Ken Valyear | Bangor University (original) (raw)

Papers by Ken Valyear

Highlights - We provide the first functional brain data of grasping with a transplanted hand. ... more Highlights

- We provide the first functional brain data of grasping with a transplanted hand.
- Normative grasp kinematics parallel normative grasp-selective fMRI responses.
- Grasp recovers despite persistent low-level deficits and changes in motor cortex.
- Grasp and its normative brain organization are restored after hand transplantation.

ABSTRACT

Hand loss can now be reversed through surgical transplantation years or decades after amputation. Remarkably, these patients come to use their new hand to skilfully grasp and manipulate objects. The brain mechanisms that make this possible are unknown. Here we test the hypothesis that the anterior intraparietal cortex (aIPC) – a multimodal region implicated in hand preshaping and error correction during grasping – plays a key role in this compensatory grasp control. Motion capture and fMRI are used to characterize hand kinematics and brain responses during visually guided grasping with a transplanted hand at 26 and 41 months post-transplant in patient DR, a former hand amputee of 13 years. Compared with matched controls, DR shows increasingly normal grasp kinematics paralleled by increasingly robust grasp-selective fMRI responses within the very same brain areas that show grasp-selectivity in controls, including the aIPC, premotor and cerebellar cortices. Paradoxically, over this same time DR exhibits significant limitations in basic sensory and motor functions, and persistent amputation-related functional reorganization of primary motor cortex. Movements of the non-transplanted hand positively activate the ipsilateral primary motor hand area – a functional marker of persistent interhemispheric amputation-related reorganization. Our data demonstrate for the first time that even after more than a decade of living as an amputee the normative functional brain organization governing the control of grasping can be restored. We propose that the aIPC and interconnected premotor and cerebellar cortices enable grasp normalization by compensating for the functional impact of reorganizational changes in primary sensorimotor cortex and targeting errors in regenerating peripheral nerves.

New findings advance our understanding of how vision is used to guide the hand during object gras... more New findings advance our understanding of how vision is used to guide the hand during object grasping.

Neuropsychologia, 2006

'The fusiform face area is not sucient for face recognition : evidence from a patient with ... more 2006) 'The fusiform face area is not sucient for face recognition : evidence from a patient with dense prosopagnosia and no occipital face area. ', Neuropsychologia., 44 (4). pp. 594-609.

Journal of Vision, 2010

Abstract We used anatomical and functional magnetic resonance imaging (fMRI) at 4 Tesla to examin... more Abstract We used anatomical and functional magnetic resonance imaging (fMRI) at 4 Tesla to examine the damaged and spared brain regions in Patient MC, a 38-year old woman with Riddoch phenomenon-awareness of moving but not static stimuli. Anatomical scans indicated extensive damage to occipitotemporal cortex bilaterally and right posterior parietal cortex. Within occipital cortex, the only spared and visually active region was a small portion of the anterior calcarine cortex bilaterally. The expected location of the lateral occipital ...

NeuroImage, 2015

The processes underlying action planning are fundamental to adaptive behavior and can be influenc... more The processes underlying action planning are fundamental to adaptive behavior and can be influenced by recent motor experience. Here, we used a novel fMRI Repetition Suppression (RS) design to test the hypotheses that action planning unfolds more efficiently for successive actions made with the same hand. More efficient processing was predicted to correspond with both faster response times (RTs) to initiate actions and reduced fMRI activity levels -RS. Consistent with these predictions, we detected faster RTs for actions made with the same hand and accompanying fMRI-RS within bilateral posterior parietal cortex and right-lateralized parietal operculum. Within posterior parietal cortex, these RS effects were localized to intraparietal and superior parietal cortices. These same areas were more strongly activated for actions involving the contralateral hand. The findings provide compelling new evidence for the specification of action plans in hand-specific terms, and indicate that these processes are sensitive to recent motor history. Consistent with computational efficiency accounts of motor history effects, the findings are interpreted as evidence for comparatively more efficient processing underlying action planning when successive actions involve the same versus opposite hand.

Psychonomic Bulletin & Review, 2013

Action selection processes such as those that underlie decisions about which hand to use for upco... more Action selection processes such as those that underlie decisions about which hand to use for upcoming actions are fundamental to adaptive motor behavior. Previous research has shown that people grasp objects in ways that reflect anticipated task demands, as well as recent movement experience. However, very few studies have addressed the possible influence of recent motor history on hand selection. In the present study, participants grasped and placed objects using either their left or right hand. The results showed shorter response times to initiate successive actions when hand was repeated, even when those actions involved distinct grasp postures and object placement movements to distinct locations. Conversely, no such planning advantage was observed for repeated grasps for successive actions made with opposite hands. The findings are consistent with the idea that choices about which hand to use in the present are influenced by which hand was used in the recent past. When the same hand can be used for successive actions, planning is made more efficient, presumably because the motor parameters that specify which hand to use can be recalled from recent memory rather than formulated anew. The findings indicate that hand selection is sensitive to recent movement experience and provide novel support for computational efficiency accounts of motor history effects.

eLife, 2013

Sophisticated tool use is a defining characteristic of the primate species but how is it supporte... more 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.

Journal of Neuroscience, 2012

For humans, daily life is characterized by routine interaction with many different tools for whic... more 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.

Experimental Brain Research, 2011

How we interact with objects depends on what we intend to do with them. In the current work, we s... more How we interact with objects depends on what we intend to do with them. In the current work, we show that priming and the kinematics of grasping depend on the goals of grasping, as well as the context in which tasks are presented. We asked participants to grasp familiar kitchen tools in order to either move them, grasp-to-move (GTM), or to demonstrate their common use, grasp-to-use (GTU). When tasks were blocked separately (Experiment 1), we found that priming was only evident for the GTU task. However, when tasks were presented in the same block of trials (Experiment 2), we observed priming for both tasks. Independent of priming, differences in kinematics and reaction times according to task were evident for both Experiments. Longer reaction times for the GTU task indicate more extensive planning, and differences in grasping reflect the characteristics of subsequent actions. Priming of real grasping is determined by task goals as well as task setting, both of which are likely to modulate how object features (affordances) are perceived and influence the planning of future actions.

Journal of Neuroscience, 2011

How and where in the human brain high-level sensorimotor processes such as intentions and decisio... more How and where in the human brain high-level sensorimotor processes such as intentions and decisions are coded remain important yet essentially unanswered questions. This is in part because, to date, decoding intended actions from brain signals has been primarily constrained to invasive neural recordings in nonhuman primates. Here we demonstrate using functional MRI (fMRI) pattern recognition techniques that we can also decode movement intentions from human brain signals, specifically object-directed grasp and reach movements, moments before their initiation. Subjects performed an event-related delayed movement task toward a single centrally located object (consisting of a small cube attached atop a larger cube). For each trial, after visual presentation of the object, one of three hand movements was instructed: grasp the top cube, grasp the bottom cube, or reach to touch the side of the object (without preshaping the hand). We found that, despite an absence of fMRI signal amplitude differences between the planned movements, the spatial activity patterns in multiple parietal and premotor brain areas accurately predicted upcoming grasp and reach movements. Furthermore, the patterns of activity in a subset of these areas additionally predicted which of the two cubes were to be grasped. These findings offer new insights into the detailed movement information contained in human preparatory brain activity and advance our present understanding of sensorimotor planning processes through a unique description of parieto-frontal regions according to the specific types of hand movements they can predict.

Journal of Cognitive Neuroscience, 2010

■ In one popular account of the human visual system, two streams are distinguished, a ventral str... more ■ 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 impor-tant 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 objectspecific 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. ■

Journal of Cognitive Neuroscience, 2010

■ When exposed to novel dynamical conditions (e.g., externally imposed forces), neurologically in... more ■ When exposed to novel dynamical conditions (e.g., externally imposed forces), neurologically intact subjects easily adjust motor commands on the basis of their own reaching errors. Subjects can also benefit from visual observation of othersʼ kinematic errors. Here, using fMRI, we scanned subjects watching movies depicting another person learning to reach in a novel dynamic environment created by a robotic device. Passive observation of reaching movements (whether or not they were perturbed by the robot) was associated with increased activation in fronto-parietal re-gions that are normally recruited in active reaching. We found significant clusters in parieto-occipital cortex, intraparietal sulcus, as well as in dorsal premotor cortex. Moreover, it appeared that part of the network that has been shown to be engaged in processing self-generated reach error is also involved in observing reach errors committed by others. Specifically, activity in left intraparietal sulcus and left dorsal premotor cortex, as well as in right cerebellar cortex, was modulated by the amplitude of observed kinematic errors. ■

NeuroImage, 2007

Neuroimaging investigations reliably describe a left-lateralized network of areas as underlying t... more Neuroimaging investigations reliably describe a left-lateralized network of areas as underlying the representations of knowledge about familiar tools. Among the critical 'nodes' of the network, an area centered within the left intraparietal sulcus (IPS) is thought to be related to the motoric representations associated with familiar tools and their usage. This area is in the vicinity of an area implicated in the control of object-directed grasping actions: the anterior intraparietal area, AIP. The current study aimed to evaluate whether this toolrelated intraparietal activity could be accounted for by the graspable nature of tools or whether it was due to additional factors such as the functionality of tools. First, we found that during a naming task activation within a discrete region of the left anterior intraparietal cortex was higher for tools than for graspable objects, but did not differ between graspable and non-graspable objects. In addition, the peak activity associated with tool naming was found to be largely distinct and consistently posterior to that associated with real object grasping. A separate region, anterior to the tool-selective focus and possibly overlapping with AIP, demonstrated weak selectivity for both tools and graspable objects relative to non-graspable objects.

NeuroImage, 2007

It has been proposed that vision-for-perception and vision-for-action are subserved by distinct s... more 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.

Current Opinion in Neurobiology, 2006

Experiments using functional neuroimaging and transcranial magnetic stimulation in humans have re... more 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.

NeuroImage, 2006

Neuroimaging investigations of the cortically defined fMRI adaptation effect and of the behaviora... more 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 objectselective 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. D

Journal of Neuroscience, 2006

In the present study, we aimed to dissociate the neural correlates of two subprocesses involved i... more 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).

Neuropsychologia, 2006

We tested functional activation for faces in patient D.F., who following acquired brain damage ha... more 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.

Neuropsychologia, 2006

We used an event-related fMR-adaptation paradigm to investigate changes in BOLD activity in the d... more 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.

Neuropsychologia, 2005

We conducted an fMRI investigation to test the widely accepted notion that the fusiform face area... more 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.

Highlights - We provide the first functional brain data of grasping with a transplanted hand. ... more Highlights

ABSTRACT

Neuropsychologia, 2006

'The fusiform face area is not sucient for face recognition : evidence from a patient with ... more 2006) 'The fusiform face area is not sucient for face recognition : evidence from a patient with dense prosopagnosia and no occipital face area. ', Neuropsychologia., 44 (4). pp. 594-609.

Journal of Vision, 2010

NeuroImage, 2015

Psychonomic Bulletin & Review, 2013

eLife, 2013

Journal of Neuroscience, 2012

Experimental Brain Research, 2011

Journal of Neuroscience, 2011

Journal of Cognitive Neuroscience, 2010

NeuroImage, 2007

Current Opinion in Neurobiology, 2006

NeuroImage, 2006

Journal of Neuroscience, 2006

Neuropsychologia, 2006

Neuropsychologia, 2005

Tool use is essential and culturally universal to human life, common to huntergatherer and modern... more Tool use is essential and culturally universal to human life, common to huntergatherer and modern advanced societies alike. Although the neuroscience of simpler visuomotor behaviours like reaching and grasping have been studied extensively, relatively little is known about the brain mechanisms underlying learned tool use.