Spatially Adjacent Regions in Posterior Cingulate Cortex Represent Familiar Faces at Different Levels of Complexity.

Extensive research has shown that perceptual information of faces is processed in a network of hierarchically-organized areas within ventral temporal cortex. For familiar and famous faces, perceptual processing of faces is normally accompanied by extraction of semantic knowledge about the social status of persons. Semantic processing of familiar faces could entail progressive stages of information abstraction. However, the cortical mechanisms supporting multistage processing of familiar faces have not been characterized. Here, using an event-related fMRI experiment, familiar faces from four celebrity groups (actors, singers, politicians, and football players) and unfamiliar faces were presented to the human subjects (both males and females) while they were engaged in a face categorization task. We systematically explored the cortical representations for faces, familiar faces, subcategories of familiar faces, and familiar face identities using whole-brain univariate analysis, searchlight-based multivariate pattern analysis (MVPA), and functional connectivity analysis. Convergent evidence from all these analyses revealed a set of overlapping regions within posterior cingulate cortex (PCC) that contained decodable fMRI responses for representing different levels of semantic knowledge about familiar faces. Our results suggest a multistage pathway in PCC for processing semantic information of faces, analogous to the multistage pathway in ventral temporal cortex for processing perceptual information of faces.SIGNIFICANCE STATEMENT Recognizing familiar faces is an important component of social communications. Previous research has shown that a distributed network of brain areas is involved in processing the semantic information of familiar faces. However, it is not clear how different levels of semantic information are represented in the brain. Here, we evaluated the multivariate response patterns across the entire cortex to discover the areas that contain information for familiar faces, subcategories of familiar faces, and identities of familiar faces. The searchlight maps revealed that different levels of semantic information are represented in topographically adjacent areas within posterior cingulate cortex (PCC). The results suggest that semantic processing of faces is mediated through progressive stages of information abstraction in PCC.

Task-dependent neural representations of visual object categories.

What do we perceive in a glance of an object? If we are questioned about it, will our perception be affected? How does the task demand influence visual processing in the brain and, consequently, our behaviour? To address these questions, we conducted an object categorisation experiment with three tasks, one at the superordinate level ('animate/inanimate') and two at the basic levels ('face/body' and 'animal/human face') along with a passive task in which participants were not required to categorise objects. To control bottom-up information and eliminate the effect of sensory-driven dissimilarity, we used a particular set of animal face images as the identical target stimuli across all tasks. We then investigated the impact of top-down task demands on behaviour and brain representations. Behavioural results demonstrated a superordinate advantage in the reaction time, while the accuracy was similar for all categorisation levels. The event-related potentials (ERPs) for all categorisation levels were highly similar except for about 170 ms and after 300 ms from stimulus onset. In these time windows, the animal/human face categorisation, which required fine-scale discrimination, elicited a differential ERP response. Similarly, decoding analysis over all electrodes showed the highest peak value of task decoding around 170 ms, followed by a few significant timepoints, generally after 300 ms. Moreover, brain responses revealed task-related neural modulation during categorisation tasks compared with the passive task. Overall, these findings demonstrate different task-related effects on the behavioural response and brain representations. The early and late components of neural modulation could be linked to perceptual and top-down processing of object categories, respectively.

Relationship between cerebrospinal fluid biomarkers and structural brain network properties in Parkinson's disease.

BACKGROUND: Pathological accumulation of α-synuclein, amyloid-ß42 , and tau proteins in the brain is considered critical for development of various neurodegenerative diseases. OBJECTIVES: We investigated the association between CSF levels of these biomarkers, brain structural connectivity, and the UPDRS in PD. METHODS: Diffusion tensor images and CSF biomarkers (α-synuclein, amyloid-ß42 , total tau, and phosphorylated tau181) from 132 drug-naïve, nondemented PD patients and 61 healthy controls were obtained from the Parkinson's Progression Markers Initiative database. After network reconstruction of structural connectivity patterns, global interconnectivity measures (including global efficiency, clustering coefficient, and characteristic path length) and local efficiency were calculated. Network properties and CSF biomarkers were compared between PD patients and healthy controls. The association of CSF biomarkers with network properties and UPDRS-III score was investigated. RESULTS: Global measures (but not local efficiency) and CSF α-synuclein were significantly lower in PD patients. Global efficiency and clustering coefficient correlated positively with α-synuclein, Aß42 , and total tau CSF levels. Furthermore, these CSF biomarkers showed no significant association with the UPDRS-III score. CONCLUSIONS: This study examined the association of CSF biomarkers that reflect the brain pathology, with structural brain connectivity and UPDRS-III in PD. Our results revealed an association between the abnormal aggregation of α-synuclein, Aß42 , and tau proteins and structural connectivity disruption in PD patients. In summary, a combination of structural imaging and measurement of CSF biomarkers provide a better understanding of the pathogenesis of PD. © 2018 International Parkinson and Movement Disorder Society.

Retinotopy versus face selectivity in macaque visual cortex.

Retinotopic organization is a ubiquitous property of lower-tier visual cortical areas in human and nonhuman primates. In macaque visual cortex, the retinotopic maps extend to higher-order areas in the ventral visual pathway, including area TEO in the inferior temporal (IT) cortex. Distinct regions within IT cortex are also selective to specific object categories such as faces. Here we tested the topographic relationship between retinotopic maps and face-selective patches in macaque visual cortex using high-resolution fMRI and retinotopic face stimuli. Distinct subregions within face-selective patches showed either (1) a coarse retinotopic map of eccentricity and polar angle, (2) a retinotopic bias to a specific location of visual field, or (3) nonretinotopic selectivity. In general, regions along the lateral convexity of IT cortex showed more overlap between retinotopic maps and face selectivity, compared with regions within the STS. Thus, face patches in macaques can be subdivided into smaller patches with distinguishable retinotopic properties.

The "parahippocampal place area" responds preferentially to high spatial frequencies in humans and monkeys.

Defining the exact mechanisms by which the brain processes visual objects and scenes remains an unresolved challenge. Valuable clues to this process have emerged from the demonstration that clusters of neurons ("modules") in inferior temporal cortex apparently respond selectively to specific categories of visual stimuli, such as places/scenes. However, the higher-order "category-selective" response could also reflect specific lower-level spatial factors. Here we tested this idea in multiple functional MRI experiments, in humans and macaque monkeys, by systematically manipulating the spatial content of geometrical shapes and natural images. These tests revealed that visual spatial discontinuities (as reflected by an increased response to high spatial frequencies) selectively activate a well-known place-selective region of visual cortex (the "parahippocampal place area") in humans. In macaques, we demonstrate a homologous cortical area, and show that it also responds selectively to higher spatial frequencies. The parahippocampal place area may use such information for detecting object borders and scene details during spatial perception and navigation.

Larger left hippocampal presubiculum is associated with lower risk of antisocial behavior in healthy adults with childhood conduct history.

Conduct Disorder (CD) is defined as aggressive, antisocial, and rule-breaking behavior during childhood. It is a major risk factor for developing antisocial personality disorder (ASPD) in adulthood. However, nearly half the CDs do not develop ASPD. Identification of reversion factors seems crucial for proper interventions. We identified 40 subjects with childhood history of CD (CC) and 1166 control subjects (HC) from Human Connectome Project. Their psychiatric, emotional, impulsivity, and personality traits were extracted. An emotion recognition task-fMRI analysis was done. We also did subregion analysis of hippocampus and amygdala in 35 CC and 69 demographically matched HCs. CC subjects scored significantly higher in antisocial-related evaluations. No differences in task-fMRI activation of amygdala and hippocampus were observed. CCs had larger subfields of the left hippocampus: presubiculum, CA3, CA4, and dentate gyrus. Further, an interaction model revealed a significant presubiculum volume × group association with antisocial, aggression, and agreeableness scores. Our study shows that healthy young adults with a prior history of CD still exhibit some forms of antisocial-like behavior with larger left hippocampal subfields, including presubiculum that also explains the variability in antisocial behavior. These larger left hippocampal subfield volumes may play a protective role against CD to ASPD conversion.

Scene-selective cortical regions in human and nonhuman primates.

fMRI studies have revealed three scene-selective regions in human visual cortex [the parahippocampal place area (PPA), transverse occipital sulcus (TOS), and retrosplenial cortex (RSC)], which have been linked to higher-order functions such as navigation, scene perception/recognition, and contextual association. Here, we document corresponding (presumptively homologous) scene-selective regions in the awake macaque monkey, based on direct comparison to human maps, using identical stimuli and largely overlapping fMRI procedures. In humans, our results showed that the three scene-selective regions are centered near-but distinct from-the gyri/sulci for which they were originally named. In addition, all these regions are located within or adjacent to known retinotopic areas. Human RSC and PPA are located adjacent to the peripheral representation of primary and secondary visual cortex, respectively. Human TOS is located immediately anterior/ventral to retinotopic area V3A, within retinotopic regions LO-1, V3B, and/or V7. Mirroring the arrangement of human regions fusiform face area (FFA) and PPA (which are adjacent to each other in cortex), the presumptive monkey homolog of human PPA is located adjacent to the monkey homolog of human FFA, near the posterior superior temporal sulcus. Monkey TOS includes the region predicted from the human maps (macaque V4d), extending into retinotopically defined V3A. A possible monkey homolog of human RSC lies in the medial bank, near peripheral V1. Overall, our findings suggest a homologous neural architecture for scene-selective regions in visual cortex of humans and nonhuman primates, analogous to the face-selective regions demonstrated earlier in these two species.

An anterior temporal face patch in human cortex, predicted by macaque maps.

Increasing evidence suggests that primate visual cortex has a specialized architecture for processing discrete object categories such as faces. Human fMRI studies have described a localized region in the fusiform gyrus [the fusiform face area (FFA)] that responds selectively to faces. In contrast, in nonhuman primates, electrophysiological and fMRI studies have instead revealed 2 apparently analogous regions of face representation: the posterior temporal face patch (PTFP) and the anterior temporal face patch (ATFP). An earlier study suggested that human FFA is homologous to the PTFP in macaque. However, in humans, no obvious homologue of the macaque ATFP has been demonstrated. Here, we used fMRI to map face-selective sites in both humans and macaques, based on equivalent stimuli in a quantitative topographic comparison. This fMRI evidence suggests that such a face-selective area exists in human anterior inferotemporal cortex, comprising the apparent homologue of the fMRI-defined ATFP in macaques.

Complementary hemispheric lateralization of language and social processing in the human brain.

Humans have a unique ability to use language for social communication. The neural architecture for language comprehension and production may have prominently emerged in the brain areas that were originally involved in social cognition. Here, we directly tested the fundamental link between language and social processing using functional magnetic resonance data (MRI) data from over 1,000 human subjects. Cortical activations in language and social tasks showed a striking similarity with a complementary hemispheric lateralization. Within core language areas, left-lateralized activations in the language task were mirrored by right-lateralized activations in the social task. Outside these areas, the activations were left lateralized in both tasks, perhaps indicating multimodal integration of social and semantic information. Our findings could have important implications in understanding neurocognitive mechanisms of social disorders such as autism.

fMRI mapping of a morphed continuum of 3D shapes within inferior temporal cortex.

Here, we mapped fMRI responses to incrementally changing shapes along a continuous 3D morph, ranging from a head ("face") to a house ("place"). The response to each shape was mapped independently by using single-stimulus imaging, and stimulus shapes were equated for lower-level visual cues. We measured activity in 2-mm samples across human inferior temporal cortex from the fusiform face area (FFA) (apparently selective for faces) to the parahippocampal place area (PPA) (apparently selective for places), testing for (i) incremental changes in the topography of FFA and PPA (predicted by the continuous-mapping model) or (ii) little or no response to the intermediate morphed shapes (predicted by the category model). Neither result occurred; instead, we found approximately linearly graded changes in the response amplitudes to graded-shape changes, without changes in topography-similar to visual responses in different lower-tier cortical areas.

The radial bias: a different slant on visual orientation sensitivity in human and nonhuman primates.

It is generally assumed that sensitivity to different stimulus orientations is mapped in a globally equivalent fashion across primate visual cortex, at a spatial scale larger than that of orientation columns. However, some evidence predicts instead that radial orientations should produce higher activity than other orientations, throughout visual cortex. Here, this radial orientation bias was robustly confirmed using (1) human psychophysics, plus fMRI in (2) humans and (3) behaving monkeys. In visual cortex, fMRI activity was at least 20% higher in the retinotopic representations of polar angle which corresponded to the radial stimulus orientations (relative to tangential). In a global demonstration of this, we activated complementary retinotopic quadrants of visual cortex by simply changing stimulus orientation, without changing stimulus location in the visual field. This evidence reveals a neural link between orientation sensitivity and the cortical retinotopy, which have previously been considered independent.

Does retinotopy influence cortical folding in primate visual cortex?

In humans and other Old World primates, much of visual cortex comprises a set of retinotopic maps, embedded in a cortical sheet with well known, identifiable folding patterns. However, the relationship between these two prominent cortical variables has not been comprehensively studied. Here, we quantitatively tested this relationship using functional and structural magnetic resonance imaging in monkeys and humans. We found that the vertical meridian of the visual field tends to be represented on gyri (convex folds), whereas the horizontal meridian is preferentially represented in sulci (concave folds), throughout visual cortex in both primate species. This relationship suggests that the retinotopic maps may constrain the pattern of cortical folding during development.

Genetic influence is linked to cortical morphology in category-selective areas of visual cortex.

Human visual cortex contains discrete areas that respond selectively to specific object categories such as faces, bodies, and places. A long-standing question is whether these areas are shaped by genetic or environmental factors. To address this question, here we analyzed functional MRI data from an unprecedented number (n = 424) of monozygotic (MZ) and dizygotic (DZ) twins. Category-selective maps were more identical in MZ than DZ twins. Within each category-selective area, distinct subregions showed significant genetic influence. Structural MRI analysis revealed that the 'genetic voxels' were predominantly located in regions with higher cortical curvature (gyral crowns in face areas and sulcal fundi in place areas). Moreover, we found that cortex was thicker and more myelinated in genetic voxels of face areas, while it was thinner and less myelinated in genetic voxels of place areas. This double dissociation suggests a differential development of face and place areas in cerebral cortex.

Predicting Blood Oxygenation Level-Dependent Activity in Fusiform Face Area from the Activity in Other Visual Areas.

Neuroimaging studies have shown that discrete regions in ventral visual pathway respond selectively to specific object categories. For example, the fusiform face area (FFA) in humans is consistently more responsive to face than nonface images. However, it is not clear how other cortical regions contribute to this preferential response in FFA. To address this question, we performed a functional magnetic resonance imaging study on human subjects watching naturalistic movie clips from human actions. We then used correlation and multivariate regression (partial least-squares regression) analyses to estimate/predict the mean BOLD (blood oxygenation level-dependent) activity in FFA, from the mean and pattern of responses in 24 visual cortical areas. Higher tier retinotopic areas V3, hV4, and LO2, motion-selective area middle temporal, body-selective areas, and non-FFA face-selective areas had the best prediction accuracy particularly when they were located ipsilateral to FFA. All non-FFA collectively could explain up to 75% of variance in the FFA response. The regression models were also designed to predict the mean activity in one face area from the pattern of activity in another face area. The prediction power was significantly higher between the occipital face area and FFA. The multivariate regression analysis provides a new framework for investigating functional connectivity between cortical areas, and it could inform hierarchical models of visual cortex.

Unconscious orientation processing.

Recent findings have shown that certain attributes of visual stimuli, like orientation, are registered in cortical areas when the stimulus is unresolvable or perceptually invisible; however, there is no evidence to show that complex forms of orientation processing (e.g., modulatory effects of orientation on the processing of other features) could occur in the absence of awareness. To address these questions, different psychophysical paradigms were designed in six experiments to probe unconscious orientation processing. First we demonstrated orientation-selective adaptation and color-contingent orientation adaptation for peripheral unresolvable Gabor patches. The next experiments showed the modulatory effects of perceptually indiscriminable orientations on apparent motion processing and attentional mechanisms. Finally we investigated disappearance patterns of unresolvable Gabor stimuli during motion-induced blindness (MIB). Abrupt changes in local unresolvable orientations truncated MIB; however, orientation-based grouping failed to affect the MIB pattern when the orientations were unresolvable. Overall results revealed that unresolvable orientations substantially influence perception at multiple levels.

An Open Resource for Non-human Primate Imaging.

Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience. Unfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers that have the necessary facilities and capabilities. The PRIMatE Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design, and procedures for the PRIME-DE consortium, as well as the initial release, consisting of 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.

Subliminal attentional modulation in crowding condition.

In the crowding phenomenon, recognition of a visual target is impaired by other similar visual stimuli (distracters) presented near the target. This effect may be due largely to insufficient resolution of spatial attention. We showed that attention could subliminally enhance orientation selective adaptation to illusory lines in the crowding condition where target-distractor separation is beyond the limit of spatial resolution of attention. Despite the traditionally held close link between attention and awareness, here we provided evidence for subliminal attentional modulation for orientation stimuli that could not have been consciously perceived.

Static motion aftereffect does not modulate positional representations in early visual areas.

A stationary stimulus is perceived to drift in the opposite direction after adaptation to a moving stimulus (static motion aftereffect (MAE)). It is commonly assumed that positional effects from the static motion aftereffect are mediated by early visual areas. Here we psychophysically showed that these positional effects did not modulate illusory line-tilt aftereffect (TAE). Since illusory contours seem to be represented at relatively early stages of visual hierarchy, we suggest that the neural substrates underlying the perception of static motion aftereffect and illusory contours are different.

Adaptation to apparent motion in crowding condition.

Visual adaptation has been successfully used for studying the neural activity of different cortical areas in response to visual stimuli when observers do not have explicit conscious access to those stimuli. We compared the orientation selective adaptation to apparent motion and its effect on the perception of stimuli with bistable apparent motion in crowded and non-crowded conditions. In the crowding paradigm conscious access to a visual stimulus is severely impaired when it is flanked by other similar stimuli in the peripheral visual field. As expected, adaptation to the target stimulus occurred in the non-crowded condition in all of the individual subjects (n=4; P<0.001). Although in the crowded condition subjects were not able to discriminate the target stimulus, adaptation to that stimulus was still preserved (P<0.001). There was no significant difference between the adaptations in the two conditions of the apparent motion (P>0.05). Imaging studies have shown that V5 cortex is the earliest visual area that specifically responds to apparent motion. Our results suggest that in certain conditions V5 may be activated while there is no explicit conscious access to the apparent motion.

Attentional modulation of adaptation to illusory lines.

Selective visual attention modulates neuronal activation in various cortical areas. This type of neuronal modulation could happen even in the early stages of visual processing where specific attributes of visual stimuli are processed. It has been shown that different forms of visual aftereffects, such as tilt aftereffect, motion aftereffect, and figural aftereffect, are modulated by attention. In this study, we investigated the effect of visual attention on adaptation to illusory lines. In the first experiment, orientation selective adaptation to a peripheral illusory line was measured in three conditions: (1) poor attention condition in which subjects performed a dual task (even-odd judgment) at the fixation point during the adaptation period, (2) partial attention condition in which subjects only observed successively presented digits at the fixation point and did not perform the task during the adaptation period, and (3) full attention condition in which no visual stimuli were presented at the fixation point. Results showed that the magnitude of adaptation systematically decreased as the attentional load at the fixation point increased. In the second experiment, two transparent illusory contours were presented during the adaptation period, and tilt aftereffects to attended and non-attended illusory lines were compared. The magnitude of tilt aftereffect to the attended illusory line was significantly greater than that to the non-attended illusory line even when non-attended illusory contour was more visually salient. Because visual areas V2 and V1 are the first stage in the processing of illusory contours, we could conclude that visual attention has modulatory effects on the activation of neurons in these areas.