Hans Op de Beeck

Spatial sensitivity of macaque inferior temporal neurons

Recent findings in dorsal visual stream areas and computational work raise the question whether neurons at the end station of the ventral visual stream can code for stimulus position. The authors provide the first detailed, quantitative data on the spatial sensitivity of neurons in the anterior part of the inferior temporal cortex (area TE) in awake, fixating monkeys. They observed a large variation in receptive field (RF) size (ranging from 2.8° to 26°). TE neurons differed in their optimal position, with a bias toward the foveal position. Moreover, the RF profiles of most TE neurons could be fitted well with a two‐dimensional Gaussian function. Most neurons had only one region of high sensitivity and showed a smooth decline in sensitivity toward more distal positions. In addition, the authors investigated some of the possible determinants of such spatial sensitivity. First, testing with low‐pass filtered versions of the stimuli revealed that the general preference for the foveal position and the size of the RFs was not due simply to TE neurons receiving input with a lower spatial resolution at more eccentric positions. The foveal position was still preferred after intense low‐pass filtering. Second, although an increase in stimulus size consistently broadened spatial sensitivity profiles, it did not change the qualitative features of these profiles. Moreover, size selectivity of TE neurons was generally position invariant. Overall, the results suggest that TE neurons can code for the position of stimuli in the central region of the visual field. J. Comp. Neurol. 426:505–518, 2000.

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.

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.

Inferotemporal neurons represent low-dimensional configurations of parameterized shapes

Behavioral studies with parameterized shapes have shown that the similarities among these complex stimuli can be represented using a low number of dimensions. Using psychophysical measurements and single-cell recordings in macaque inferotemporal (IT) cortex, we found an agreement between low-dimensional parametric configurations of shapes and the representation of shape similarity at the behavioral and neuronal level. The shape configurations, computed from both the perceived and neuron-based similarities, revealed a low number of dimensions and contained the same stimulus order as the parametric configurations. However, at a metric level, the behavioral and neural representations deviated consistently from the parametric configurations. These findings suggest an ordinally faithful but metrically biased representation of shape similarity in IT.

Against hyperacuity in brain reading: Spatial smoothing does not hurt multivariate fMRI analyses?

Abstract Recently it has been suggested that multivariate analyses of functional magnetic resonance imaging (fMRI) data can detect high spatial frequency components of cortical signals, like sub-millimeter columns. This ‘hyperacuity’ seems to be at odds with the common assumption that the fMRI signal has a low spatial resolution due to the spatial spread of the underlying hemodynamic events. To resolve this apparent contradiction, I checked a very straightforward prediction of the hyperacuity hypothesis: if multivariate analyses are picking up a small-scale functional organization, then it can be expected that smoothing will be detrimental to the ability to decode these fine-scale spatial signals. I tested this prediction using data obtained with two paradigms to which multivariate techniques have been applied previously, including the decoding of grating orientation from the pattern of activity in primary visual cortex. It was found that smoothing does not decrease the sensitivity of multivariate analyses. Further simulations in which the scale of cortical organization was known indicate that this effect of smoothing contradicts the idea that the patterns detected with multivariate techniques reflect a fine-scale spatial organization.

Perceived Shape Similarity among Unfamiliar Objects and the Organization of the Human Object Vision Pathway

Humans rely heavily on shape similarity among objects for object categorization and identification. Studies using functional magnetic resonance imaging (fMRI) have shown that a large region in human occipitotemporal cortex processes the shape of meaningful as well as unfamiliar objects. Here, we investigate whether the functional organization of this region as measured with fMRI is related to perceived shape similarity. We found that unfamiliar object classes that are rated as having a similar shape were associated with a very similar response pattern distributed across object-selective cortex, whereas object classes that were rated as being very different in shape were associated with a more different response pattern. Human observers, as well as object-selective cortex, were very sensitive to differences in shape features of the objects such as straight versus curved versus “spiky” edges, more so than to differences in overall shape envelope. Response patterns in retinotopic areas V1, V2, and V4 were not found to be related to perceived shape. The functional organization in area V3 was partially related to perceived shape but without a stronger sensitivity for shape features relative to overall shape envelope. Thus, for unfamiliar objects, the organization of human object-selective cortex is strongly related to perceived shape, and this shape-based organization emerges gradually throughout the object vision pathway.

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.

Feedback of visual object information to foveal retinotopic cortex

The mammalian visual system contains an extensive web of feedback connections projecting from higher cortical areas to lower areas, including primary visual cortex. Although multiple theories have been proposed, the role of these connections in perceptual processing is not understood. We found that the pattern of functional magnetic resonance imaging response in human foveal retinotopic cortex contained information about objects presented in the periphery, far away from the fovea, which has not been predicted by prior theories of feedback. This information was position invariant, correlated with perceptual discrimination accuracy and was found only in foveal, but not peripheral, retinotopic cortex. Our data cannot be explained by differential eye movements, activation from the fixation cross, or spillover activation from peripheral retinotopic cortex or from lateral occipital complex. Instead, our findings indicate that position-invariant object information from higher cortical areas is fed back to foveal retinotopic cortex, enhancing task performance.

Tuning for shape dimensions in macaque inferior temporal cortex.

It is widely assumed that distributed bell‐shaped tuning (e.g. Radial Basis functions) characterizes the shape selectivity of macaque inferior temporal (IT) neurons, analogous to the orientation or spatial frequency tuning found in early visual cortex. Demonstrating such tuning properties requires testing the responses of neurons for different values along dimensions of shape. We recorded the responses of single macaque IT neurons to variations of a rectangle and a triangle along simple shape dimensions, such as taper and axis curvature. The neurons showed systematic response modulation along these dimensions, with the greatest response, on average, to the highest values on the dimensions, e.g. to the most curved shapes. Within the range of values tested, the response functions were monotonic rather than bell‐shaped. Multi‐dimensional scaling of the neural responses showed that these simple shape dimensions were coded orthogonally by IT neurons: the degree and direction of responses modulation (i.e. the increase or decrease of responses along a dimension) was independent for the different dimensions. Furthermore, for combinations of curvature‐related and other simple shape dimensions, the joint tuning was separable, that is well predicted by the product of the tuning for each of the dimensions. The independence of dimensional tuning may provide the neural basis for the independence of psychophysical judgements of multidimensional stimuli.

Distributed subordinate specificity for bodies, faces, and buildings in human ventral visual cortex.

Previous studies have revealed regions in human visual cortex with a strong preference for faces, headless bodies, and buildings. We investigated whether the pattern of activity in these category-selective regions is related to more subordinate distinctions among objects. Our experiments included two types of faces (elderly faces and baby faces), body parts (hands and torsos), and buildings (rural buildings and skyscrapers). Multi-voxel pattern analyses revealed very clear differences in the activation pattern between hands and torsos, and smaller but significant differences in the activation pattern between the two face conditions and between the two building conditions. The subordinate specificity was very distributed, as all category-selective regions were most selective for the distinction between hands and torsos, independently from their preferred category. The selectivity for hands versus torsos was preserved across exemplars and image orientations in all category-selective regions, indicating that the distributed subordinate selectivity is related to relatively invariant and higher-order properties of the images.