of a common, flexible system underlying capacity limits across tasks in PPC that may take the form of a saliency map.

Human brain representations of internally generated outcomes of approximate calculation revealed by ultra-high-field brain imaging.

Much of human culture's advanced technology owes its existence to the ability to mentally manipulate quantities. Neuroscience has described the brain regions overall recruited by numerical tasks and the neuronal codes representing individual quantities during perceptual tasks. Nevertheless, it remains unknown how quantity representations are combined or transformed during mental computations and how specific quantities are coded in the brain when generated as the result of internal computations rather than evoked by a stimulus. Here, we imaged the brains of adult human subjects at 7 Tesla during an approximate calculation task designed to disentangle in- and outputs of the computation from the operation itself. While physically presented sample numerosities were distinguished in activity patterns along the dorsal visual pathway and within frontal and occipito-temporal regions, a representation of the internally generated result was most prominently detected in higher order regions such as angular gyrus and lateral prefrontal cortex. Behavioral precision in the task was related to cross-decoding performance between sample and result representations in medial IPS regions. This suggests the transformation of sample into result may be carried out within dorsal stream sensory-motor integration regions, and resulting outputs maintained for task purposes in higher-level regions in a format possibly detached from sensory-evoked inputs.

Temporal tuning properties along the human ventral visual stream.

Both our environment and our behavior contain many spatiotemporal regularities. Preferential and differential tuning of neural populations to these regularities can be demonstrated by assessing rate dependence of neural responses evoked during continuous periodic stimulation. Here, we used functional magnetic resonance imaging to measure regional variations of temporal sensitivity along the human ventral visual stream. By alternating one face and one house stimulus, we combined sufficient low-level signal modulation with changes in semantic meaning and could therefore drive all tiers of visual cortex strongly enough to assess rate dependence. We found several dissociations between early visual cortex and middle- and higher-tier regions. First, there was a progressive slowing down of stimulation rates yielding peak responses along the ventral visual stream. This finding shows the width of temporal integration windows to increase at higher hierarchical levels. Next, for fixed rates, early but not higher visual cortex responses additionally depended on the length of stimulus exposure, which may indicate increased persistence of responses to short stimuli at higher hierarchical levels. Finally, attention, which was recruited by an incidental task, interacted with stimulation rate and shifted tuning peaks toward lower frequencies. Together, these findings quantify neural response properties that are likely to be operational during natural vision and that provide putative neurofunctional substrates of mechanisms that are relevant in several psychophysical phenomena as masking and the attentional blink. Moreover, they illustrate temporal constraints for translating the deployment of attention into enhanced neural responses and thereby account for lower limits of attentional dwell time.

Reduced 2D form coherence and 3D structure from motion sensitivity in developmental dyscalculia.

Developmental dyscalculia (DD) is a specific learning disability affecting the development of numerical and arithmetical skills. The origin of DD is typically attributed to the suboptimal functioning of key regions within the dorsal visual stream (parietal cortex) which support numerical cognition. While DD individuals are often impaired in visual numerosity perception, the extent to which they also show a wider range of visual dysfunctions is poorly documented. In the current study we measured sensitivity to global motion (translational and flow), 2D static form (Glass patterns) and 3D structure from motion in adults with DD and control subjects. While sensitivity to global motion was comparable across groups, thresholds for static form and structure from motion were higher in the DD compared to the control group, irrespective of associated reading impairments. Glass pattern sensitivity predicted numerical abilities, and this relation could not be explained by recently reported differences in visual crowding. Since global form sensitivity has often been considered an index of ventral stream function, our findings could indicate a cortical dysfunction extending beyond the dorsal visual stream. Alternatively, they would fit with a role of parietal cortex in form perception under challenging conditions requiring multiple element integration.

Specialization for written words over objects in the visual cortex.

The Visual Word Form Area (VWFA) is part of the left ventral visual stream that underlies the invariant identification of visual words. It remains debated whether this region is truly selective for words relative to common objects; why this particular part of the visual system is reproducibly engaged in reading; and whether reading expertise also relies on perceptual learning within earlier visual areas. In this fMRI study we matched written words and line-drawings of objects in luminance, contour length and number of features. We then compared them to control images made by scrambling procedures that kept local features intact. Greater responses to written words than to objects were found not only in the VWFA, but also in areas V1/V2 and V3v/V4. Furthermore, by contrasting stimuli reduced either to line junctions (vertices) or to line midsegments, we showed that the VWFA partially overlaps with regions of ventral visual cortex particularly sensitive to the presence of line junctions that are useful for object recognition. Our results indicate that preferential processing of written words can be observed at multiple levels of the visual system. It is possible that responses in early visual areas might be due to some remaining differences between words and controls not eliminated in the present stimuli. However, our results concur with recent comparisons of literates and illiterates and suggest that these early visual activations reflect the effects of perceptual learning under pressure for fast, parallel processing that is more prominent in reading than other visual cognitive processes.

Spontaneous local variations in ongoing neural activity bias perceptual decisions.

Neural variability in responding to identical repeated stimuli has been related to trial-by-trial fluctuations in ongoing activity, yet the neural and perceptual consequences of these fluctuations remain poorly understood. Using functional neuroimaging, we recorded brain activity in subjects who reported perceptual decisions on an ambiguous figure, Rubin's vase-faces picture, which was briefly presented at variable intervals of > or = 20 s. Prestimulus activity in the fusiform face area, a cortical region preferentially responding to faces, was higher when subjects subsequently perceived faces instead of the vase. This finding suggests that endogenous variations in prestimulus neuronal activity biased subsequent perceptual inference. Furnishing evidence that evoked sensory responses, we then went on to show that the pre- and poststimulus activity interact in a nonlinear way and the ensuing perceptual decisions depend upon the prestimulus context in which they occur.

Resources Underlying Visuo-Spatial Working Memory Enable Veridical Large Numerosity Perception.

Humans can quickly approximate how many objects are in a visual image, but no clear consensus has been achieved on the cognitive resources underlying this ability. Previous work has lent support to the notion that mechanisms which explicitly represent the locations of multiple objects in the visual scene within a mental map are critical for both visuo-spatial working memory and enumeration (at least for relatively small numbers of items). Regarding the cognitive underpinnings of large numerosity perception, an issue currently subject to much controversy is why numerosity estimates are often non-veridical (i.e., susceptible to biases from non-numerical quantities). Such biases have been found to be particularly pronounced in individuals with developmental dyscalculia (DD), a learning disability affecting the acquisition of arithmetic skills. Motivated by findings showing that DD individuals are also often impaired in visuo-spatial working memory, we hypothesized that resources supporting this type of working memory, which allow for the simultaneous identification of multiple objects, might also be critical for precise and unbiased perception of larger numerosities. We therefore tested whether loading working memory of healthy adult participants during discrimination of large numerosities would lead to increased interference from non-numerical quantities. Participants performed a numerosity discrimination task on multi-item arrays in which numerical and non-numerical stimulus dimensions varied congruently or incongruently relative to each other, either in isolation or in the context of a concurrent visuo-spatial or verbal working memory task. During performance of the visuo-spatial, but not verbal, working memory task, precision in numerosity discrimination decreased, participants' choices became strongly biased by item size, and the strength of this bias correlated with measures of arithmetical skills. Moreover, the interference between numerosity and working memory tasks was bidirectional, with number discrimination impacting visuo-spatial (but not verbal) performance. Overall, these results suggest that representing visual numerosity in a way that is unbiased by non-numerical quantities relies on processes which explicitly segregate/identify the locations of multiple objects that are shared with visuo-spatial (but not verbal) working memory. This shared resource may potentially be impaired in DD, explaining the observed co-occurrence of working memory and numerosity discrimination deficits in this clinical population.

Separate coding of different gaze directions in the superior temporal sulcus and inferior parietal lobule.

Electrophysiological recording in the anterior superior temporal sulcus (STS) of monkeys has demonstrated separate cell populations responsive to direct and averted gaze. Human functional imaging has demonstrated posterior STS activation in gaze processing, particularly in coding the intentions conveyed by gaze, but to date has provided no evidence of dissociable coding of different gaze directions. Because the spatial resolution typical of group-based fMRI studies (approximately 6-10 mm) exceeds the size of cellular patches sensitive to different facial characteristics (1-4 mm in monkeys), a more sensitive technique may be required. We therefore used fMRI adaptation, which is considered to offer superior resolution, to investigate whether the human anterior STS contains representations of different gaze directions, as suggested by non-human primate research. Subjects viewed probe faces gazing left, directly ahead, or right. Adapting to leftward gaze produced a reduction in BOLD response to left relative to right (and direct) gaze probes in the anterior STS and inferior parietal cortex; rightward gaze adaptation produced a corresponding reduction to right gaze probes. Consistent with these findings, averted gaze in the adapted direction was misidentified as direct. Our study provides the first human evidence of dissociable neural systems for left and right gaze.

A disconnection account of Gerstmann syndrome: functional neuroanatomy evidence.

OBJECTIVE: To examine the functional neuroanatomy that could account for pure Gerstmann syndrome, which is the selective association of acalculia, finger agnosia, left-right disorientation, and agraphia. METHODS: We used structural and functional neuroimaging at high spatial resolution in healthy subjects to seek a shared cortical substrate of the Grundstörung posited by Gerstmann, ie, a common functional denominator accounting for this clinical tetrad. We construed a functional activation paradigm that mirrors each of the four clinical deficits in Gerstmann syndrome and determined cortical activation patterns. We then applied fiber tracking to diffusion tensor images and used cortical activation foci in the four functional domains as seed regions. RESULTS: None of the subjects showed parietal overlap of cortical activation patterns from the four cognitive domains. In every subject, however, the parietal activation patterns across all four domains consistently connected to a small region of subcortical parietal white matter at a location that is congruent with the lesion in a well-documented case of pure Gerstmann syndrome. INTERPRETATION: Our functional neuroimaging findings are not in agreement with Gerstmann's postulate of damage to a common cognitive function underpinning clinical semiology. Our evidence from intact functional neuroanatomy suggests that pure forms of Gerstmann's tetrad do not arise from lesion to a shared cortical substrate but from intraparietal disconnection after damage to a focal region of subcortical white matter.

Activity in face-responsive brain regions is modulated by invisible, attended faces: evidence from masked priming.

It is often assumed that neural activity in face-responsive regions of primate cortex correlates with conscious perception of faces. However, whether such activity occurs without awareness is still debated. Using functional magnetic resonance imaging (fMRI) in conjunction with a novel masked face priming paradigm, we observed neural modulations that could not be attributed to perceptual awareness. More specifically, we found reduced activity in several classic face-processing regions, including the "fusiform face area," "occipital face area," and superior temporal sulcus, when a face was preceded by a briefly flashed image of the same face, relative to a different face, even when 2 images of the same face differed. Importantly, unlike most previous studies, which have minimized awareness by using conditions of inattention, the present results occurred when the stimuli (the primes) were attended. By contrast, when primes were perceived consciously, in a long-lag priming paradigm, we found repetition-related activity increases in additional frontal and parietal regions. These data not only demonstrate that fMRI activity in face-responsive regions can be modulated independently of perceptual awareness, but also document where such subliminal face-processing occurs (i.e., restricted to face-responsive regions of occipital and temporal cortex) and to what extent (i.e., independent of the specific image).

Individual Brain Charting dataset extension, second release of high-resolution fMRI data for cognitive mapping.

We present an extension of the Individual Brain Charting dataset -a high spatial-resolution, multi-task, functional Magnetic Resonance Imaging dataset, intended to support the investigation on the functional principles governing cognition in the human brain. The concomitant data acquisition from the same 12 participants, in the same environment, allows to obtain in the long run finer cognitive topographies, free from inter-subject and inter-site variability. This second release provides more data from psychological domains present in the first release, and also yields data featuring new ones. It includes tasks on e.g. mental time travel, reward, theory-of-mind, pain, numerosity, self-reference effect and speech recognition. In total, 13 tasks with 86 contrasts were added to the dataset and 63 new components were included in the cognitive description of the ensuing contrasts. As the dataset becomes larger, the collection of the corresponding topographies becomes more comprehensive, leading to better brain-atlasing frameworks. This dataset is an open-access facility; raw data and derivatives are publicly available in neuroimaging repositories.

Discriminability of numerosity-evoked fMRI activity patterns in human intra-parietal cortex reflects behavioral numerical acuity.

Areas of the primate intraparietal cortex have been identified as an important substrate of numerical cognition. In human fMRI studies, activity patterns in these and other areas have allowed researchers to read out the numerosity a subject is viewing, but the relation of such decodable information with behavioral numerical proficiency remains unknown. Here, we estimated the precision of behavioral numerosity discrimination (internal Weber fraction) in twelve adult subjects based on psychophysical testing in a delayed numerosity comparison task outside the scanner. FMRI data were then recorded during a similar task, to obtain the accuracy with which the same sample numerosities could be read out from evoked brain activity patterns, as a measure of the precision of the neuronal representation. Sample numerosities were decodable in both early visual and intra-parietal cortex with approximately equal accuracy on average. In parietal cortex, smaller numerosities were better discriminated than larger numerosities of the same ratio, paralleling smaller behavioral Weber fractions for smaller numerosities. Furthermore, in parietal but not early visual cortex, fMRI decoding performance was correlated with behavioral number discrimination acuity across subjects (subjects with a more precise behavioral Weber fraction measured prior to scanning showed greater discriminability of fMRI activity patterns in intraparietal cortex, and more specifically, the right LIP region). These results suggest a crucial role for intra-parietal cortex in supporting a numerical representation which is explicitly read out for numerical decisions and behavior.

Attentional amplification of neural codes for number independent of other quantities along the dorsal visual stream.

Humans and other animals base important decisions on estimates of number, and intraparietal cortex is thought to provide a crucial substrate of this ability. However, it remains debated whether an independent neuronal processing mechanism underlies this 'number sense', or whether number is instead judged indirectly on the basis of other quantitative features. We performed high-resolution 7 Tesla fMRI while adult human volunteers attended either to the numerosity or an orthogonal dimension (average item size) of visual dot arrays. Along the dorsal visual stream, numerosity explained a significant amount of variance in activation patterns, above and beyond non-numerical dimensions. Its representation was selectively amplified and progressively enhanced across the hierarchy when task relevant. Our results reveal a sensory extraction mechanism yielding information on numerosity separable from other dimensions already at early visual stages and suggest that later regions along the dorsal stream are most important for explicit manipulation of numerical quantity.