Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques.

The existence of color-processing regions in the human ventral visual pathway (VVP) has long been known from patient and imaging studies, but their location in the cortex relative to other regions, their selectivity for color compared with other properties (shape and object category), and their relationship to color-processing regions found in nonhuman primates remain unclear. We addressed these questions by scanning 13 subjects with fMRI while they viewed two versions of movie clips (colored, achromatic) of five different object classes (faces, scenes, bodies, objects, scrambled objects). We identified regions in each subject that were selective for color, faces, places, and object shape, and measured responses within these regions to the 10 conditions in independently acquired data. We report two key findings. First, the three previously reported color-biased regions (located within a band running posterior-anterior along the VVP, present in most of our subjects) were sandwiched between face-selective cortex and place-selective cortex, forming parallel bands of face, color, and place selectivity that tracked the fusiform gyrus/collateral sulcus. Second, the posterior color-biased regions showed little or no selectivity for object shape or for particular stimulus categories and showed no interaction of color preference with stimulus category, suggesting that they code color independently of shape or stimulus category; moreover, the shape-biased lateral occipital region showed no significant color bias. These observations mirror results in macaque inferior temporal cortex (Lafer-Sousa and Conway, 2013), and taken together, these results suggest a homology in which the entire tripartite face/color/place system of primates migrated onto the ventral surface in humans over the course of evolution. SIGNIFICANCE STATEMENT: Here we report that color-biased cortex is sandwiched between face-selective and place-selective cortex on the bottom surface of the brain in humans. This face/color/place organization mirrors that seen on the lateral surface of the temporal lobe in macaques, suggesting that the entire tripartite system is homologous between species. This result validates the use of macaques as a model for human vision, making possible more powerful investigations into the connectivity, precise neural codes, and development of this part of the brain. In addition, we find substantial segregation of color from shape selectivity in posterior regions, as observed in macaques, indicating a considerable dissociation of the processing of shape and color in both species.

Pitch-Responsive Cortical Regions in Congenital Amusia.

Congenital amusia is a lifelong deficit in music perception thought to reflect an underlying impairment in the perception and memory of pitch. The neural basis of amusic impairments is actively debated. Some prior studies have suggested that amusia stems from impaired connectivity between auditory and frontal cortex. However, it remains possible that impairments in pitch coding within auditory cortex also contribute to the disorder, in part because prior studies have not measured responses from the cortical regions most implicated in pitch perception in normal individuals. We addressed this question by measuring fMRI responses in 11 subjects with amusia and 11 age- and education-matched controls to a stimulus contrast that reliably identifies pitch-responsive regions in normal individuals: harmonic tones versus frequency-matched noise. Our findings demonstrate that amusic individuals with a substantial pitch perception deficit exhibit clusters of pitch-responsive voxels that are comparable in extent, selectivity, and anatomical location to those of control participants. We discuss possible explanations for why amusics might be impaired at perceiving pitch relations despite exhibiting normal fMRI responses to pitch in their auditory cortex: (1) individual neurons within the pitch-responsive region might exhibit abnormal tuning or temporal coding not detectable with fMRI, (2) anatomical tracts that link pitch-responsive regions to other brain areas (e.g., frontal cortex) might be altered, and (3) cortical regions outside of pitch-responsive cortex might be abnormal. The ability to identify pitch-responsive regions in individual amusic subjects will make it possible to ask more precise questions about their role in amusia in future work.

Interpreting fMRI data: maps, modules and dimensions.

Neuroimaging research over the past decade has revealed a detailed picture of the functional organization of the human brain. Here we focus on two fundamental questions that are raised by the detailed mapping of sensory and cognitive functions and illustrate these questions with findings from the object-vision pathway. First, are functionally specific regions that are located close together best understood as distinct cortical modules or as parts of a larger-scale cortical map? Second, what functional properties define each cortical map or module? We propose a model in which overlapping continuous maps of simple features give rise to discrete modules that are selective for complex stimuli.

Attention and biased competition in multi-voxel object representations.

The biased-competition theory accounts for attentional effects at the single-neuron level: It predicts that the neuronal response to simultaneously-presented stimuli is a weighted average of the response to isolated stimuli, and that attention biases the weights in favor of the attended stimulus. Perception, however, relies not on single neurons but on larger neuronal populations. The responses of such populations are in part reflected in large-scale multivoxel fMRI activation patterns. Because the pooling of neuronal responses into blood-oxygen-level-dependent signals is nonlinear, fMRI effects of attention need not mirror those observed at the neuronal level. Thus, to bridge the gap between neuronal responses and human perception, it is fundamental to understand attentional influences in large-scale multivariate representations of simultaneously-presented objects. Here, we ask how responses to simultaneous stimuli are combined in multivoxel fMRI patterns, and how attention affects the paired response. Objects from four categories were presented singly, or in pairs such that each category was attended, unattended, or attention was divided between the two. In a multidimensional voxel space, the response to simultaneously-presented categories was well described as a weighted average. The weights were biased toward the preferred category in category-selective regions. Consistent with single-unit reports, attention shifted the weights by approximately 30% in favor of the attended stimulus. These findings extend the biased-competition framework to the realm of large-scale multivoxel brain activations.

Only some spatial patterns of fMRI response are read out in task performance.

Classification methods show that the spatial pattern of a functional magnetic resonance imaging response across the cortex contains category information, but whether such patterns are used, or 'read out', in behavioral performance remains untested. We show that although the spatial pattern in both the retinotopic and lateral occipital cortex (LOC) in humans contains category information, only in the LOC is the pattern stronger for correct than for incorrect trials. Thus, some, but not all, spatial patterns are read out during task performance.

A stable topography of selectivity for unfamiliar shape classes in monkey inferior temporal cortex.

The inferior temporal (IT) cortex in monkeys plays a central role in visual object recognition and learning. Previous studies have observed patches in IT cortex with strong selectivity for highly familiar object classes (e.g., faces), but the principles behind this functional organization are largely unknown due to the many properties that distinguish different object classes. To unconfound shape from meaning and memory, we scanned monkeys with functional magnetic resonance imaging while they viewed classes of initially novel objects. Our data revealed a topography of selectivity for these novel object classes across IT cortex. We found that this selectivity topography was highly reproducible and remarkably stable across a 3-month interval during which monkeys were extensively trained to discriminate among exemplars within one of the object classes. Furthermore, this selectivity topography was largely unaffected by changes in behavioral task and object retinal position, both of which preserve shape. In contrast, it was strongly influenced by changes in object shape. The topography was partially related to, but not explained by, the previously described pattern of face selectivity. Together, these results suggest that IT cortex contains a large-scale map of shape that is largely independent of meaning, familiarity, and behavioral task.

Discrimination training alters object representations in human extrastriate cortex.

Visual object recognition relies critically on learning. However, little is known about the effect of object learning in human visual cortex, and in particular how the spatial distribution of training effects relates to the distribution of object and face selectivity across the cortex before training. We scanned human subjects with high-resolution functional magnetic resonance imaging (fMRI) while they viewed novel object classes, both before and after extensive training to discriminate between exemplars within one of these object classes. Training increased the strength of the response in visual cortex to trained objects compared with untrained objects. However, training did not simply induce a uniform increase in the response to trained objects: the magnitude of this training effect varied substantially across subregions of extrastriate cortex, with some showing a twofold increase in response to trained objects and others (including the right fusiform face area) showing no significant effect of training. Furthermore, the spatial distribution of training effects could not be predicted from the spatial distribution of either pretrained responses or face selectivity. Instead, training changed the spatial distribution of activity across the cortex. These findings support a dynamic view of the ventral visual pathway in which the cortical representation of an object category is continuously modulated by experience.

Reorganization of visual processing in macular degeneration.

Macular degeneration (MD), the leading cause of visual impairment in the developed world, damages the central retina, often obliterating foveal vision and severely disrupting everyday tasks such as reading, driving, and face recognition. In such cases, the macular damage eliminates the normal retinal input to a large region of visual cortex, comprising tens of square centimeters of surface area in each hemisphere, which is normally responsive only to foveal stimuli. Using functional magnetic resonance imaging, we asked whether this deprived cortex simply becomes inactive in subjects with MD, or whether it takes on new functional properties. In two adult MD subjects with extensive bilateral central retinal lesions, we found that parts of visual cortex (including primary visual cortex) that normally respond only to central visual stimuli are strongly activated by peripheral stimuli. Such activation was not observed (1) with visual stimuli presented to the position of the former fovea and (2) in control subjects with visual stimuli presented to corresponding parts of peripheral retina. These results demonstrate large-scale reorganization of visual processing in MD and will likely prove important in any effort to develop new strategies for rehabilitation of MD subjects.

Distinct Cortical Pathways for Music and Speech Revealed by Hypothesis-Free Voxel Decomposition.

The organization of human auditory cortex remains unresolved, due in part to the small stimulus sets common to fMRI studies and the overlap of neural populations within voxels. To address these challenges, we measured fMRI responses to 165 natural sounds and inferred canonical response profiles ("components") whose weighted combinations explained voxel responses throughout auditory cortex. This analysis revealed six components, each with interpretable response characteristics despite being unconstrained by prior functional hypotheses. Four components embodied selectivity for particular acoustic features (frequency, spectrotemporal modulation, pitch). Two others exhibited pronounced selectivity for music and speech, respectively, and were not explainable by standard acoustic features. Anatomically, music and speech selectivity concentrated in distinct regions of non-primary auditory cortex. However, music selectivity was weak in raw voxel responses, and its detection required a decomposition method. Voxel decomposition identifies primary dimensions of response variation across natural sounds, revealing distinct cortical pathways for music and speech.

Deformation-Invariant Sparse Coding for Modeling Spatial Variability of Functional Patterns in the Brain.

For a given cognitive task such as language processing, the location of corresponding functional regions in the brain may vary across subjects relative to anatomy. We present a probabilistic generative model that accounts for such variability as observed in fMRI data. We relate our approach to sparse coding that estimates a basis consisting of functional regions in the brain. Individual fMRI data is represented as a weighted sum of these functional regions that undergo deformations. We demonstrate the proposed method on a language fMRI study. Our method identified activation regions that agree with known literature on language processing and established correspondences among activation regions across subjects, producing more robust group-level effects than anatomical alignment alone.

A preference for contralateral stimuli in human object- and face-selective cortex.

Visual input from the left and right visual fields is processed predominantly in the contralateral hemisphere. Here we investigated whether this preference for contralateral over ipsilateral stimuli is also found in high-level visual areas that are important for the recognition of objects and faces. Human subjects were scanned with functional magnetic resonance imaging (fMRI) while they viewed and attended faces, objects, scenes, and scrambled images in the left or right visual field. With our stimulation protocol, primary visual cortex responded only to contralateral stimuli. The contralateral preference was smaller in object- and face-selective regions, and it was smallest in the fusiform gyrus. Nevertheless, each region showed a significant preference for contralateral stimuli. These results indicate that sensitivity to stimulus position is present even in high-level ventral visual cortex.