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Face-processing occurs across ventral and lateral visual streams, which are involved in static and dynamic face perception, respectively. However, the nature of spatial computations across streams is unknown. Using functional MRI and population receptive field (pRF) mapping, we measured pRFs in face-selective regions. Results reveal that spatial computations by pRFs in ventral face-selective regions are concentrated around the center of gaze (fovea), but spatial computations in lateral face-selective regions extend peripherally. Diffusion MRI reveals that these differences are mirrored by a preponderance of white matter connections between ventral face-selective regions and foveal early visual cortex (EVC), while connections with lateral regions are distributed more uniformly across EVC eccentricities. These findings suggest a rethinking of spatial computations in face-selective regions, showing that they vary across ventral and lateral streams, and further propose that spatial computations in high-level regions are scaffolded by the fine-grain pattern of white matter connections from EVC., Humans process faces using face-selective regions in the ventral and lateral streams which perform different tasks. Here, the authors show via functional and diffusion MRI that the spatial computations in face-selective regions vary across streams, constrained by connections from early visual areas.

The detection and segmentation of meaningful figures from their background is a core function of vision. While work in non-human primates has implicated early visual mechanisms in this figure-ground modulation, neuroimaging in humans has instead largely ascribed the processing of figures and objects to higher stages of the visual hierarchy. Here, we used high-field fMRI at 7Tesla to measure BOLD responses to task-irrelevant orientation-defined figures in human early visual cortex, and employed a novel population receptive field (pRF) mapping-based approach to resolve the spatial profiles of two constituent mechanisms of figure-ground modulation: a local boundary response, and a further enhancement spanning the full extent of the figure region that is driven by global differences in features. Reconstructing the distinct spatial profiles of these effects reveals that figure enhancement modulates responses in human early visual cortex in a manner consistent with a mechanism of automatic, contextually-driven feedback from higher visual areas.Significance StatementA core function of the visual system is to parse complex 2D input into meaningful figures. We do so constantly and seamlessly, both by processing information about visible edges and by analyzing large-scale differences between figures and background. While influential neurophysiology work has characterized an intriguing mechanism that enhances V1 responses to perceptual figures, we have a poor understanding of how the early visual system contributes to figure-ground processing in humans. Here, we use advanced computational analysis methods and high-field human fMRI data to resolve the distinct spatial profiles of local edge and global figure enhancement in the early visual system (V1 and LGN); the latter is distinct and consistent a mechanism of automatic, stimulus-driven feedback from higher-level visual areas.

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., It is unknown whether spatial processing in the ventral (‘what’) stream contributes to high-level visual recognition. Here the authors show that spatial processing in face-selective regions directly contributes to whole face recognition behavior.

Spatial processing by receptive fields is a core property of the visual system. However, it is unknown how spatial coding 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. In face-selective regions, but not primary visual cortex, pRFs and overall visual field coverage were smaller and shifted downward in response to face inversion. From these measurements, we successfully predicted the relative behavioral detriment of face inversion at different positions in the visual field. This correspondence between neural measurements and behavior demonstrates how spatial integration in face-selective regions enables holistic processing. 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.

Face-processing occurs across ventral and lateral visual streams, which are involved in static and dynamic face perception, respectively. However, the nature of spatial computations across streams is unknown. Using functional MRI and novel population receptive field (pRF) mapping, we measured pRFs in face-selective regions. Results reveal that spatial computations by pRFs in ventral face-selective regions are concentrated around the center of gaze (fovea), but spatial computations in lateral face-selective regions extend peripherally. Diffusion MRI reveals that these differences are mirrored by a preponderance of white matter connections between ventral face-selective regions and foveal early visual cortex (EVC), while connections with lateral regions are distributed more uniformly across EVC eccentricities. These findings suggest a rethinking of spatial computations in face-selective regions, showing that they vary across ventral and lateral streams, and further propose that spatial computations in high-level regions are scaffolded by the fine-grain pattern of white matter connections from EVC.

Summary Nearly all of the information that reaches the primary visual cortex (V1) of the brain passes from the retina through the lateral geniculate nucleus (LGN) of the thalamus. Although the LGN's role in relaying feedforward signals from the retina to the cortex is well understood [ 1 , 2 ], the functional role of the extensive feedback it receives from the cortex has remained elusive [ 3 , 4 , 5 , 6 ]. Here, we investigated whether corticothalamic feedback may contribute to perceptual processing in the LGN in a manner that is distinct from top-down effects of attention [ 7 , 8 , 9 , 10 ]. We used high-resolution fMRI at 7 Tesla to simultaneously measure responses to orientation-defined figures in the human LGN and V1. We found robust enhancement of perceptual figures throughout the early visual system, which could be distinguished from the effects of covert spatial attention [ 11 , 12 , 13 ]. In a second experiment, we demonstrated that figure enhancement occurred in the LGN even when the figure and surrounding background were presented dichoptically (i.e., to different eyes). As binocular integration primarily occurs in V1 [ 14 , 15 ], these results implicate a mechanism of automatic, contextually sensitive feedback from binocular visual cortex underlying figure-ground modulation in the LGN. Our findings elucidate the functional mechanisms of this core function of the visual system [ 16 , 17 , 18 ], which allows people to segment and detect meaningful figures in complex visual environments. The involvement of the LGN in this rich, contextually informed visual processing—despite showing minimal feedforward selectivity for visual features [ 19 , 20 ]—underscores the role of recurrent processing at the earliest stages of visual processing.

Summary 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.

The visual system employs a sophisticated balance of attentional mechanisms: salient stimuli are prioritized for visual processing, yet observers can also ignore such stimuli when their goals require directing attention elsewhere. A powerful determinant of visual salience is local feature contrast: if a local region differs from its immediate surround along one or more feature dimensions, it will appear more salient. We used high-resolution functional MRI (fMRI) at 7T to characterize the modulatory effects of bottom-up salience and top-down voluntary attention within multiple sites along the early visual pathway, including visual areas V1–V4 and the lateral geniculate nucleus (LGN). Observers viewed arrays of spatially distributed gratings, where one of the gratings immediately to the left or right of fixation differed from all other items in orientation or motion direction, making it salient. To investigate the effects of directed attention, observers were cued to attend to the grating to the left or right of fixation, which was either salient or nonsalient. Results revealed reliable additive effects of top-down attention and stimulus-driven salience throughout visual areas V1–hV4. In comparison, the LGN exhibited significant attentional enhancement but was not reliably modulated by orientation- or motion-defined salience. Our findings indicate that top-down effects of spatial attention can influence visual processing at the earliest possible site along the visual pathway, including the LGN, whereas the processing of orientation- and motion-driven salience primarily involves feature-selective interactions that take place in early cortical visual areas. NEW & NOTEWORTHY While spatial attention allows for specific, goal-driven enhancement of stimuli, salient items outside of the current focus of attention must also be prioritized. We used 7T fMRI to compare salience and spatial attentional enhancement along the early visual hierarchy. We report additive effects of attention and bottom-up salience in early visual areas, suggesting that salience enhancement is not contingent on the observer’s attentional state.

Developmental prosopagnosia (DP) is characterized by deficits in face recognition without gross brain abnormalities. However, the neural basis of DP is not well understood. We measured population receptive fields (pRFs) in ventral visual cortex of DPs and typical adults to assess the contribution of spatial integration to face processing. While DPs showed typical retinotopic organization of ventral visual cortex and normal pRF sizes in early visual areas, we found significantly reduced pRF sizes in face-selective regions and in intermediate areas hV4 and VO1. Across both typicals and DPs, face recognition ability correlated positively with pRF size in both face-selective regions and VO1, whereby participants with larger pRFs perform better. However, face recognition ability is correlated with both pRF size and ROI volume only in face-selective regions. These findings suggest that smaller pRF sizes in DP may reflect a deficit in spatial integration affecting holistic processing required for face recognition.

Humans reliably recognize faces across a range of viewpoints, but the neural substrates supporting this ability remain unclear. Recent work suggests that neural selectivity to mirror-symmetric viewpoints of faces, found across a large network of visual areas, may constitute a key computational step in achieving full viewpoint invariance. In this study, we used repetitive transcranial magnetic stimulation (rTMS) to test the hypothesis that the occipital face area (OFA), putatively a key node in the face network, plays a causal role in face viewpoint symmetry perception. Each participant underwent both offline rTMS to the right OFA and sham stimulation, preceding blocks of behavioral trials. After each stimulation period, the participant performed one of two behavioral tasks involving presentation of faces in the peripheral visual field: (1) judging the viewpoint symmetry; or (2) judging the angular rotation. rTMS applied to the right OFA significantly impaired performance in both tasks when stimuli were presented in the contralateral, left visual field. Interestingly, however, rTMS had a differential effect on the two tasks performed ipsilaterally. Although viewpoint symmetry judgments were significantly disrupted, we observed no effect on the angle judgment task. This interaction, caused by ipsilateral rTMS, provides support for models emphasizing the role of interhemispheric crosstalk in the formation of viewpoint-invariant face perception.SIGNIFICANCE STATEMENTFaces are among the most salient objects we encounter during our everyday activities. Moreover, we are remarkably adept at identifying people at a glance, despite the diversity of viewpoints during our social encounters. Here, we investigate the cortical mechanisms underlying this ability by focusing on effects of viewpoint symmetry, i.e., the invariance of neural responses to mirror-symmetric facial viewpoints. We did this by temporarily disrupting neural processing in the occipital face area (OFA) using transcranial magnetic stimulation. Our results demonstrate that the OFA causally contributes to judgments facial viewpoints and suggest that effects of viewpoint symmetry, previously observed using fMRI, arise from an interhemispheric integration of visual information even when only one hemisphere receives direct visual stimulation.

Scenes and objects are effortlessly processed and integrated by the human visual system. Given the distinct neural and behavioral substrates of scene and object processing, it is likely that individuals sometimes preferentially rely on one process or the other when viewing canonical "scene" or "object" stimuli. This would allow the visual system to maximize the specific benefits of these 2 types of processing. It is less obvious which of these modes of perception would be invoked during naturalistic visual transition between a focused view of a single object and an expansive view of an entire scene, particularly at intermediate views that may not be assigned readily to either stimulus category. In the current study, we asked observers to report their online perception of such dynamic image sequences, which zoomed and panned between a canonical view of a single object and an entire scene. We found a large and consistent effect of prior perception, or hysteresis, on the classification of the sequence: observers classified the sequence as an object for several seconds longer if the trial started at the object view and zoomed out, whereas scenes were perceived for longer on trials beginning with a scene view. This hysteresis effect resisted several manipulations of the movie stimulus and of the task performed, but hinged on the perceptual history built by unidirectional progression through the image sequence. Multiple experiments confirmed that this hysteresis effect was not purely decisional and was more prominent for transitions between corresponding objects and scenes than between other high-level stimulus classes. This finding suggests that the competitive mechanisms underlying hysteresis may be especially prominent in the perception of objects and scenes. We propose that hysteresis aids in disambiguating perception during naturalistic visual transitions, which may facilitate a dynamic balance between scene and object processing to enhance processing efficiency.

Using dot displays, Halberda, Sires, and Feigenson (2006) showed that observers could simultaneously encode the numerosity of two spatially overlapping sets and the superset of all items at a glance. With the brief display and the masking used in Halberda et al., the task required observers to encode the colors of each set in order to select and enumerate all the dots in that set. As such, the observed capacity limit for set enumeration could reflect a limit in visual short-term memory (VSTM) capacity for the set color rather than a limit in set enumeration per se. Here, we largely replicated Halberda et al. and found successful enumeration of approximately two sets (the superset was not probed). We also found that only about two and a half colors could be remembered from the colored dot displays whether or not the enumeration task was performed concurrently with the color VSTM task. Because observers must remember the color of a set prior to enumerating it, the under three-item VSTM capacity for color necessarily dictates that set enumeration capacity in this paradigm could not exceed two sets. Thus, the ability to enumerate multiple spatially overlapping sets is likely limited by VSTM capacity to retain the discriminating feature of these sets. This relationship suggests that the capacity for set enumeration cannot be considered independently from the capacity for the set's defining features.