A cortical surface template for human neuroscience.

Neuroimaging data analysis relies on normalization to standard anatomical templates to resolve macroanatomical differences across brains. Existing human cortical surface templates sample locations unevenly because of distortions introduced by inflation of the folded cortex into a standard shape. Here we present the onavg template, which affords uniform sampling of the cortex. We created the onavg template based on openly available high-quality structural scans of 1,031 brains-25 times more than existing cortical templates. We optimized the vertex locations based on cortical anatomy, achieving an even distribution. We observed consistently higher multivariate pattern classification accuracies and representational geometry inter-participant correlations based on onavg than on other templates, and onavg only needs three-quarters as much data to achieve the same performance compared with other templates. The optimized sampling also reduces CPU time across algorithms by 1.3-22.4% due to less variation in the number of vertices in each searchlight.

Modeling naturalistic face processing in humans with deep convolutional neural networks.

Deep convolutional neural networks (DCNNs) trained for face identification can rival and even exceed human-level performance. The ways in which the internal face representations in DCNNs relate to human cognitive representations and brain activity are not well understood. Nearly all previous studies focused on static face image processing with rapid display times and ignored the processing of naturalistic, dynamic information. To address this gap, we developed the largest naturalistic dynamic face stimulus set in human neuroimaging research (700+ naturalistic video clips of unfamiliar faces). We used this naturalistic dataset to compare representational geometries estimated from DCNNs, behavioral responses, and brain responses. We found that DCNN representational geometries were consistent across architectures, cognitive representational geometries were consistent across raters in a behavioral arrangement task, and neural representational geometries in face areas were consistent across brains. Representational geometries in late, fully connected DCNN layers, which are optimized for individuation, were much more weakly correlated with cognitive and neural geometries than were geometries in late-intermediate layers. The late-intermediate face-DCNN layers successfully matched cognitive representational geometries, as measured with a behavioral arrangement task that primarily reflected categorical attributes, and correlated with neural representational geometries in known face-selective topographies. Our study suggests that current DCNNs successfully capture neural cognitive processes for categorical attributes of faces but less accurately capture individuation and dynamic features.

Developmental prosopagnosics have widespread selectivity reductions across category-selective visual cortex.

Developmental prosopagnosia (DP) is a neurodevelopmental disorder characterized by severe deficits with facial identity recognition. It is unclear which cortical areas contribute to face processing deficits in DP, and no previous studies have investigated whether other category-selective areas function normally in DP. To address these issues, we scanned 22 DPs and 27 controls using a dynamic localizer consisting of video clips of faces, scenes, bodies, objects, and scrambled objects. We then analyzed category selectivity, a measure of the tuning of a cortical area to a particular visual category. DPs exhibited reduced face selectivity in all 12 face areas, and the reductions were significant in three posterior and two anterior areas. DPs and controls showed similar responses to faces in other category-selective areas, which suggests the DPs' behavioral deficits with faces result from problems restricted to the face network. DPs also had pronounced scene-selectivity reductions in four of six scene-selective areas and marginal body-selectivity reductions in two of four body-selective areas. Our results demonstrate that DPs have widespread deficits throughout the face network, and they are inconsistent with a leading account of DP which proposes that posterior face-selective areas are normal in DP. The selectivity reductions in other category-selective areas indicate many DPs have deficits spread across high-level visual cortex.

Predicting individual face-selective topography using naturalistic stimuli.

Subject-specific, functionally defined areas are conventionally estimated with functional localizers and a simple contrast analysis between responses to different stimulus categories. Compared with functional localizers, naturalistic stimuli provide several advantages such as stronger and widespread brain activation, greater engagement, and increased subject compliance. In this study we demonstrate that a subject's idiosyncratic functional topography can be estimated with high fidelity from that subject's fMRI data obtained while watching a naturalistic movie using hyperalignment to project other subjects' localizer data into that subject's idiosyncratic cortical anatomy. These findings lay the foundation for developing an efficient tool for mapping functional topographies for a wide range of perceptual and cognitive functions in new subjects based only on fMRI data collected while watching an engaging, naturalistic stimulus and other subjects' localizer data from a normative sample.

Attentional modulation differentially affects ventral and dorsal face areas in both normal participants and developmental prosopagnosics.

Face-selective cortical areas that can be divided into a ventral stream and a dorsal stream. Previous findings indicate selective attention to particular aspects of faces have different effects on the two streams. To better understand the organization of the face network and whether deficits in attentional modulation contribute to developmental prosopagnosia (DP), we assessed the effect of selective attention to different face aspects across eight face-selective areas. Our results from normal participants found that ROIs in the ventral pathway (OFA, FFA) responded strongly when attention was directed to identity and expression, and ROIs in the dorsal pathway (pSTS-FA, IFG-FA) responded the most when attention was directed to facial expression. Response profiles generated by attention to different face aspects were comparable in DPs and normals. Our results demonstrate attentional modulation affects the ventral and dorsal steam face areas differently and indicate deficits in attentional modulation do not contribute to DP.

Eye movements and retinotopic tuning in developmental prosopagnosia.

Despite extensive investigation, the causes and nature of developmental prosopagnosia (DP)-a severe face identification impairment in the absence of acquired brain injury-remain poorly understood. Drawing on previous work showing that individuals identified as being neurotypical (NT) show robust individual differences in where they fixate on faces, and recognize faces best when the faces are presented at this location, we defined and tested four novel hypotheses for how atypical face-looking behavior and/or retinotopic face encoding could impair face recognition in DP: (a) fixating regions of poor information, (b) inconsistent saccadic targeting, (c) weak retinotopic tuning, and (d) fixating locations not matched to the individual's own face tuning. We found no support for the first three hypotheses, with NTs and DPs consistently fixating similar locations and showing similar retinotopic tuning of their face perception performance. However, in testing the fourth hypothesis, we found preliminary evidence for two distinct phenotypes of DP: (a) Subjects characterized by impaired face memory, typical face perception, and a preference to look high on the face, and (b) Subjects characterized by profound impairments to both face memory and perception and a preference to look very low on the face. Further, while all NTs and upper-looking DPs performed best when faces were presented near their preferred fixation location, this was not true for lower-looking DPs. These results suggest that face recognition deficits in a substantial proportion of people with DP may arise not from aberrant face gaze or compromised retinotopic tuning, but from the suboptimal matching of gaze to tuning.

Cross-movie prediction of individualized functional topography.

Participant-specific, functionally defined brain areas are usually mapped with functional localizers and estimated by making contrasts between responses to single categories of input. Naturalistic stimuli engage multiple brain systems in parallel, provide more ecologically plausible estimates of real-world statistics, and are friendly to special populations. The current study shows that cortical functional topographies in individual participants can be estimated with high fidelity from naturalistic stimuli. Importantly, we demonstrate that robust, individualized estimates can be obtained even when participants watched different movies, were scanned with different parameters/scanners, and were sampled from different institutes across the world. Our results create a foundation for future studies that allow researchers to estimate a broad range of functional topographies based on naturalistic movies and a normative database, making it possible to integrate high-level cognitive functions across datasets from laboratories worldwide.

Hominoid-specific sulcal variability is related to face perception ability.

The relationship among brain structure, brain function, and behavior is of major interest in neuroscience, evolutionary biology, and psychology. This relationship is especially intriguing when considering hominoid-specific brain structures because they cannot be studied in widely examined models in neuroscience such as mice, marmosets, and macaques. The fusiform gyrus (FG) is a hominoid-specific structure critical for face processing that is abnormal in individuals with developmental prosopagnosia (DPs)-individuals who have severe deficits recognizing the faces of familiar people in the absence of brain damage. While previous studies have found anatomical and functional differences in the FG between DPs and NTs, no study has examined the shallow tertiary sulcus (mid-fusiform sulcus, MFS) within the FG that is a microanatomical, macroanatomical, and functional landmark in humans, as well as was recently shown to be present in non-human hominoids. Here, we implemented pre-registered analyses of neuroanatomy and face perception in NTs and DPs. Results show that the MFS was shorter in DPs than NTs. Furthermore, individual differences in MFS length in the right, but not left, hemisphere predicted individual differences in face perception. These results support theories linking brain structure and function to perception, as well as indicate that individual differences in MFS length can predict individual differences in face processing. Finally, these findings add to growing evidence supporting a relationship between morphological variability of late developing, tertiary sulci and individual differences in cognition.

An fMRI dataset in response to "The Grand Budapest Hotel", a socially-rich, naturalistic movie.

Naturalistic stimuli evoke strong, consistent, and information-rich patterns of brain activity, and engage large extents of the human brain. They allow researchers to compare highly similar brain responses across subjects, and to study how complex representations are encoded in brain activity. Here, we describe and share a dataset where 25 subjects watched part of the feature film "The Grand Budapest Hotel" by Wes Anderson. The movie has a large cast with many famous actors. Throughout the story, the camera shots highlight faces and expressions, which are fundamental to understand the complex narrative of the movie. This movie was chosen to sample brain activity specifically related to social interactions and face processing. This dataset provides researchers with fMRI data that can be used to explore social cognitive processes and face processing, adding to the existing neuroimaging datasets that sample brain activity with naturalistic movies.

Normal composite face effects in developmental prosopagnosia.

Upright face perception is thought to involve holistic processing, whereby local features are integrated into a unified whole. Consistent with this view, the top half of one face appears to fuse perceptually with the bottom half of another, when aligned spatially and presented upright. This 'composite face effect' reveals a tendency to integrate information from disparate regions when faces are presented canonically. In recent years, the relationship between susceptibility to the composite effect and face recognition ability has received extensive attention both in participants with normal face recognition and participants with developmental prosopagnosia. Previous results suggest that individuals with developmental prosopagnosia may show reduced susceptibility to the effect suggestive of diminished holistic face processing. Here we describe two studies that examine whether developmental prosopagnosia is associated with reduced composite face effects. Despite using independent samples of developmental prosopagnosics and different composite procedures, we find no evidence for reduced composite face effects. The experiments yielded similar results; highly significant composite effects in both prosopagnosic groups that were similar in magnitude to the effects found in participants with normal face processing. The composite face effects exhibited by both samples and the controls were greatly diminished when stimulus arrangements were inverted. Our finding that the whole-face binding process indexed by the composite effect is intact in developmental prosopagnosia indicates that other factors are responsible for developmental prosopagnosia. These results are also inconsistent with suggestions that susceptibility to the composite face effect and face recognition ability are tightly linked. While the holistic process revealed by the composite face effect may be necessary for typical face perception, it is not sufficient; individual differences in face recognition ability likely reflect variability in multiple sequential processes.

Normal voice processing after posterior superior temporal sulcus lesion.

The right posterior superior temporal sulcus (pSTS) shows a strong response to voices, but the cognitive processes generating this response are unclear. One possibility is that this activity reflects basic voice processing. However, several fMRI and magnetoencephalography findings suggest instead that pSTS serves as an integrative hub that combines voice and face information. Here we investigate whether right pSTS contributes to basic voice processing by testing Faith, a patient whose right pSTS was resected, with eight behavioral tasks assessing voice identity perception and recognition, voice sex perception, and voice expression perception. Faith performed normally on all the tasks. Her normal performance indicates right pSTS is not necessary for intact voice recognition and suggests that pSTS activations to voices reflect higher-level processes.