Jesse Gomez

Functionally Defined White Matter Reveals Segregated Pathways in Human Ventral Temporal Cortex Associated with Category-Specific Processing

It is unknown if the white-matter properties associated with specific visual networks selectively affect category-specific processing. In a novel protocol we combined measurements of white-matter structure, functional selectivity, and behavior in the same subjects. We find two parallel white-matter pathways along the ventral temporal lobe connecting to either face-selective or place-selective regions. Diffusion properties of portions of these tracts adjacent to face- and place-selective regions of ventral temporal cortex correlate with behavioral performance for face or place processing, respectively. Strikingly, adults with developmental prosopagnosia (face blindness) express an atypical structure-behavior relationship near face-selective cortex, suggesting that white-matter atypicalities in this region may have behavioral consequences. These data suggest that examining the interplay between cortical function, anatomical connectivity, and visual behavior is integral to understanding functional networks and their role in producing visual abilities and deficits.

Microstructural proliferation in human cortex is coupled with the development of face processing

Brain structure and function mature together Our ability to recognize faces improves from infancy to adulthood. This improvement depends on specific face-selective regions in the visual system. Gomez et al. tested face memory and place recognition in children and adults while scanning relevant brain regions. Anatomical changes co-occurred with functional changes in the brain. Some regions in the high-level visual cortex showed profound developmental maturation, whereas others were stable. Thus, improvements in face recognition involve an interplay between structural and functional changes in the brain. Science, this issue p. 68 Developmental improvements in face recognition occur together with tissue proliferation in face-selective brain regions. How does cortical tissue change as brain function and behavior improve from childhood to adulthood? By combining quantitative and functional magnetic resonance imaging in children and adults, we find differential development of high-level visual areas that are involved in face and place recognition. Development of face-selective regions, but not place-selective regions, is dominated by microstructural proliferation. This tissue development is correlated with specific increases in functional selectivity to faces, as well as improvements in face recognition, and ultimately leads to differentiated tissue properties between face- and place-selective regions in adulthood, which we validate with postmortem cytoarchitectonic measurements. These data suggest a new model by which emergent brain function and behavior result from cortical tissue proliferation rather than from pruning exclusively.

The Functional Neuroanatomy of Human Face Perception

Face perception is critical for normal social functioning and is mediated by a network of regions in the ventral visual stream. In this review, we describe recent neuroimaging findings regarding the macro- and microscopic anatomical features of the ventral face network, the characteristics of white matter connections, and basic computations performed by population receptive fields within face-selective regions composing this network. We emphasize the importance of the neural tissue properties and white matter connections of each region, as these anatomical properties may be tightly linked to the functional characteristics of the ventral face network. We end by considering how empirical investigations of the neural architecture of the face network may inform the development of computational models and shed light on how computations in the face network enable efficient face perception.

The Face-Processing Network Is Resilient to Focal Resection of Human Visual Cortex.

Human face perception requires a network of brain regions distributed throughout the occipital and temporal lobes with a right hemisphere advantage. Present theories consider this network as either a processing hierarchy beginning with the inferior occipital gyrus (occipital face area; IOG-faces/OFA) or a multiple-route network with nonhierarchical components. The former predicts that removing IOG-faces/OFA will detrimentally affect downstream stages, whereas the latter does not. We tested this prediction in a human patient (Patient S.P.) requiring removal of the right inferior occipital cortex, including IOG-faces/OFA. We acquired multiple fMRI measurements in Patient S.P. before and after a preplanned surgery and multiple measurements in typical controls, enabling both within-subject/across-session comparisons (Patient S.P. before resection vs Patient S.P. after resection) and between-subject/across-session comparisons (Patient S.P. vs controls). We found that the spatial topology and selectivity of downstream ipsilateral face-selective regions were stable 1 and 8 month(s) after surgery. Additionally, the reliability of distributed patterns of face selectivity in Patient S.P. before versus after resection was not different from across-session reliability in controls. Nevertheless, postoperatively, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1 of the resected hemisphere. Diffusion weighted imaging in Patient S.P. and controls identifies white matter tracts connecting retinotopic areas to downstream face-selective regions, which may contribute to the stable and plastic features of the face network in Patient S.P. after surgery. Together, our results support a multiple-route network of face processing with nonhierarchical components and shed light on stable and plastic features of high-level visual cortex following focal brain damage. SIGNIFICANCE STATEMENT Brain networks consist of interconnected functional regions commonly organized in processing hierarchies. Prevailing theories predict that damage to the input of the hierarchy will detrimentally affect later stages. We tested this prediction with multiple brain measurements in a rare human patient requiring surgical removal of the putative input to a network processing faces. Surprisingly, the spatial topology and selectivity of downstream face-selective regions are stable after surgery. Nevertheless, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1. White matter connections from outside the face network may support these stable and plastic features. As processing hierarchies are ubiquitous in biological and nonbiological systems, our results have pervasive implications for understanding the construction of resilient networks.

Defining the most probable location of the parahippocampal place area using cortex-based alignment and cross-validation.

ABSTRACT The parahippocampal place area (PPA) is a widely studied high‐level visual region in the human brain involved in place and scene processing. The goal of the present study was to identify the most probable location of place‐selective voxels in medial ventral temporal cortex. To achieve this goal, we first used cortex‐based alignment (CBA) to create a probabilistic place‐selective region of interest (ROI) from one group of 12 participants. We then tested how well this ROI could predict place selectivity in each hemisphere within a new group of 12 participants. Our results reveal that a probabilistic ROI (pROI) generated from one group of 12 participants accurately predicts the location and functional selectivity in individual brains from a new group of 12 participants, despite between subject variability in the exact location of place‐selective voxels relative to the folding of parahippocampal cortex. Additionally, the prediction accuracy of our pROI is significantly higher than that achieved by volume‐based Talairach alignment. Comparing the location of the pROI of the PPA relative to published data from over 500 participants, including data from the Human Connectome Project, shows a striking convergence of the predicted location of the PPA and the cortical location of voxels exhibiting the highest place selectivity across studies using various methods and stimuli. Specifically, the most predictive anatomical location of voxels exhibiting the highest place selectivity in medial ventral temporal cortex is the junction of the collateral and anterior lingual sulci. Methodologically, we make this pROI freely available (vpnl.stanford.edu/PlaceSelectivity), which provides a means to accurately identify a functional region from anatomical MRI data when fMRI data are not available (for example, in patient populations). Theoretically, we consider different anatomical and functional factors that may contribute to the consistent anatomical location of place selectivity relative to the folding of high‐level visual cortex. HIGHLIGHTSA probabilistic place ROI was created from cortex‐based alignment in 24 participantsCross‐validation shows that this ROI predicts place selectivity in new participantsThis ROI predicts voxels with peak place selectivity in >500 participantsThe collateral/lingual sulcal junction is most predictive of place selectivityWe share this predictive ROI with the field (vpnl.stanford.edu/PlaceSelectivity)

The functional neuroanatomy of face perception: from brain measurements to deep neural networks

A central goal in neuroscience is to understand how processing within the ventral visual stream enables rapid and robust perception and recognition. Recent neuroscientific discoveries have significantly advanced understanding of the function, structure and computations along the ventral visual stream that serve as the infrastructure supporting this behaviour. In parallel, significant advances in computational models, such as hierarchical deep neural networks (DNNs), have brought machine performance to a level that is commensurate with human performance. Here, we propose a new framework using the ventral face network as a model system to illustrate how increasing the neural accuracy of present DNNs may allow researchers to test the computational benefits of the functional architecture of the human brain. Thus, the review (i) considers specific neural implementational features of the ventral face network, (ii) describes similarities and differences between the functional architecture of the brain and DNNs, and (iii) provides a hypothesis for the computational value of implementational features within the brain that may improve DNN performance. Importantly, this new framework promotes the incorporation of neuroscientific findings into DNNs in order to test the computational benefits of fundamental organizational features of the visual system.

Development differentially sculpts receptive fields across human visual cortex

Receptive fields (RFs) processing information in restricted parts of the visual field are a key property of neurons in the visual system. However, how RFs develop in humans is unknown. Using fMRI and population receptive field (pRF) modeling in children and adults, we determined where and how pRFs develop across the ventral visual stream. We find that pRF properties in visual field maps, V1 through VO1, are adult-like by age 5. However, pRF properties in face- and word-selective regions develop into adulthood, increasing the foveal representation and the visual field coverage for faces in the right hemisphere and words in the left hemisphere. Eye-tracking indicates that pRF changes are related to changing fixation patterns on words and faces across development. These findings suggest a link between viewing behavior of faces and words and the differential development of pRFs across visual cortex, potentially due to competition on foveal coverage.

Novel childhood experience suggests eccentricity drives organization of human visual cortex

The functional organization of human high-level visual cortex, such as face and place-selective regions, is strikingly consistent across individuals. A fundamental, unanswered question in neuroscience is what dimensions of visual information constrain the development and topography of this shared brain organization? To answer this question, we scanned with fMRI a unique group of adults who, as children, engaged in extensive experience with a novel stimulus— Pokémon —that varied along critical dimensions (foveal bias, rectilinearity, size, animacy) from other ecological categories such as faces and places. We find that experienced adults not only demonstrate distinct and consistent distributed cortical responses to Pokémon, but their activations suggest that it is the experienced retinal eccentricity during childhood that predicts the locus of distributed responses to Pokémon in adulthood. These data advance our understanding about how childhood experience and functional constraints shape the functional organization of the human brain.

Apparent thinning of visual cortex during childhood is associated with myelination, not pruning

Microstructural mechanisms underlying apparent cortical thinning during childhood development are unknown. Using functional, quantitative, and diffusion magnetic resonance imaging in children and adults, we tested if tissue growth (lower T1 relaxation time and mean diffusivity (MD)) or pruning (higher T1 and MD) underlies cortical thinning in ventral temporal cortex (VTC). After age 5, T1 and MD decreased in mid and deep cortex of functionally-defined regions in lateral VTC, and in their adjacent white matter. T1 and MD decreases were (i) consistent with tissue growth related to myelin proliferation, which we verified with adult postmortem histology and (ii) correlated with apparent cortical thinning. Thus, contrary to prevailing theories, cortical tissue does not thin during childhood, it becomes more myelinated, shifting the gray-white matter boundary deeper into cortex. As tissue growth is prominent in regions with protracted functional development, our data suggest an intriguing hypothesis that functional development and myelination are interlinked.

Learning to Read Increases the Informativeness of Distributed Ventral Temporal Responses

Becoming a proficient reader requires substantial learning over many years. However, it is unknown how learning to read affects development of distributed visual representations across human ventral temporal cortex (VTC). Using fMRI and a data-driven, computational approach, we quantified the development of distributed VTC responses to characters (pseudowords and numbers) versus other domains in children, preteens, and adults. Results reveal anatomical- and hemisphere-specific development. With development, distributed responses to words and characters became more distinctive and informative in lateral but not medial VTC, and in the left but not right hemisphere. While the development of voxels with both positive and negative preference to words affected distributed information, only development of voxels with positive preference to words (i.e., word-selective) was correlated with reading ability. These data show that developmental increases in informativeness of distributed left lateral VTC responses are related to proficient reading and have important implications for both developmental theories and for elucidating neural mechanisms of reading disabilities.