Kenneth F. Valyear

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 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.

The involvement of the "fusiform face area" in processing facial expression.

We conducted an fMRI investigation to test the widely accepted notion that the fusiform face area (FFA) mediates the processing of facial identity but not expression. Participants attended either to the identity or to the expression of the same set of faces. If the processing of identity is neuroanatomically dissociable from that of expression, then one might expect the FFA to show higher activation when processing identity as opposed to expression. Contrary to this prediction, the FFA showed higher activation for judgments of expression. Furthermore, the FFA was sensitive to variations in expression even when attention was directed to identity. Finally, an independent observation showed higher activation in the FFA for passive viewing of faces when expression was varied as compared to when it remained constant. These findings suggest an interactive network for the processing of expression and identity, in which information about expression is computed from the unique structure of individual faces.

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.

Decoding the neural mechanisms of human tool use

Sophisticated tool use is a defining characteristic of the primate species but how is it supported by the brain, particularly the human brain? Here we show, using functional MRI and pattern classification methods, that tool use is subserved by multiple distributed action-centred neural representations that are both shared with and distinct from those of the hand. In areas of frontoparietal cortex we found a common representation for planned hand- and tool-related actions. In contrast, in parietal and occipitotemporal regions implicated in hand actions and body perception we found that coding remained selectively linked to upcoming actions of the hand whereas in parietal and occipitotemporal regions implicated in tool-related processing the coding remained selectively linked to upcoming actions of the tool. The highly specialized and hierarchical nature of this coding suggests that hand- and tool-related actions are represented separately at earlier levels of sensorimotor processing before becoming integrated in frontoparietal cortex. DOI: http://dx.doi.org/10.7554/eLife.00425.001

Observing learned object-specific functional grasps preferentially activates the ventral stream

In one popular account of the human visual system, two streams are distinguished, a ventral stream specialized for perception and a dorsal stream specialized for action. The skillful use of familiar tools, however, is likely to involve the cooperation of both streams. Using functional magnetic resonance imaging, we scanned individuals while they viewed short movies of familiar tools being grasped in ways that were either consistent or inconsistent with how tools are typically grasped during use. Typical-for-use actions were predicted to preferentially activate parietal areas important for tool use. Instead, our results revealed several areas within the ventral stream, as well as the left posterior middle temporal gyrus, as preferentially active for our typical-for-use actions. We believe these findings reflect sensitivity to learned semantic associations and suggest a special role for these areas in representing object-specific actions. We hypothesize that during actual tool use a complex interplay between the two streams must take place, with ventral stream areas providing critical input as to how an object should be engaged in accordance with stored semantic knowledge.

Orientation sensitivity to graspable objects: An fMRI adaptation study

It has been proposed that vision-for-perception and vision-for-action are subserved by distinct streams of visual processing, the ventral and dorsal stream, respectively [Milner, A. D., Goodale, M. A., 1995. The visual brain in action. Oxford University Press, Oxford]. Such a distinction has been supported by a recent functional magnetic resonance (fMR) adaptation study [Valyear, K. F., Culham, J. C., Sharif, N., Westwood, D., Goodale, M. A., 2006. A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: A human fMRI study. Neuropsychologia 44, 218-228], which demonstrated selectivity to object identity but not object orientation within the ventral stream, and selectivity to object orientation but not object identity within the dorsal stream. These results were interpreted as suggesting that changes to object identity (but not to orientation) would alter the representation of the stimulus in the perceptual/recognition system, whereas changes in object orientation (but not necessarily identity) would alter the coding of the stimulus within a visuomotor system concerned with behaviour such as grasping. If orientation sensitivity in the dorsal stream does reflect such a potential for action, then this sensitivity should be specific to graspable objects. Using an fMR adaptation paradigm, we presented participants with an image of either a graspable or non-graspable stimulus, followed by the same image in either the original orientation or its mirror image. One region within the dorsal stream, the lateral occipito-parietal junction (lOPJ), was shown to be sensitive to orientation changes for graspable stimuli; this region did not show orientation sensitivity for non-graspable stimuli. Thus, it appears that the sensitivity to orientation changes in this region is specific to graspable objects, presumably because such changes affect the affordances of graspable but not non-graspable objects.

The relationship between fMRI adaptation and repetition priming

Neuroimaging investigations of the cortically defined fMRI adaptation effect and of the behaviorally defined repetition priming effect have provided useful insights into how visual information is perceived and stored in the brain. Yet, although both phenomena are typically associated with reduced activation in visually responsive brain regions as a result of stimulus repetition, it is presently unknown whether they rely on common or dissociable neural mechanisms. In an event-related fMRI experiment, we manipulated fMRI adaptation and repetition priming orthogonally. Subjects made comparative size judgments for pairs of stimuli that depicted either the same or different objects; some of the pairs presented during scanning had been shown previously and others were new. This design allowed us to examine whether object-selective regions in occipital and temporal cortex were sensitive to adaptation, priming, or both. Critically, it also allowed us to test whether any region showing sensitivity to both manipulations displayed interactive or additive effects. Only a partial overlap was found between areas that were sensitive to fMRI adaptation and those sensitive to repetition priming. Moreover, in most of the object-selective regions that showed both effects, the reduced activation associated with the two phenomena were additive rather than interactive. Together, these findings suggest that fMRI adaptation and repetition priming can be dissociated from one another in terms of their neural mechanisms.

fMRI Repetition Suppression for Familiar But Not Arbitrary Actions with Tools

For humans, daily life is characterized by routine interaction with many different tools for which corresponding actions are specified and performed according to well-learned procedures. The current study used functional MRI (fMRI) repetition suppression (RS) to identify brain areas underlying the transformation of visually defined tool properties to corresponding motor programs for conventional use. Before grasping and demonstrating how to use a specific tool, participants passively viewed either the same (repeated) tool or a different (non-repeated) tool. Repetition of tools led to reduced fMRI signals (RS) within a selective network of parietal and premotor areas. Comparison with newly learned, arbitrarily defined control actions revealed specificity of RS for tool use, thought to reflect differences in the extent of previous sensorimotor experience. The findings indicate that familiar tools are visually represented within the same sensorimotor areas underlying their dexterous use according to learned properties defined by previous experience. This interpretation resonates with the broader concept of affordance specification considered fundamental to action planning and execution whereby action-relevant object properties (affordances) are visually represented in sensorimotor areas. The current findings extend this view to reveal that affordance specification in humans includes learned object properties defined by previous sensorimotor experience. From an evolutionary perspective, the neural mechanisms identified in the current study offer clear survival advantage, providing fast efficient transformation of visual information to appropriate motor responses based on previous experience.