FMRI Reveals a Dissociation between Grasping and Perceiving the Size of Real 3D Objects

Background Almost 15 years after its formulation, evidence for the neuro-functional dissociation between a dorsal action stream and a ventral perception stream in the human cerebral cortex is still based largely on neuropsychological case studies. To date, there is no unequivocal evidence for separate visual computations of object features for performance of goal-directed actions versus perceptual tasks in the neurologically intact human brain. We used functional magnetic resonance imaging to test explicitly whether or not brain areas mediating size computation for grasping are distinct from those mediating size computation for perception. Methodology/Principal Findings Subjects were presented with the same real graspable 3D objects and were required to perform a number of different tasks: grasping, reaching, size discrimination, pattern discrimination or passive viewing. As in prior studies, the anterior intraparietal area (AIP) in the dorsal stream was more active during grasping, when object size was relevant for planning the grasp, than during reaching, when object properties were irrelevant for movement planning (grasping>reaching). Activity in AIP showed no modulation, however, when size was computed in the context of a purely perceptual task (size = pattern discrimination). Conversely, the lateral occipital (LO) cortex in the ventral stream was modulated when size was computed for perception (size>pattern discrimination) but not for action (grasping = reaching). Conclusions/Significance While areas in both the dorsal and ventral streams responded to the simple presentation of 3D objects (passive viewing), these areas were differentially activated depending on whether the task was grasping or perceptual discrimination, respectively. The demonstration of dual coding of an object for the purposes of action on the one hand and perception on the other in the same healthy brains offers a substantial contribution to the current debate about the nature of the neural coding that takes place in the dorsal and ventral streams

Separate channels for processing form, texture, and color: Evidence from fMRI adaptation and visual object agnosia

Previous neuroimaging research suggests that although object shape is analyzed in the lateral occipital cortex, surface properties of objects, such as color and texture, are dealt with in more medial areas, close to the collateral sulcus (CoS). The present study sought to determine whether there is a single medial region concerned with surface properties in general or whether instead there are multiple foci independently extracting different surface properties. We used stimuli varying in their shape, texture, or color, and tested healthy participants and 2 object-agnosic patients, in both a discrimination task and a functional MR adaptation paradigm. We found a double dissociation between medial and lateral occipitotemporal cortices in processing surface (texture or color) versus geometric (shape) properties, respectively. In Experiment 2, we found that the medial occipitotemporal cortex houses separate foci for color (within anterior CoS and lingual gyrus) and texture (caudally within posterior CoS). In addition, we found that areas selective for shape, texture, and color individually were quite distinct from those that respond to all of these features together (shape and texture and color). These latter areas appear to correspond to those associated with the perception of complex stimuli such as faces and places

Representational content of occipitotemporal and parietal tool areas

It is now established that the perception of tools engages a left-lateralized network of frontoparietal and occipitotemporal cortical regions. Nevertheless, the precise computational role played by these areas is not yet well understood. To address this question, we used functional MRI to investigate the distribution of responses to pictures of tools and hands relative to other object categories in the so-called “tool” areas. Although hands and tools are visually not alike and belong to different object categories, these are both functionally linked when considering the common role of hands and tools in object manipulation. This distinction can provide insight into the differential functional role of areas within the “tool” network. Results demonstrated that images of hands and tools activate a common network of brain areas in the left intraparietal sulcus (IPS), left lateral occipitotemporal cortex (LOTC) and ventral occipitotemporal cortex (VOTC). Importantly, multivoxel pattern analysis revealed that the distribution of hand and tool response patterns in these regions differs. These observations provide support for the idea that the left IPS, left LOTC and VOTC might have distinct computational roles with regard to tool use. Specifically, these results suggest that while left IPS supports tool action-related computations and VOTC primarily encodes category specific aspects of objects, left LOTC bridges ventro occipitotemporal perception-related and parietal action-related representations by encoding both types of object information

Patient DF's visual brain in action : visual feedforward control in patient with visual form agnosia

Patient DF, who developed visual form agnosia following ventral-stream damage, is unable to discriminate the width of objects, performing at chance, for example, when asked to open her thumb and forefinger a matching amount. Remarkably, however, DF adjusts her hand aperture to accommodate the width of objects when reaching out to pick them up (grip scaling). While this spared ability to grasp objects is presumed to be mediated by visuomotor modules in her relatively intact dorsal stream, it is possible that it may rely abnormally on online visual or haptic feedback. We report here that DF’s grip scaling remained intact when her vision was completely suppressed during grasp movements, and it still dissociated sharply from her poor perceptual estimates of target size. We then tested whether providing trial-by-trial haptic feedback after making such perceptual estimates might improve DF’s performance, but found that they remained significantly impaired. In a final experiment, we re-examined whether DF’s grip scaling depends on receiving veridical haptic feedback during grasping. In one condition, the haptic feedback was identical to the visual targets, while in a second, the feedback was of a constant intermediate width while the visual target varied trial by trial. Despite such false feedback, DF still scaled her grip aperture to the visual widths of the target blocks, showing only normal adaptation to the false haptically-experienced width. Taken together, these results strengthen the view that DF’s spared grasping relies on a normal mode of dorsal-stream functioning, based chiefly on visual feedforward processing

DF's visual brain in action: the role of tactile cues

Patient DF, an extensively-tested woman with visual form agnosia from ventral-stream damage, is able to scale her grip aperture to match a goal object's geometry when reaching out to pick it up, despite being unable to explicitly distinguish amongst objects on the basis of their different geometries. Using evidence from a range of sources, including functional MRI, we have proposed that she does this through a functionally intact visuomotor system housed within the dorsal stream of the posterior parietal lobe. More recently, however, Schenk (2012a). The Journal of Neuroscience, 32(6), 2013–2017; Schenk (2012b). Trends in Cognitive Sciences, 16(5), 258–259. has argued that DF performs well in visually guided grasping, not through spared and functioning visuomotor networks in the dorsal stream, but because haptic feedback about the locations of the edges of the target is available to calibrate her grasps in such tasks, whereas it is not available in standard visual perceptual tasks. We have tested this 'calibration hypothesis' directly, by presenting DF with a grasping task in which the visible width of a target varied from trial to trial while its actual width remained the same. According to the calibration hypothesis, because haptic feedback was completely uninformative, DF should be unable to calibrate her grip aperture in this task. Contrary to this prediction, we found that DF continued to scale her grip aperture to the visual width of the targets and did so well within the range of healthy controls. We also found that DF's inability to distinguish shapes perceptually is not improved by providing haptic feedback. These findings strengthen the notion that DF’s spared visuomotor abilities are driven largely by visual feedforward processing of the geometric properties of the target. Crucially, these findings also indicate that simple tactile contact with an object is needed for the visuomotor dorsal stream to be engaged, and accordingly enables DF to execute visually guided grasping successfully. This need for actions to have a tangible endpoint provides an important new modification of the Two Visual Systems theory

Separate processing of texture and form in the ventral stream : evidence from fMRI and visual agnosia.

Real-life visual object recognition requires the processing of more than just geometric (shape, size, and orientation) properties. Surface properties such as color and texture are equally important, particularly for providing information about the material properties of objects. Recent neuroimaging research suggests that geometric and surface properties are dealt with separately, within the lateral occipital cortex (LOC) and the collateral sulcus (CoS), respectively. Here we compared objects that either differed in aspect ratio or in surface texture only, keeping all other visual properties constant. Results on brain-intact participants confirmed that surface texture activates an area in the posterior CoS, quite distinct from the area activated by shape within LOC. We also tested two patients with visual object agnosia, one of whom (DF) performed well on the texture task but at chance on the shape task, while the other (MS) showed the converse pattern. This behavioral double dissociation was matched by a parallel neuroimaging dissociation, with activation in CoS but not LOC in patient DF, and activation in LOC but not CoS in patient MS. These data provide presumptive evidence that the areas respectively activated by shape and texture play a causally necessary role in the perceptual discrimination of these features

Fast Visuomotor Processing of Redundant Targets: The Role of the Right Temporo-Parietal Junction

Parallel processing of multiple sensory stimuli is critical for efficient, successful interaction with the environment. An experimental approach to studying parallel processing in sensorimotor integration is to examine reaction times to multiple copies of the same stimulus. Reaction times to bilateral copies of light flashes are faster than to single, unilateral light flashes. These faster responses may be due to ‘statistical facilitation’ between independent processing streams engaged by the two copies of the light flash. On some trials, however, reaction times are faster than predicted by statistical facilitation. This indicates that a neural ‘coactivation’ of the two processing streams must have occurred. Here we use fMRI to investigate the neural locus of this coactivation. Subjects responded manually to the detection of unilateral light flashes presented to the left or right visual hemifield, and to the detection of bilateral light flashes. We compared the bilateral trials where subjects' reaction times exceeded the limit predicted by statistical facilitation to bilateral trials that did not exceed the limit. Activity in the right temporo-parietal junction was higher in those bilateral trials that showed coactivation than in those that did not. These results suggest the neural coactivation observed in visuomotor integration occurs at a cognitive rather than sensory or motor stage of processing

Accurate Visuomotor Control below the Perceptual Threshold of Size Discrimination

Background: Human resolution for object size is typically determined by psychophysical methods that are based on conscious perception. In contrast, grasping of the same objects might be less conscious. It is suggested that grasping is mediated by mechanisms other than those mediating conscious perception. In this study, we compared the visual resolution for object size of the visuomotor and the perceptual system. Methodology/Principal Findings: In Experiment 1, participants discriminated the size of pairs of objects once through perceptual judgments and once by grasping movements toward the objects. Notably, the actual size differences were set below the Just Noticeable Difference (JND). We found that grasping trajectories reflected the actual size differences between the objects regardless of the JND. This pattern was observed even in trials in which the perceptual judgments were erroneous. The results of an additional control experiment showed that these findings were not confounded by task demands. Participants were not aware, therefore, that their size discrimination via grasp was veridical. Conclusions/Significance: We conclude that human resolution is not fully tapped by perceptually determined thresholds

The Human Homologue of Macaque Area V6A

In macaque monkeys, V6A is a visuomotor area located in the anterior bank of the POs, dorsal and anterior to retinotopically-organized extrastriate area V6 (Galletti et al 1996). Unlike V6, V6A represents both contra- and ipsilateral visual fields and is broadly retinotopically organized (Galletti et al 1999b). The contralateral lower visual field is over-represented in V6A. The central 20°-30° of the visual field are mainly represented dorsally (V6Ad) and the periphery ventrally (V6Av), at the border with V6. Both sectors of area V6A contain arm movement-related cells, active during spatially-directed reaching movements (Gamberini et al., 2011). In humans, we previously mapped the retinotopic organization of area V6 (Pitzalis et al., 2006). Here, using phase-encoded fMRI, cortical surface-based analysis and wide-field retinotopic mapping, we define a new cortical region that borders V6 anteriorly and shows a clear over-representation of the contralateral lower visual field and of the periphery. As with macaque V6A, the eccentricity increases moving ventrally within the area. The new region contains a non-mirror-image representation of the visual field. Functional mapping reveals that, as in macaque V6A, the new region, but not the nearby area V6, responds during finger pointing and reaching movements. Based on similarity in position, retinotopic properties, functional organization and relationship with the neighbouring extrastriate visual areas, we propose that the new cortical region is the human homologue of macaque area V6A

Fix Your Eyes in the Space You Could Reach: Neurons in the Macaque Medial Parietal Cortex Prefer Gaze Positions in Peripersonal Space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping