Jody C. Culham

Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas

Although both reaching and grasping require transporting the hand to the object location, only grasping also requires processing of object shape, size and orientation to preshape the hand. Behavioural and neuropsychological evidence suggests that the object processing required for grasping relies on different neural substrates from those mediating object recognition. Specifically, whereas object recognition is believed to rely on structures in the ventral (occipitotemporal) stream, object grasping appears to rely on structures in the dorsal (occipitoparietal) stream. We used functional magnetic resonance imaging (fMRI) to determine whether grasping (compared to reaching) produced activation in dorsal areas, ventral areas, or both. We found greater activity for grasping than reaching in several regions, including anterior intraparietal (AIP) cortex. We also performed a standard object perception localizer (comparing intact vs. scrambled 2D object images) in the same subjects to identify the lateral occipital complex (LOC), a ventral stream area believed to play a critical role in object recognition. Although LOC was activated by the objects presented on both grasping and reaching trials, there was no greater activity for grasping compared to reaching. These results suggest that dorsal areas, including AIP, but not ventral areas such as LOC, play a fundamental role in computing object properties during grasping.

Human parietal cortex in action

Experiments using functional neuroimaging and transcranial magnetic stimulation in humans have revealed regions of the parietal lobes that are specialized for particular visuomotor actions, such as reaching, grasping and eye movements. In addition, the human parietal cortex is recruited by processing and perception of action-related information, even when no overt action occurs. Such information can include object shape and orientation, knowledge about how tools are employed and the understanding of actions made by other individuals. We review the known subregions of the human posterior parietal cortex and the principles behind their organization.

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.

Attention Response Functions: Characterizing Brain Areas Using fMRI Activation during Parametric Variations of Attentional Load

We derived attention response functions for different cortical areas by plotting neural activity (measured by fMRI) as a function of attentional load in a visual tracking task. In many parietal and frontal cortical areas, activation increased with load over the entire range of loads tested, suggesting that these areas are directly involved in attentional processes. However, in other areas (FEF and parietal area 7), strong activation was observed even at the lowest attentional load (compared to a passive baseline using identical stimuli), but little or no additional activation was seen with increasing load. These latter areas appear to play a different role, perhaps supporting task-relevant functions that do not vary with load, such as the suppression of eye movements.

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.

The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area.

We tested functional activation for faces in patient D.F., who following acquired brain damage has a profound deficit in object recognition based on form (visual form agnosia) and also prosopagnosia that is undocumented to date. Functional imaging demonstrated that like our control observers, D.F. shows significantly more activation when passively viewing face compared to scene images in an area that is consistent with the fusiform face area (FFA) (p < 0.01). Control observers also show occipital face area (OFA) activation; however, whereas D.F.s lesions appear to overlap the OFA bilaterally. We asked, given that D.F. shows FFA activation for faces, to what extent is she able to recognize faces? D.F. demonstrated a severe impairment in higher level face processing--she could not recognize face identity, gender or emotional expression. In contrast, she performed relatively normally on many face categorization tasks. D.F. can differentiate faces from non-faces given sufficient texture information and processing time, and she can do this is independent of color and illumination information. D.F. can use configural information for categorizing faces when they are presented in an upright but not a sideways orientation and given that she also cannot discriminate half-faces she may rely on a spatially symmetric feature arrangement. Faces appear to be a unique category, which she can classify even when she has no advance knowledge that she will be shown face images. Together, these imaging and behavioral data support the importance of the integrity of a complex network of regions for face identification, including more than just the FFA--in particular the OFA, a region believed to be associated with low-level processing.

A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams : A human fMRI study

We used an event-related fMR-adaptation paradigm to investigate changes in BOLD activity in the dorsal and ventral visual streams as a function of object identity and object orientation. Participants viewed successive paired images of real-world, graspable objects, separated by a visual mask. The second image of each pair was either: (i) the same as the first image, (ii) different only in identity, (iii) different only in orientation, or (iv) different in both identity and orientation. A region in the parieto-occipital cortex (dorsal stream) showed a selective increase in BOLD activity with changes in object orientation, but was insensitive to changes in object identity. In contrast, a region in the temporo-occipital cortex (ventral stream) showed a selective increase in activity with changes in identity, but was insensitive to changes in orientation. The differential sensitivity to orientation and identity is consistent with the idea that the dorsal stream plays a critical role in the visual control of object-directed actions while the ventral stream plays a critical role in object perception.

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.

Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach

According to Milner and Goodales theory of the two visual streams, the dorsal (action) stream controls actions in real-time, whereas the ventral (perceptual) stream stores longer-term information for object identification. By this account, the dorsal stream subserves actions carried out immediately. However, when a delay is required before the response, the ventral (perceptual) stream is recruited. Indeed, a neuroimaging study from our lab has found reactivation of an area within the ventral stream, the lateral occipital (LO) cortex, at the time of action even when no visual stimulus was present. To tease apart the contribution of specific areas within the dorsal and ventral streams to the online control of grasping under immediate and delayed conditions, we used transcranial magnetic stimulation (TMS) to the anterior intraparietal sulcus (aIPS) and to LO. We show that while TMS to aIPS affected grasp under both immediate and delayed conditions, TMS to LO influenced grasp only under delayed movement conditions. The effects of TMS were restricted to early movement kinematics (i.e. within 300 ms) due to the transient nature of TMS, which was always delivered simultaneous with movement onset. We discuss the implications of our findings in relation to interactions between the dorsal and ventral streams.