Cristiana Cavina-Pratesi

The role of parietal cortex in visuomotor control : What have we learned from neuroimaging?

Research from macaque neurophysiology and human neuropsychology has implicated the parietal cortex in the sensory control of action. Functional neuroimaging has been very valuable in localizing and characterizing specific regions of the human brain involved in visuomotor actions involving different effectors, such as the eyes, head, arms and hands. Here, we review the areas discovered by human neuroimaging, including the putative functional equivalents of the following macaque regions: parietal eye fields (PEF), ventral intraparietal (VIP) area, parietal reach region (PRR) and the anterior intraparietal (AIP) area. We discuss the challenges of studying realistic movements in the imaging environment, the lateralization of visuomotor function, caveats involved in proposing interspecies homologies and the limitations and future directions for neuroimaging studies of visuomotor control.

Functional Magnetic Resonance Imaging Reveals the Neural Substrates of Arm Transport and Grip Formation in Reach-to-Grasp Actions in Humans

Picking up a cup requires transporting the arm to the cup (transport component) and preshaping the hand appropriately to grasp the handle (grip component). Here, we used functional magnetic resonance imaging to examine the human neural substrates of the transport component and its relationship with the grip component. Participants were shown three-dimensional objects placed either at a near location, adjacent to the hand, or at a far location, within reach but not adjacent to the hand. Participants performed three tasks at each location as follows: (1) touching the object with the knuckles of the right hand; (2) grasping the object with the right hand; or (3) passively viewing the object. The transport component was manipulated by positioning the object in the far versus the near location. The grip component was manipulated by asking participants to grasp the object versus touching it. For the first time, we have identified the neural substrates of the transport component, which include the superior parieto-occipital cortex and the rostral superior parietal lobule. Consistent with past studies, we found specialization for the grip component in bilateral anterior intraparietal sulcus and left ventral premotor cortex; now, however, we also find activity for the grasp even when no transport is involved. In addition to finding areas specialized for the transport and grip components in parietal cortex, we found an integration of the two components in dorsal premotor cortex and supplementary motor areas, two regions that may be important for the coordination of reach and grasp.

Redundant target effect and intersensory facilitation from visual-tactile interactions in simple reaction time

In a simple reaction time (RT) task, normal observers responded faster to simultaneous visual and tactile stimuli than to single visual or tactile stimuli. RT to simultaneous visual and tactile stimuli was also faster than RT to simultaneous dual visual or tactile stimuli. The advantage for RT to combined visual-tactile stimuli over RT to the other types of stimulation could be accounted for by intersensory neural facilitation rather than by probability summation. The direction of gaze (and presumably of visual attention) to space regions near to or far from the site of tactile stimulation had no effect on tactile RT. However, RT to single or dual tactile stimuli was fastest when observers could see the sites of tactile stimulation on their hands both directly and through a mirror at the same time. All these effects can be ascribed to the convergence of tactile and visual inputs onto neural centers which contain flexible multimodal representations of body parts.

Is That within Reach? fMRI Reveals That the Human Superior Parieto-Occipital Cortex Encodes Objects Reachable by the Hand

Macaque neurophysiology and human neuropsychology results suggest that parietal cortex encodes a unique representation of space within reach of the arm. Here, we used slow event-related functional magnetic resonance imaging (fMRI) to investigate whether human brain areas involved in reaching are more activated by objects within reach versus beyond reach. In experiment 1, graspable objects were placed at three possible locations on a platform: two reachable locations and one beyond reach. On some trials, participants reached to touch or grasp objects at the reachable location; on other trials participants passively viewed objects at one of the three locations. A reach-related area in the superior parieto-occipital cortex (SPOC) was more activated for targets within reach than beyond. In experiment 2, we investigated whether this SPOC response occurred when visual and motor confounds were controlled and whether it was modulated when a tool extended the effective range of the arm. On some trials, participants performed grasping and reaching actions to a reachable object location using either the hand alone or a tool; on other trials, participants passively viewed reachable and unreachable object locations. SPOC was significantly more active for passively viewed objects within reach of the hand versus beyond reach, regardless of whether or not a tool was available. Interestingly, these findings suggest that neural responses within brain areas coding actions (such as SPOC for reaching) may reflect automatic processing of motor affordances (such as reachability with the hand).

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.

Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex

The perception of object-directed actions performed by either hands or tools recruits regions in left fronto-parietal cortex. Here, using functional MRI (fMRI), we tested whether the common role of hands and tools in object manipulation is also reflected in the distribution of response patterns to these categories in visual cortex. In two experiments we found that static pictures of hands and tools activated closely overlapping regions in left lateral occipitotemporal cortex (LOTC). Left LOTC responses to tools selectively overlapped with responses to hands but not with responses to whole bodies, nonhand body parts, other objects, or visual motion. Multivoxel pattern analysis in left LOTC indicated a high degree of similarity between response patterns to hands and tools but not between hands or tools and other body parts. Finally, functional connectivity analysis showed that the left LOTC hand/tool region was selectively connected, relative to neighboring body-, motion-, and object-responsive regions, with regions in left intraparietal sulcus and left premotor cortex that have previously been implicated in hand/tool action-related processing. Taken together, these results suggest that action-related object properties shared by hands and tools are reflected in the organization of high-order visual cortex. We propose that the functional organization of high-order visual cortex partly reflects the organization of downstream functional networks, such as the fronto-parietal action network, due to differences within visual cortex in the connectivity to these networks.

Dissociable Neural Responses to Hands and Non-Hand Body Parts in Human Left Extrastriate Visual Cortex

Accumulating evidence points to a map of visual regions encoding specific categories of objects. For example, a region in the human extrastriate visual cortex, the extrastriate body area (EBA), has been implicated in the visual processing of bodies and body parts. Although in the monkey, neurons selective for hands have been reported, in humans it is unclear whether areas selective for individual body parts such as the hand exist. Here, we conducted two functional MRI experiments to test for hand-preferring responses in the human extrastriate visual cortex. We found evidence for a hand-preferring region in left lateral occipitotemporal cortex in all 14 participants. This region, located in the lateral occipital sulcus, partially overlapped with left EBA, but could be functionally and anatomically dissociated from it. In experiment 2, we further investigated the functional profile of hand- and body-preferring regions by measuring responses to hands, fingers, feet, assorted body parts (arms, legs, torsos), and non-biological handlike stimuli such as robotic hands. The hand-preferring region responded most strongly to hands, followed by robotic hands, fingers, and feet, whereas its response to assorted body parts did not significantly differ from baseline. By contrast, EBA responded most strongly to body parts, followed by hands and feet, and did not significantly respond to robotic hands or fingers. Together, these results provide evidence for a representation of the hand in extrastriate visual cortex that is distinct from the representation of other body parts.

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 differed either 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 2 patients with visual object agnosia, one of whom (DF) performed well on the texture task but at chance on the shape task, whereas 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.

Dissociating Arbitrary Stimulus-Response Mapping from Movement Planning during Preparatory Period: Evidence from Event-Related Functional Magnetic Resonance Imaging

In the present study, we aimed to dissociate the neural correlates of two subprocesses involved in the preparatory period in the context of arbitrary, prelearned stimulus-response (S-R) associations, namely, S-R mapping and movement planning (MP). We teased apart these two subprocesses by comparing three tasks in which the complexity of both S-R mapping and MP were independently manipulated: simple reaction time (SRT) task, go/no-go reaction time (GNGRT) task, and choice reaction time (CRT) task. We found that a more complex S-R mapping, which is the common element differentiating CRT and GNGRT from SRT, was associated with higher brain activation in the left superior parietal lobe (SPL). Conversely, a greater number of planned finger movements, which is the common difference between CRT and both SRT and GNGRT, was associated with higher brain activation in a number of frontal areas, including the left supplementary motor area (SMA), left dorsal premotor cortex (dPM), and left anterior cingulate cortex (ACC). The left-hemisphere dominance for S-R mapping could be related to the fact that arbitrary S-R mapping is often verbally mediated in humans. Overall, these results suggest a clear dissociation in the preparatory-set period between the more abstract role of left SPL in activating the appropriate S-R associations and the more concrete role played by the SMA, dPM, and ACC in preparing the required motor programs.