Position selectivity in face-sensitive visual cortex to facial and nonfacial stimuli: an fMRI study.

BACKGROUND: Evidence for position sensitivity in object-selective visual areas has been building. On one hand, most of the relevant studies have utilized stimuli for which the areas are optimally selective and examine small sections of cortex. On the other hand, visual field maps established with nonspecific stimuli have been found in increasingly large areas of visual cortex, though generally not in areas primarily responsive to faces. METHODS: fMRI was used to study the position sensitivity of the occipital face area (OFA) and the fusiform face area (FFA) to both standard rotating wedge retinotopic mapping stimuli and quadrant presentations of synthetic facial stimuli. Analysis methods utilized were both typical, that is, mean univariate BOLD signals and multivoxel pattern analysis (MVPA), and novel, that is, distribution of voxels to pattern classifiers and use of responses to nonfacial retinotopic mapping stimuli to classify responses to facial stimuli. RESULTS: Polar angle sensitivity was exhibited to standard retinotopic mapping stimuli with a stronger contralateral bias in OFA than in FFA, a stronger bias toward the vertical meridian in FFA than in OFA, and a bias across both areas toward the inferior visual field. Contralateral hemispheric lateralization of both areas was again shown using synthetic face stimuli based on univariate BOLD signals, MVPA, and the biased contribution of voxels toward multivariate classifiers discriminating the contralateral visual field. Classifiers based on polar angle responsivity were used to classify the patterns of activation above chance levels to face stimuli in the OFA but not in the FFA. CONCLUSIONS: Both the OFA and FFA exhibit quadrant sensitivity to face stimuli, though the OFA exhibits greater position responsivity across stimuli than the FFA and includes overlap in the response pattern to the disparate stimulus types. Such biases are consistent with varying position sensitivity along different surfaces of occipito-temporal cortex.

Spatial characteristics of motion-sensitive mechanisms change with age and stimulus spatial frequency.

Contrast-dependent interactions between classical (CRF) and non-classical regions (nCRF) of visual neuron receptive fields are well documented in primate visual cortex. Physiological models that describe CRF and nCRF interactions in single neurons have recently been applied to psychophysical measures of spatial summation and suppression in motion perception of young adults (Tadin & Lappin, 2005). We wished to determine whether such models could account for the reduction in spatial suppression that occurs in normal aging (Betts et al., 2005). We applied three models to duration thresholds obtained in a simple motion discrimination task using drifting Gabor stimuli that ranged in spatial frequency from 0.5 to 4c/deg. We found that a model in which the center CRF and surrounding nCRF are represented as spatially-overlapping excitatory and inhibitory 2D Gaussians with independent contrast response functions, which we call the Gain model, could account for the effects of aging simply by increasing the spatial extent of the CRF. Two additional models were evaluated. The Size model, which varied the size of the CRF as a function of contrast, produced CRF and nCRF size constants that departed significantly from physiological estimates of receptive field sizes. The Drive model, which yoked the activation of the suppressive nCRF to the CRF response, yielded reasonable fits to the data and suggested an age-related decline in the strength of suppression from the nCRF. However, the Drive model estimated the CRF size parameter to be equal to, or even slightly larger than, the nCRF size parameter, which is inconsistent with the physiological literature. Our findings therefore suggest that the Gain model provides the most plausible estimates of receptive field sizes. Based on this model, age-related increases in the size of central excitatory receptive fields relative to the inhibitory surrounds may contribute to behavioral measures of reduced spatial suppression found in older observers.

Decoding of faces and face components in face-sensitive human visual cortex.

A great challenge to the field of visual neuroscience is to understand how faces are encoded and represented within the human brain. Here we show evidence from functional magnetic resonance imaging (fMRI) for spatially distributed processing of the whole face and its components in face-sensitive human visual cortex. We used multi-class linear pattern classifiers constructed with a leave-one-scan-out verification procedure to discriminate brain activation patterns elicited by whole faces, the internal features alone, and the external head outline alone. Furthermore, our results suggest that whole faces are represented disproportionately in the fusiform cortex (FFA) whereas the building blocks of faces are represented disproportionately in occipitotemporal cortex (OFA). Faces and face components may therefore be organized with functional clustering within both the FFA and OFA, but with specialization for face components in the OFA and the whole face in the FFA.

Heterogeneous structure in face-selective human occipito-temporal cortex.

It is well established that the human visual system contains a distributed network of regions that are involved in processing faces, but our understanding of how faces are represented within these face-sensitive brain areas is incomplete. We used fMRI to investigate whether face-sensitive brain areas are solely tuned for whole faces, or whether they contain heterogeneous populations of neurons tuned to individual components of the face as well as whole faces, as suggested by physiological investigations in nonhuman primates. The middle fusiform gyrus (fusiform face area, or FFA) and the inferior occipital gyrus (occipital face area, or OFA) produced robust BOLD activation to synthetic whole face stimuli, but also to the internal facial features and head outlines. BOLD responses to whole face stimuli in FFA were significantly reduced after adaptation to whole faces, but not after adaptation to features or head outlines, whereas activation to head outlines was reduced after adaptation to both whole faces and head outlines. OFA showed no significant adaptation effects for matching adaptation and test conditions, but did exhibit cross-adaptation between whole faces and head outlines. The internal face features did not produce any significant adaptation within either FFA or OFA. Our results are consistent with a model in which independent populations of whole face-, feature-, and head outline-tuned neurons exist within face-sensitive regions of human occipito-temporal cortex, which in turn would support tasks such as viewpoint processing, emotion classification, and identity discrimination.

Spatial characteristics of center-surround antagonism in younger and older adults.

Sensitivity to motion direction is affected by stimulus size, contrast (D. Tadin & J. S. Lappin, 2005; D. Tadin, J. S. Lappin, L. A. Gilroy, & R. Blake, 2003), and observer age (L. R. Betts, C. P. Taylor, A. B. Sekuler, & P. J. Bennett, 2005). Here, we investigated the effect of spatial frequency on motion discrimination and how sensitivity changes in older adulthood. We measured stimulus duration thresholds for younger (18-30 years) and older (60-75 years) observers using drifting Gabor gratings that differed in size, spatial frequency, and contrast. A simple model characterized age differences in the threshold-vs.-size functions. The model parameter fits were consistent with an age-related decrease in the strength of spatial suppression. The model also provided good fits to the thresholds when plotted as a function of the total stimulus contrast energy, which suggests that age-related changes in summation and suppression can be modeled as reduced sensitivity to contrast energy. The summation parameter scaled according to stimulus spatial frequency in younger observers only. Suppression strength decreased as a function of spatial frequency in both age groups. Our findings provide additional evidence for age-related changes in summation and suppression mechanisms and suggest that the total contrast energy in the stimulus plays an important role in determining sensitivity to motion direction in both younger and older adults.

The effects of aging on orientation discrimination.

The current experiments measured orientation discrimination thresholds in younger (mean age approximately 23 years) and older (mean age approximately 66 years) subjects. In Experiment 1, the contrast needed to discriminate Gabor patterns (0.75, 1.5, and 3c/deg) that differed in orientation by 12deg was measured for different levels of external noise. At all three spatial frequencies, discrimination thresholds were significantly higher in older than younger subjects when external noise was low, but not when external noise was high. In Experiment 2, discrimination thresholds were measured as a function of stimulus contrast by varying orientation while contrast was fixed. The resulting threshold-vs-contrast curves had very similar shapes in the two age groups, although the curve obtained from older subjects was shifted to slightly higher contrasts. At contrasts greater than 0.05, thresholds in both older and younger subjects were approximately constant at 0.5deg. The results from Experiments 1 and 2 suggest that age differences in orientation discrimination are due solely to differences in equivalent input noise. Using the same methods as Experiment 1, Experiment 3 measured thresholds in 6 younger observers as a function of external noise and retinal illuminance. Although reducing retinal illumination increased equivalent input noise, the effect was much smaller than the age difference found in Experiment 1. Therefore, it is unlikely that differences in orientation discrimination were due solely to differences in retinal illumination. Our findings are consistent with recent physiological experiments that have found elevated spontaneous activity and reduced orientation tuning on visual cortical neurons in senescent cats (Hua, T., Li, X., He, L., Zhou, Y., Wang, Y., Leventhal, A. G. (206). Functional degradation of visual cortical cells in old cats. Neurobiology Aging, 27(1), 155-162) and monkeys (Yu, S., Wang, Y., Li, X., Zhou, Y. & Leventhal, A. G. (2006). Functional degradation of visual cortex in senescent rhesus monkeys. Neuroscience, 140(3), 1023-1029; Leventhal, A. G., Wang, Y., Pu, M., Zhou, Y. & Ma. Y. (2003). GABA and its agonists improved visual cortical function in senescent monkeys. Science,300 (5620), 812-815).

Distributed neural plasticity for shape learning in the human visual cortex.

Expertise in recognizing objects in cluttered scenes is a critical skill for our interactions in complex environments and is thought to develop with learning. However, the neural implementation of object learning across stages of visual analysis in the human brain remains largely unknown. Using combined psychophysics and functional magnetic resonance imaging (fMRI), we show a link between shape-specific learning in cluttered scenes and distributed neuronal plasticity in the human visual cortex. We report stronger fMRI responses for trained than untrained shapes across early and higher visual areas when observers learned to detect low-salience shapes in noisy backgrounds. However, training with high-salience pop-out targets resulted in lower fMRI responses for trained than untrained shapes in higher occipitotemporal areas. These findings suggest that learning of camouflaged shapes is mediated by increasing neural sensitivity across visual areas to bolster target segmentation and feature integration. In contrast, learning of prominent pop-out shapes is mediated by associations at higher occipitotemporal areas that support sparser coding of the critical features for target recognition. We propose that the human brain learns novel objects in complex scenes by reorganizing shape processing across visual areas, while taking advantage of natural image correlations that determine the distinctiveness of target shapes.

Aging reduces center-surround antagonism in visual motion processing.

Discriminating the direction of motion of a low-contrast pattern becomes easier with increasing stimulus area. However, increasing the size of a high-contrast pattern makes it more difficult for observers to discriminate motion. This surprising result, termed spatial suppression, is thought to be mediated by a form of center-surround suppression found throughout the visual pathway. Here, we examine the counterintuitive hypothesis that aging alters such center-surround interactions in ways that improve performance in some tasks. We found that older observers required briefer stimulus durations than did younger observers to extract information about stimulus direction in conditions using large, high-contrast patterns. We suggest that this age-related improvement in motion discrimination may be linked to reduced GABAergic functioning in the senescent brain, which reduces center-surround suppression in motion-selective neurons.