Kevin S. Weiner

Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study.

Single-cell studies in the macaque have reported selective neural responses evoked by visual presentations of faces and bodies. Consistent with these findings, functional magnetic resonance imaging studies in humans and monkeys indicate that regions in temporal cortex respond preferentially to faces and bodies. However, it is not clear how these areas correspond across the two species. Here, we directly compared category-selective areas in macaques and humans using virtually identical techniques. In the macaque, several face- and body part-selective areas were found located along the superior temporal sulcus (STS) and middle temporal gyrus (MTG). In the human, similar to previous studies, face-selective areas were found in ventral occipital and temporal cortex and an additional face-selective area was found in the anterior temporal cortex. Face-selective areas were also found in lateral temporal cortex, including the previously reported posterior STS area. Body part-selective areas were identified in the human fusiform gyrus and lateral occipitotemporal cortex. In a first experiment, both monkey and human subjects were presented with pictures of faces, body parts, foods, scenes, and man-made objects, to examine the response profiles of each category-selective area to the five stimulus types. In a second experiment, face processing was examined by presenting upright and inverted faces. By comparing the responses and spatial relationships of the areas, we propose potential correspondences across species. Adjacent and overlapping areas in the macaque anterior STS/MTG responded strongly to both faces and body parts, similar to areas in the human fusiform gyrus and posterior STS. Furthermore, face-selective areas on the ventral bank of the STS/MTG discriminated both upright and inverted faces from objects, similar to areas in the human ventral temporal cortex. Overall, our findings demonstrate commonalities and differences in the wide-scale brain organization between the two species and provide an initial step toward establishing functionally homologous category-selective areas.

The functional architecture of the ventral temporal cortex and its role in categorization

Visual categorization is thought to occur in the human ventral temporal cortex (VTC), but how this categorization is achieved is still largely unknown. In this Review, we consider the computations and representations that are necessary for categorization and examine how the microanatomical and macroanatomical layout of the VTC might optimize them to achieve rapid and flexible visual categorization. We propose that efficient categorization is achieved by organizing representations in a nested spatial hierarchy in the VTC. This spatial hierarchy serves as a neural infrastructure for the representational hierarchy of visual information in the VTC and thereby enables flexible access to category information at several levels of abstraction.

Sparsely-distributed organization of face and limb activations in human ventral temporal cortex

Functional magnetic resonance imaging (fMRI) has identified face- and body part-selective regions, as well as distributed activation patterns for object categories across human ventral temporal cortex (VTC), eliciting a debate regarding functional organization in VTC and neural coding of object categories. Using high-resolution fMRI, we illustrate that face- and limb-selective activations alternate in a series of largely nonoverlapping clusters in lateral VTC along the inferior occipital gyrus (IOG), fusiform gyrus (FG), and occipito-temporal sulcus (OTS). Both general linear model (GLM) and multivoxel pattern (MVP) analyses show that face- and limb-selective activations minimally overlap and that this organization is consistent across experiments and days. We provide a reliable method to separate two face-selective clusters on the middle and posterior FG (mFus and pFus), and another on the IOG using their spatial relation to limb-selective activations and retinotopic areas hV4, VO-1/2, and hMT+. Furthermore, these activations show a gradient of increasing face selectivity and decreasing limb selectivity from the IOG to the mFus. Finally, MVP analyses indicate that there is differential information for faces in lateral VTC (containing weakly- and highly-selective voxels) relative to non-selective voxels in medial VTC. These findings suggest a sparsely-distributed organization where sparseness refers to the presence of several face- and limb-selective clusters in VTC, and distributed refers to the presence of different amounts of information in highly-, weakly-, and non-selective voxels. Consequently, theories of object recognition should consider the functional and spatial constraints of neural coding across a series of minimally overlapping category-selective clusters that are themselves distributed.

Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception

Face-selective neural responses in the human fusiform gyrus have been widely examined. However, their causal role in human face perception is largely unknown. Here, we used a multimodal approach of electrocorticography (ECoG), high-resolution functional magnetic resonance imaging (fMRI), and electrical brain stimulation (EBS) to directly investigate the causal role of face-selective neural responses of the fusiform gyrus (FG) in face perception in a patient implanted with subdural electrodes in the right inferior temporal lobe. High-resolution fMRI identified two distinct FG face-selective regions [mFus-faces and pFus-faces (mid and posterior fusiform, respectively)]. ECoG revealed a striking anatomical and functional correspondence with fMRI data where a pair of face-selective electrodes, positioned 1 cm apart, overlapped mFus-faces and pFus-faces, respectively. Moreover, electrical charge delivered to this pair of electrodes induced a profound face-specific perceptual distortion during viewing of real faces. Specifically, the subject reported a “metamorphosed” appearance of faces of people in the room. Several controls illustrate the specificity of the effect to the perception of faces. EBS of mFus-faces and pFus-faces neither produced a significant deficit in naming pictures of famous faces on the computer, nor did it affect the appearance of nonface objects. Further, the appearance of faces remained unaffected during both sham stimulation and stimulation of a pair of nearby electrodes that were not face-selective. Overall, our findings reveal a striking convergence of fMRI, ECoG, and EBS, which together offer a rare causal link between functional subsets of the human FG network and face perception.

The mid-fusiform sulcus: A landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex

Human ventral temporal cortex (VTC) plays a pivotal role in high-level vision. An under-studied macroanatomical feature of VTC is the mid-fusiform sulcus (MFS), a shallow longitudinal sulcus separating the lateral and medial fusiform gyrus (FG). Here, we quantified the morphological features of the MFS in 69 subjects (ages 7-40), and investigated its relationship to both cytoarchitectonic and functional divisions of VTC with four main findings. First, despite being a minor sulcus, we found that the MFS is a stable macroanatomical structure present in all 138 hemispheres with morphological characteristics developed by age 7. Second, the MFS is the locus of a lateral-medial cytoarchitectonic transition within the posterior FG serving as the boundary between cytoarchitectonic regions FG1 and FG2. Third, the MFS predicts a lateral-medial functional transition in eccentricity bias representations in children, adolescents, and adults. Fourth, the anterior tip of the MFS predicts the location of a face-selective region, mFus-faces/FFA-2. These findings are the first to illustrate that a macroanatomical landmark identifies both cytoarchitectonic and functional divisions of high-level sensory cortex in humans and have important implications for understanding functional and structural organization in the human brain.

Not one extrastriate body area: Using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex

The prevailing view of human lateral occipitotemporal cortex (LOTC) organization suggests a single area selective for images of the human body (extrastriate body area, EBA) that highly overlaps with the human motion-selective complex (hMT+). Using functional magnetic resonance imaging with higher resolution (1.5mm voxels) than past studies (3-4mm voxels), we examined the fine-scale spatial organization of these activations relative to each other, as well as to visual field maps in LOTC. Rather than one contiguous EBA highly overlapping hMT+, results indicate three limb-selective activations organized in a crescent surrounding hMT+: (1) an activation posterior to hMT+ on the lateral occipital sulcus/middle occipital gyrus (LOS/MOG) overlapping the lower vertical meridian shared between visual field maps LO-2 and TO-1, (2) an activation anterior to hMT+ on the middle temporal gyrus (MTG) consistently overlapping the lower vertical meridian of TO-2 and extending outside presently defined visual field maps, and (3) an activation inferior to hMT+ on the inferotemporal gyrus (ITG) overlapping the parafoveal representation of the TO cluster. This crescent organization of limb-selective activations surrounding hMT+ is reproducible over a span of three years and is consistent across different image types used for localization. Further, these regions exhibit differential position properties: preference for contralateral image presentation decreases and preference for foveal presentation increases from the limb-selective LOS to the MTG. Finally, the relationship between limb-selective activations and visual field maps extends to the dorsal stream where a posterior IPS activation overlaps V7. Overall, our measurements demonstrate a series of LOTC limb-selective activations that 1) have separate anatomical and functional boundaries, 2) overlap distinct visual field maps, and 3) illustrate differential position properties. These findings indicate that category selectivity alone is an insufficient organization principle for defining brain areas. Instead, multiple properties are necessary in order to parcellate and understand the functional organization of high-level visual cortex.

Functional Heterogeneity in Posterior Parietal Cortex Across Attention and Episodic Memory Retrieval

While attention is critical for event memory, debate has arisen regarding the extent to which posterior parietal cortex (PPC) activation during episodic retrieval reflects engagement of PPC-mediated mechanisms of attention. Here, we directly examined the relationship between attention and memory, within and across subjects, using functional magnetic resonance imaging attention-mapping and episodic retrieval paradigms. During retrieval, 4 functionally dissociable PPC regions were identified. Specifically, 2 PPC regions positively tracked retrieval outcomes: lateral intraparietal sulcus (latIPS) indexed graded item memory strength, whereas angular gyrus (AnG) tracked recollection. By contrast, 2 other PPC regions demonstrated nonmonotonic relationships with retrieval: superior parietal lobule (SPL) tracked retrieval reaction time, consistent with a graded engagement of top-down attention, whereas temporoparietal junction displayed a complex pattern of below-baseline retrieval activity, perhaps reflecting disengagement of bottom-up attention. Analyses of retrieval effects in PPC topographic spatial attention maps (IPS0-IPS5; SPL1) revealed that IPS5 and SPL1 exhibited a nonmonotonic relationship with retrieval outcomes resembling that in the SPL region, further suggesting that SPL activation during retrieval reflects top-down attention. While demands on PPC attention mechanisms vary during retrieval attempts, the present functional parcellation of PPC indicates that 2 additional mechanisms (mediated by latIPS and AnG) positively track retrieval outcomes.

The vertical occipital fasciculus: A century of controversy resolved by in vivo measurements

Significance The vertical occipital fasciculus (VOF) is a major white-matter fascicle connecting dorsal and ventral visual cortex. Few vision scientists or cognitive neuroscientists are aware of the VOFs existence. The scarcity of papers on this important pathway stems from the contentious history surrounding its discovery by Wernicke in 1881. We review the conflict surrounding the classic, postmortem, VOF measurements, and we introduce modern, in vivo methods to precisely characterize the VOFs cortical terminations and unique tissue properties. The new VOF measurements provide insight into the communication between ventral stream regions involved in form perception and dorsal stream regions involved in eye movements and attention. The vertical occipital fasciculus (VOF) is the only major fiber bundle connecting dorsolateral and ventrolateral visual cortex. Only a handful of studies have examined the anatomy of the VOF or its role in cognition in the living human brain. Here, we trace the contentious history of the VOF, beginning with its original discovery in monkey by Wernicke (1881) and in human by Obersteiner (1888), to its disappearance from the literature, and recent reemergence a century later. We introduce an algorithm to identify the VOF in vivo using diffusion-weighted imaging and tractography, and show that the VOF can be found in every hemisphere (n = 74). Quantitative T1 measurements demonstrate that tissue properties, such as myelination, in the VOF differ from neighboring white-matter tracts. The terminations of the VOF are in consistent positions relative to cortical folding patterns in the dorsal and ventral visual streams. Recent findings demonstrate that these same anatomical locations also mark cytoarchitectonic and functional transitions in dorsal and ventral visual cortex. We conclude that the VOF is likely to serve a unique role in the communication of signals between regions on the ventral surface that are important for the perception of visual categories (e.g., words, faces, bodies, etc.) and regions on the dorsal surface involved in the control of eye movements, attention, and motion perception.

The improbable simplicity of the fusiform face area

The fusiform face area (FFA) is described as an easily identifiable module on the fusiform gyrus. However, the organization of face-selective regions in ventral temporal cortex (VTC) is more complex than this prevailing view. We highlight methodological factors contributing to these complexities and the extensive variability in how the FFA is identified. We suggest a series of constraints to aid researchers when defining any functionally specialized region with a pleasing realization: anatomy matters.

fMRI-Adaptation and Category Selectivity in Human Ventral Temporal Cortex: Regional Differences Across Time Scales

Repeating object images produces stimulus-specific repetition suppression referred to as functional magnetic resonance imaging-adaptation (fMRI-A) in ventral temporal cortex (VTC). However, the effects of stimulus repetition on functional selectivity are largely unknown. We investigated the effects of short-lagged (SL, immediate) and long-lagged (LL, many intervening stimuli) repetitions on category selectivity in VTC using high-resolution fMRI. We asked whether repetition produces scaling or sharpening of fMRI responses both within category-selective regions as well as in the distributed response pattern across VTC. Results illustrate that repetition effects across time scales vary quantitatively along an anterior-posterior axis and qualitatively along a lateral-medial axis. In lateral VTC, both SL and LL repetitions produce proportional fMRI-A with no change in either selectivity or distributed responses as predicted by a scaling model. Further, there is larger fMRI-A in anterior subregions irrespective of category selectivity. Medial VTC exhibits similar scaling effects during SL repetitions. However, for LL repetitions, both the selectivity and distributed pattern of responses vary with category in medial VTC as predicted by a sharpening model. Specifically, there is larger fMRI-A for nonpreferred categories compared with the preferred category, and category selectivity does not predict fMRI-A across the pattern of distributed response. Finally, simulations indicate that different neural mechanisms likely underlie fMRI-A in medial compared to lateral VTC. These results have important implications for future fMRI-A experiments because they suggest that fMRI-A does not reflect a universal neural mechanism and that results of fMRI-A experiments will likely be paradigm independent in lateral VTC but paradigm dependent in medial VTC.