Linda Henriksson

Spatial frequency tuning in human retinotopic visual areas

Human medial occipital cortex comprises multiple visual areas, each with a distinct retinotopic representation of visual environment. We measured spatial frequency (SF) tuning curves with functional magnetic resonance imaging (fMRI) and found consistent differences between these areas. Areas V1, V2, VP, V3, V4v, and V3A were all band-pass tuned, with progressively lower SF optima in V1, V2, and V3A. In VP and V3, the SF optima were similar to optima in V2, whereas V4v showed more individual variation and scattered SF representations on the cortical surface. Area V5+ showed low-pass SF tuning. In each area, the SF optimum declined with increasing eccentricity. After accounting for the cortical magnification, the cortical extent of the optimal spatial wavelengths was approximately constant across eccentricity in V1, which suggests an anatomical constraint for the optimal SF, and this extent is actually comparable to the extent of horizontal connections within primate V1. The optimal spatial wavelengths in the visual field are also of similar extent to the spatial summation fields of macaque V1. The progressive decline in the SF tuning from V1 to V2 and V3A is compatible with the view that these areas represent visual information at different spatial scales.

Training-induced cortical representation of a hemianopic hemifield

Background: Patients with homonymous hemianopia often have some residual sensitivity for visual stimuli in their blind hemifield. Previous imaging studies suggest an important role for extrastriate cortical areas in such residual vision, but results of training to improve vision in patients with hemianopia are conflicting. Objective: To show that intensive training with flicker stimulation in the chronic stage of stroke can reorganise visual cortices of an adult patient. Methods: A 61-year-old patient with homonymous hemianopia was trained with flicker stimulation, starting 22 months after stroke. Changes in functioning during training were documented with magnetoencephalography, and the cortical organisation after training was examined with functional magnetic resonance imaging (fMRI). Results: Both imaging methods showed that, after training, visual information from both hemifields was processed mainly in the intact hemisphere. The fMRI mapping results showed the representations of both the blind and the normal hemifield in the same set of cortical areas in the intact hemisphere, more specifically in the visual motion-sensitive area V5, in a region around the superior temporal sulcus and in retinotopic visual areas V1 (primary visual cortex), V2, V3 and V3a. Conclusions: Intensive training of a blind hemifield can induce cortical reorganisation in an adult patient, and this case shows an ipsilateral representation of the trained visual hemifield in several cortical areas, including the primary visual cortex.

Multifocal fMRI mapping of visual cortical areas

The multifocal mapping of electroretinograms and visual evoked potentials has established an important role in both basic research and in diagnostic procedures. We have developed a multifocal mapping method for fMRI, which allows detailed analysis of multiple local visual field representations in the cortex with excellent spatial resolution. Visual field was divided into 60 regions in a dartboard configuration, scaled according to the human magnification factor. Within blocks of 7 s, half of the regions were stimulated with checkerboard patterns contrast reversing at 8 reversals per second, while the other half remained inactive at uniform luminance. The subset of active regions changed with each 7-s block, according to an orthogonal design. Functional MRI was done with a 3-T GE Signa and analyzed with SPM2. A general linear model was fitted producing activation maps for each of the 60 regions, and local signal changes were quantified from V1. These activation maps were next assigned to 3D surface models of the cortical sheet, and then unfolded, using the Brain à la Carte software package. Phase-encoded retinotopic analysis of conventional design served as qualitative comparison data. With multifocal fMRI, all regions were mapped with good signal-to-noise ratio in V1, and subsets of regions showed activation in V2 and V3. This method allows rapid and direct exploration of multiple local visual responses, and is thus able to give complementary information to phase encoded mapping of retinotopic areas.

Centrality of Social Interaction in Human Brain Function.

People are embedded in social interaction that shapes their brains throughout lifetime. Instead of emerging from lower-level cognitive functions, social interaction could be the default mode via which humans communicate with their environment. Should this hypothesis be true, it would have profound implications on how we think about brain functions and how we dissect and simulate them. We suggest that the research on the brain basis of social cognition and interaction should move from passive spectator science to studies including engaged participants and simultaneous recordings from the brains of the interacting persons.

Representation of Cross-Frequency Spatial Phase Relationships in Human Visual Cortex

An image patch can be locally decomposed into sinusoidal waves of different orientations, spatial frequencies, amplitudes, and phases. The local phase information is essential for perception, because important visual features like edges emerge at locations of maximal local phase coherence. Detection of phase coherence requires integration of spatial frequency information across multiple spatial scales. Models of early visual processing suggest that the visual system should implement phase-sensitive pooling of spatial frequency information in the identification of broadband edges. We used functional magnetic resonance imaging (fMRI) adaptation to look for phase-sensitive neural responses in the human visual cortex. We found sensitivity to the phase difference between spatial frequency components in all studied visual areas, including the primary visual cortex (V1). Control experiments demonstrated that these results were not explained by differences in contrast or position. Next, we compared fMRI responses for broadband compound grating stimuli with congruent and random phase structures. All studied visual areas showed stronger responses for the stimuli with congruent phase structure. In addition, selectivity to phase congruency increased from V1 to higher-level visual areas along both the ventral and dorsal streams. We conclude that human V1 already shows phase-sensitive pooling of spatial frequencies, but only higher-level visual areas might be capable of pooling spatial frequency information across spatial scales typical for broadband natural images.

Retinotopic Maps, Spatial Tuning, and Locations of Human Visual Areas in Surface Coordinates Characterized with Multifocal and Blocked fMRI Designs

The localization of visual areas in the human cortex is typically based on mapping the retinotopic organization with functional magnetic resonance imaging (fMRI). The most common approach is to encode the response phase for a slowly moving visual stimulus and to present the result on an individuals reconstructed cortical surface. The main aims of this study were to develop complementary general linear model (GLM)-based retinotopic mapping methods and to characterize the inter-individual variability of the visual area positions on the cortical surface. We studied 15 subjects with two methods: a 24-region multifocal checkerboard stimulus and a blocked presentation of object stimuli at different visual field locations. The retinotopic maps were based on weighted averaging of the GLM parameter estimates for the stimulus regions. In addition to localizing visual areas, both methods could be used to localize multiple retinotopic regions-of-interest. The two methods yielded consistent retinotopic maps in the visual areas V1, V2, V3, hV4, and V3AB. In the higher-level areas IPS0, VO1, LO1, LO2, TO1, and TO2, retinotopy could only be mapped with the blocked stimulus presentation. The gradual widening of spatial tuning and an increase in the responses to stimuli in the ipsilateral visual field along the hierarchy of visual areas likely reflected the increase in the average receptive field size. Finally, after registration to Freesurfers surface-based atlas of the human cerebral cortex, we calculated the mean and variability of the visual area positions in the spherical surface-based coordinate system and generated probability maps of the visual areas on the average cortical surface. The inter-individual variability in the area locations decreased when the midpoints were calculated along the spherical cortical surface compared with volumetric coordinates. These results can facilitate both analysis of individual functional anatomy and comparisons of visual cortex topology across studies.

Faciotopy—A face-feature map with face-like topology in the human occipital face area

The occipital face area (OFA) and fusiform face area (FFA) are brain regions thought to be specialized for face perception. However, their intrinsic functional organization and status as cortical areas with well-defined boundaries remains unclear. Here we test these regions for “faciotopy”, a particular hypothesis about their intrinsic functional organisation. A faciotopic area would contain a face-feature map on the cortical surface, where cortical patches represent face features and neighbouring patches represent features that are physically neighbouring in a face. The faciotopy hypothesis is motivated by the idea that face regions might develop from a retinotopic protomap and acquire their selectivity for face features through natural visual experience. Faces have a prototypical configuration of features, are usually perceived in a canonical upright orientation, and are frequently fixated in particular locations. To test the faciotopy hypothesis, we presented images of isolated face features at fixation to subjects during functional magnetic resonance imaging. The responses in V1 were best explained by low-level image properties of the stimuli. OFA, and to a lesser degree FFA, showed evidence for faciotopic organization. When a single patch of cortex was estimated for each face feature, the cortical distances between the feature patches reflected the physical distance between the features in a face. Faciotopy would be the first example, to our knowledge, of a cortical map reflecting the topology, not of a part of the organism itself (its retina in retinotopy, its body in somatotopy), but of an external object of particular perceptual significance.

Quantitative multifocal fMRI shows active suppression in human V1

Multifocal functional magnetic resonance imaging has recently been introduced as an alternative method for retinotopic mapping, and it enables effective functional localization of multiple regions‐of‐interest in the visual cortex. In this study we characterized interactions in V1 with spatially and temporally identical stimuli presented alone, or as a part of a nine‐region multifocal stimulus. We compared stimuli at different contrasts, collinear and orthogonal orientations and spatial frequencies one octave apart. Results show clear attenuation of BOLD signal from the central region in the multifocal condition. The observed modulation in BOLD signal could be produced either by neural suppression resulting from stimulation of adjacent regions of visual field, or alternatively by hemodynamic saturation or stealing effects in V1. However, we find that attenuation of the central response persists through a range of contrasts, and that its strength varies with relative orientation and spatial frequency of the central and surrounding stimulus regions, indicating active suppression mechanisms of neural origin. Our results also demonstrate that the extent of the signal spreading is commensurate with the extent of the horizontal connections in primate V1. Hum Brain Mapp, 2008.

Visual representations are dominated by intrinsic fluctuations correlated between areas

Intrinsic cortical dynamics are thought to underlie trial-to-trial variability of visually evoked responses in animal models. Understanding their function in the context of sensory processing and representation is a major current challenge. Here we report that intrinsic cortical dynamics strongly affect the representational geometry of a brain region, as reflected in response-pattern dissimilarities, and exaggerate the similarity of representations between brain regions. We characterized the representations in several human visual areas by representational dissimilarity matrices (RDMs) constructed from fMRI response-patterns for natural image stimuli. The RDMs of different visual areas were highly similar when the response-patterns were estimated on the basis of the same trials (sharing intrinsic cortical dynamics), and quite distinct when patterns were estimated on the basis of separate trials (sharing only the stimulus-driven component). We show that the greater similarity of the representational geometries can be explained by coherent fluctuations of regional-mean activation within visual cortex, reflecting intrinsic dynamics. Using separate trials to study stimulus-driven representations revealed clearer distinctions between the representational geometries: a Gabor wavelet pyramid model explained representational geometry in visual areas V1–3 and a categorical animate–inanimate model in the object-responsive lateral occipital cortex.

Perception and Processing of Faces in the Human Brain Is Tuned to Typical Feature Locations

Faces are salient social stimuli whose features attract a stereotypical pattern of fixations. The implications of this gaze behavior for perception and brain activity are largely unknown. Here, we characterize and quantify a retinotopic bias implied by typical gaze behavior toward faces, which leads to eyes and mouth appearing most often in the upper and lower visual field, respectively. We found that the adult human visual system is tuned to these contingencies. In two recognition experiments, recognition performance for isolated face parts was better when they were presented at typical, rather than reversed, visual field locations. The recognition cost of reversed locations was equal to ∼60% of that for whole face inversion in the same sample. Similarly, an fMRI experiment showed that patterns of activity evoked by eye and mouth stimuli in the right inferior occipital gyrus could be separated with significantly higher accuracy when these features were presented at typical, rather than reversed, visual field locations. Our findings demonstrate that human face perception is determined not only by the local position of features within a face context, but by whether features appear at the typical retinotopic location given normal gaze behavior. Such location sensitivity may reflect fine-tuning of category-specific visual processing to retinal input statistics. Our findings further suggest that retinotopic heterogeneity might play a role for face inversion effects and for the understanding of conditions affecting gaze behavior toward faces, such as autism spectrum disorders and congenital prosopagnosia. SIGNIFICANCE STATEMENT Faces attract our attention and trigger stereotypical patterns of visual fixations, concentrating on inner features, like eyes and mouth. Here we show that the visual system represents face features better when they are shown at retinal positions where they typically fall during natural vision. When facial features were shown at typical (rather than reversed) visual field locations, they were discriminated better by humans and could be decoded with higher accuracy from brain activity patterns in the right occipital face area. This suggests that brain representations of face features do not cover the visual field uniformly. It may help us understand the well-known face-inversion effect and conditions affecting gaze behavior toward faces, such as prosopagnosia and autism spectrum disorders.