Paul E. Downing

FMRI evidence for objects as the units of attentional selection

Contrasting theories of visual attention emphasize selection by spatial location, visual features (such as motion or colour) or whole objects. Here we used functional magnetic resonance imaging (fMRI) to test key predictions of the object-based theory, which proposes that pre-attentive mechanisms segment the visual array into discrete objects, groups, or surfaces, which serve as targets for visual attention. Subjects viewed stimuli consisting of a face transparently superimposed on a house, with one moving and the other stationary. In different conditions, subjects attended to the face, the house or the motion. The magnetic resonance signal from each subjects fusiform face area, parahippocampal place area and area MT/MST provided a measure of the processing of faces, houses and visual motion, respectively. Although all three attributes occupied the same location, attending to one attribute of an object (such as the motion of a moving face) enhanced the neural representation not only of that attribute but also of the other attribute of the same object (for example, the face), compared with attributes of the other object (for example, the house). These results cannot be explained by models in which attention selects locations or features, and provide physiological evidence that whole objects are selected even when only one visual attribute is relevant.

Interactions between visual working memory and selective attention.

The relationship between working memory and selective attention has traditionally been discussed as operating in one direction: Attention filters incoming information, allowing only relevant information into short-term processing stores. This study tested the prediction that the contents of visual working memory also influence the guidance of selective attention. Participants held a sample object in working memory on each trial. Two objects, one matching the sample and the other novel, were then presented simultaneously. As measured by a probe task, attention shifted to the object matching the sample. This effect generalized across object type, attentional-probe task, and working memory task. In contrast, a matched task with no memory requirement showed the opposite pattern, demonstrating that this effect is not simply due to exposure to the sample. These results confirm a specific prediction about the influence of working memory contents on the guidance of attention.

Competition in visual working memory for control of search

Recent perspectives on selective attention posit a central role for visual working memory (VWM) in the top‐down control of attention. According to the biased‐competition model (Desimone & Duncan, 1995), active maintenance of an object in VWM gives matching (Downing, 2000) or related (Moores, Laiti, & Chelazzi, 2003) objects in the environment a competitive advantage over other objects in gaining access to limited processing resources. Participants in this study performed a visual search task while simultaneously maintaining a second item in VWM. On half of the trials, this item appeared as a distractor item in the search array. We found no evidence that this item interferes with successful selection of the search target, as measured with response time in a target detection task and accuracy in a target discrimination task. These results are consistent with two general models: One in which a representation of the current task biases the competition between items in a unitary VWM, or one in which VWM is fractionated to allow for maintenance of critical items that are not immediately relevant to the task.

Functional Magnetic Resonance Imaging Investigation of Overlapping Lateral Occipitotemporal Activations Using Multi-Voxel Pattern Analysis

Several functional areas are proposed to reside in human lateral occipitotemporal cortex, including the motion-selective human homolog of macaque area MT (hMT), object-form-selective lateral occipital complex (LO), and body-selective extrastriate body area (EBA). Indeed, several functional magnetic resonance imaging (fMRI) studies have reported significant activation overlap among these regions. The standard interpretation of this overlap would be that the common areas of activation reflect engagement of common neural systems. Alternatively, motion, object form, and body form may be processed independently within this general region. To distinguish these possibilities, we first analyzed the lateral occipitotemporal responses to motion, objects, bodies, and body parts with whole-brain group-average analyses and within-subjects functional region of interest (ROI) analyses. The activations elicited by these stimuli, each relative to a matched control, overlapped substantially in the group analysis. When hMT, LO, and EBA were defined functionally within subjects, each ROI in each hemisphere (except right-hemisphere hMT) showed significant selectivity for motion, intact objects, bodies, and body parts, although only the peak voxel of each region was tested. In contrast, multi-voxel analyses of variations in selectivity patterns revealed that visual motion, object form, and the form of the human body elicited three relatively independent patterns of fMRI activity in lateral occipitotemporal cortex. Multi-voxel approaches, in contrast to other methods, can reveal the functional significance of overlapping fMRI activity in extrastriate cortex and, by extension, elsewhere in the brain.

Surface-Based Information Mapping Reveals Crossmodal Vision–Action Representations in Human Parietal and Occipitotemporal Cortex

Many lines of evidence point to a tight linkage between the perceptual and motoric representations of actions. Numerous demonstrations show how the visual perception of an action engages compatible activity in the observers motor system. This is seen for both intransitive actions (e.g., in the case of unconscious postural imitation) and transitive actions (e.g., grasping an object). Although the discovery of “mirror neurons” in macaques has inspired explanations of these processes in human action behaviors, the evidence for areas in the human brain that similarly form a crossmodal visual/motor representation of actions remains incomplete. To address this, in the present study, participants performed and observed hand actions while being scanned with functional MRI. We took a data-driven approach by applying whole-brain information mapping using a multivoxel pattern analysis (MVPA) classifier, performed on reconstructed representations of the cortical surface. The aim was to identify regions in which local voxelwise patterns of activity can distinguish among different actions, across the visual and motor domains. Experiment 1 tested intransitive, meaningless hand movements, whereas experiment 2 tested object-directed actions (all right-handed). Our analyses of both experiments revealed crossmodal action regions in the lateral occipitotemporal cortex (bilaterally) and in the left postcentral gyrus/anterior parietal cortex. Furthermore, in experiment 2 we identified a gradient of bias in the patterns of information in the left hemisphere postcentral/parietal region. The postcentral gyrus carried more information about the effectors used to carry out the action (fingers vs. whole hand), whereas anterior parietal regions carried more information about the goal of the action (lift vs. punch). Taken together, these results provide evidence for common neural coding in these areas of the visual and motor aspects of actions, and demonstrate further how MVPA can contribute to our understanding of the nature of distributed neural representations.

The effect of viewpoint on body representation in the extrastriate body area

Functional neuroimaging has revealed several brain regions that are selective for the visual appearance of others, in particular the face. More recent evidence points to a lateral temporal region that responds to the visual appearance of the human body (extrastriate body area or EBA). We tested whether this region distinguishes between egocentric and allocentric views of the self and other people. EBA activity increased significantly for allocentric relative to egocentric views in the right hemisphere, but was not influenced by identity. Whole-brain analyses revealed several regions that were influenced by viewpoint or identity. Modulation of EBA activity by viewpoint was modest relative to modulation by stimulus class. We propose that the EBA plays a relatively early role in social vision.

An event-related potential component sensitive to images of the human body.

One of the critical functions of vision is to provide information about other individuals. Neuroimaging experiments examining the cortical regions that analyze the appearance of other people have found partially overlapping networks that respond selectively to human faces and bodies. In event-related potential (ERP) studies, faces systematically elicit a negative component peaking 170 ms after presentation - the N170. To characterize the electrophysiological response to human bodies, we compared the ERPs elicited by faces, bodies and various control stimuli. In Experiment 1, a comparison of ERPs elicited by faces, bodies, objects and places showed that pictures of the human body (without the head) elicit a negative component peaking at 190 ms (an N190). While broadly similar to the N170, the N190 differs in both spatial distribution and amplitude from the N1 components elicited by faces, objects and scenes and peaks significantly later than the N170. The difference between N190 and N170 was further supported using topographic analyses of ERPs and source localization techniques. A unique, stable map topography was found to characterize human bodies between 130 and 230 ms. In Experiment 2, we tested the four conditions from Experiment 1, as well as intact and scrambled silhouettes and stick figures of the human body. We found that intact silhouettes and stick figures elicited significantly greater N190 amplitudes than their scrambled counterparts. Thus, the N190 generalizes to some degree to schematic depictions of the human form. Overall, our findings are consistent with intertwined, but functionally distinct, neural representations of the human face and body.

Within-subject reproducibility of category- specific visual activation with functional MRI

We used functional magnetic resonance imaging (fMRI) to investigate within‐subject reproducibility of activation in higher level, category‐specific visual areas to validate the functional localization approach widely used for these areas. The brain areas investigated included the extrastriate body area (EBA), which responds selectively to human bodies, the fusiform face area (FFA) and the occipital face area (OFA), which respond selectively to faces, and the parahippocampal place area (PPA), which responds selectively to places and scenes. All six subjects showed significant bilateral activation in the four areas. Reproducibility was very high for all areas, both within a scanning session and between scanning sessions separated by 3 weeks. Within sessions, the mean distance between peak voxels of the same area localized by using different functional runs was 1.5 mm. The mean distance between peak voxels of areas localized in different sessions was 2.9 mm. Functional reproducibility, as expressed by the stability of T‐values across sessions, was high for both within‐session and between‐session comparisons. We conclude that within subjects, high‐level category‐specific visual areas can be localized robustly across scanning sessions. Hum Brain Mapp, 2005.

The role of occipitotemporal body-selective regions in person perception

The visual appearance of others’ bodies is a powerful source of information about the people around us. This information is implicit in the stimulus and must be extracted and made explicit by the coordination of activity in multiple cortical areas. Here we consider the contribution to this process of two strongly body-selective occipitotemporal regions identified in human neuroimaging experiments: the extrastriate body area (EBA) and the fusiform body area (FBA). We address the evidence and arguments behind numerous recent proposals that EBA and FBA build explicit representations of identity, emotion, body movements, or goal-directed actions from the visual appearance of bodies, and also explore the contribution of these regions to motor control. We argue that the current evidence does not support a model in which EBA and FBA directly perform any of these higher-level functions. Instead, we argue that these regions comprise populations of neurons that encode fine details of the shape and posture of the bodies of people in the current percept. In doing so, they provide a powerful but cognitively unelaborated perceptual framework that allows other cortical systems to exploit the rich, socially relevant information that is conveyed by the body.

The role of the extrastriate body area in action perception

Abstract Numerous cortical regions respond to aspects of the human form and its actions. What is the contribution of the extrastriate body area (EBA) to this network? In particular, is the EBA involved in constructing a dynamic representation of observed actions? We scanned 16 participants with fMRI while they viewed two kinds of stimulus sequences. In the coherent condition, static frames from a movie of a single, intransitive whole-body action were presented in the correct order. In the incoherent condition, a series of frames from multiple actions (involving one actor) were presented. ROI analyses showed that the EBA, unlike area MT + and the posterior superior temporal sulcus, responded more to the incoherent than to the coherent conditions. Whole brain analyses revealed increased activation to the coherent sequences in parietal and frontal regions that have been implicated in the observation and control of movement. We suggest that the EBA response adapts when succeeding images depict relatively similar postures (coherent condition) compared to relatively different postures (incoherent condition). We propose that the EBA plays a unique role in the perception of action, by representing the static structure, rather than dynamic aspects, of the human form.