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Scott H. Frey

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8 papers

1 author row

YNICL Journal 2023 Journal Article

Reorganization of sensorimotor representations of the intact limb after upper but not lower limb traumatic amputation

Michelle Marneweck
Cooper Gardner
Neil M. Dundon
Jolinda Smith
Scott H. Frey

It is becoming increasingly clear that limb loss induces wider spread reorganization of representations of the body that are nonadjacent to the affected cortical territory. Data from upper extremity amputees reveal intrusion of the representation of the ipsilateral intact limb into the former hand territory. Here we test for the first time whether this reorganization of the intact limb into the deprived cortex is specific to the neurological organization of the upper limbs or reflects large scale adaptation that is triggered by any unilateral amputation. BOLD activity was measured as human subjects with upper limb and lower limb traumatic amputation and their controls moved the toes on each foot, open and closed each hand and pursed their lips. Subjects with amputation were asked to imagine moving the missing limb while remaining still. Bayesian pattern component modeling of fMRI data showed that intact ipsilateral movements and contralateral movements of the hand and foot were distinctly represented in the deprived sensorimotor cortex years after upper limb amputation. In contrast, there was evidence reminiscent of contralateral specificity for hand and foot movements following lower limb amputation, like that seen in controls. We propose the cortical reorganization of the intact limb to be a function of use-dependent plasticity that is more specific to the consequence of upper limb loss of forcing an asymmetric reliance on the intact hand and arm. The contribution of this reorganization to phantom pain or a heightened risk of overuse and resultant maladaptive plasticity needs investigating before targeting such reorganization in intervention.

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YNIMG Journal 2020 Journal Article

Interhemispheric transfer of post-amputation cortical plasticity within the human somatosensory cortex

Kenneth F. Valyear
Benjamin A. Philip
Carmen M. Cirstea
Pin-Wei Chen
Nathan A. Baune
Noah Marchal
Scott H. Frey

Animal models reveal that deafferenting forelimb injuries precipitate reorganization in both contralateral and ipsilateral somatosensory cortices. The functional significance and duration of these effects are unknown, and it is unclear whether they also occur in injured humans. We delivered cutaneous stimulation during functional magnetic resonance imaging (fMRI) to map the sensory cortical representation of the intact hand and lower face in a group of chronic, unilateral, upper extremity amputees (N = 19) and healthy matched controls (N = 29). Amputees exhibited greater activity than controls within the deafferented former sensory hand territory (S1f) during stimulation of the intact hand, but not of the lower face. Despite this cortical reorganization, amputees did not differ from controls in tactile acuity on their intact hands. S1f responses during hand stimulation were unrelated to tactile acuity, pain, prosthesis usage, or time since amputation. These effects appeared specific to the deafferented somatosensory modality, as fMRI visual mapping paradigm failed to detect any differences between groups. We conclude that S1f becomes responsive to cutaneous stimulation of the intact hand of amputees, and that this modality-specific reorganizational change persists for many years, if not indefinitely. The functional relevance of these changes, if any, remains unknown.

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YNIMG Journal 2019 Journal Article

Grasping with a new hand: Improved performance and normalized grasp-selective brain responses despite persistent functional changes in primary motor cortex and low-level sensory and motor impairments

Kenneth F. Valyear
Daniela Mattos
Benjamin A. Philip
Christina Kaufman
Scott H. Frey

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.

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YNICL Journal 2018 Journal Article

It takes two to pantomime: Communication meets motor cognition

Lisa Finkel
Katharina Hogrefe
Scott H. Frey
Georg Goldenberg
Jennifer Randerath

For over a century, pantomime of tool use has been employed to diagnose limb apraxia, a disorder of motor cognition primarily induced by left brain damage. While research consistently implicates damage to a left fronto-temporo-parietal network in limb apraxia, findings are inconsistent regarding the impact of damage to anterior versus posterior nodes within this network on pantomime. Complicating matters is the fact that tool use pantomime can be affected and evaluated at multiple levels. For instance, the production of tool use gestures requires the consideration of semantic characteristics (e.g. how to communicate the action intention) as well as motor features (e.g. forming grip and movement). Together, these factors may contribute substantially to apparent discrepancies in previously reported findings regarding neural correlates of tool use pantomime. In the current study, 67 stroke patients with unilateral left-brain damage performed a classic pantomime task. In order to analyze different error characteristics, we evaluated the proper use of grip and movement for each pantomime. For certain objects, healthy subjects may use body parts as representative for the object, e.g. use of the fingers to indicate scissors blades. To specify the pathological use of body parts as the object (BPO) we only assessed pantomime items that were not prone to this response in healthy participants. We performed modern voxel-based lesion analyses on MRI or CT data to determine associations between brain injury and the frequency of the specific types of pantomime errors. Our results support a model in which anterior and posterior nodes of the left fronto-temporo-parietal network contribute differentially to pantomime of tool use. More precisely, damage in the inferior frontal cortex reaching to the temporal pole is associated with an increased frequency of BPO errors, whereas damage to the inferior parietal lobe is predominantly linked to an increased frequency of movement and/or grip errors. Our work suggests that the validity of attempts to specify the neural correlates of limb apraxia based on tool use pantomime depends on differentiating the specific types of errors committed. We conclude that successful tool use pantomime involves dissociable functions with communicative aspects represented in more anterior (rather ventral) regions and motor-cognitive aspects in more posterior (rather dorsal) nodes of a left fronto-temporo-parietal network.

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YNIMG Journal 2015 Journal Article

Human posterior parietal cortex mediates hand-specific planning

Kenneth F. Valyear
Scott H. Frey

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.

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YNIMG Journal 2014 Journal Article

Differential contributions of the superior and inferior parietal cortex to feedback versus feedforward control of tools

Kristen L. Macuga
Scott H. Frey

Damage to the superior and/or inferior parietal lobules (SPL, IPL) (Sirigu et al. , 1996) or cerebellum (Grealy and Lee, 2011) can selectively disrupt motor imagery, motivating the hypothesis that these regions participate in predictive (i. e. , feedforward) control. If so, then the SPL, IPL, and cerebellum should show greater activity as the demands on feedforward control increase from visually-guided execution (closed-loop) to execution without visual feedback (open-loop) to motor imagery. Using fMRI and a Fitts' reciprocal aiming task with tools directed at targets in far space, we found that the SPL and cerebellum exhibited greater activity during closed-loop control. Conversely, open-loop and imagery conditions were associated with increased activity within the IPL and prefrontal areas. These results are consistent with a superior-to-inferior gradient in the representation of feedback-to-feedforward control within the posterior parietal cortex. Additionally, the anterior SPL displayed greater activity when aiming movements were performed with a stick vs. laser pointer. This may suggest that it is involved in the remapping of far into near (reachable) space (Maravita and Iriki, 2004), or in distalization of the end-effector from hand to stick (Arbib et al. , 2009).

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YNIMG Journal 2012 Journal Article

Neural representations involved in observed, imagined, and imitated actions are dissociable and hierarchically organized

Kristen L. Macuga
Scott H. Frey

The fact that action observation, motor imagery and execution are associated with partially overlapping increases in parieto-frontal areas has been interpreted as evidence for reliance of these behaviors on a common system of motor representations. However, studies that include all three conditions within a single paradigm are rare, and consequently, there is a dearth of knowledge concerning the distinct mechanisms involved in these functions. Here we report key differences in neural representations subserving observation, imagery, and synchronous imitation of a repetitive bimanual finger-tapping task using fMRI under conditions in which visual stimulation is carefully controlled. Relative to rest, observation, imagery, and synchronous imitation are all associated with widespread increases in cortical activity. Importantly, when effects of visual stimulation are properly controlled, each of these conditions is found to have its own unique neural signature. Relative to observation or imagery, synchronous imitation shows increased bilateral activity along the central sulcus (extending into precentral and postcentral gyri), in the cerebellum, supplementary motor area (SMA), parietal operculum, and several motor-related subcortical areas. No areas show greater increases for imagery vs. synchronous imitation; however, relative to synchronous imitation, observation is associated with greater increases in caudal SMA activity than synchronous imitation. Compared to observation, imagery increases activation in pre-SMA and left inferior frontal cortex, while no areas show the inverse effect. Region-of-interest (ROI) analyses reveal that areas involved in bimanual open-loop movements respond most to synchronous imitation (primary sensorimotor, classic SMA, and cerebellum), and less vigorously to imagery and observation. The differential activity between conditions suggests an alternative hierarchical model in which these behaviors all rely on partially independent mechanisms.

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YNIMG Journal 2011 Journal Article

Handedness-dependent and -independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning

Kimberley Martin
Stéphane Jacobs
Scott H. Frey

When planning grasping actions, right-handers show left-lateralized responses in the anterior intraparietal sulcus (aIPS) and ventral premotor cortex (vPMC), two areas that are also implicated in sensorimotor control of grasp. We investigated whether a similar cerebral asymmetry is evident in strongly left-handed individuals. Fourteen participants were trained to grasp an object appearing in a variety of orientations with their left and right hands and with a novel mechanical tool (operated with either hand). BOLD fMRI data were then acquired while they decided prospectively whether an over- or under-hand grip would be most comfortable for grasping the same stimulus set while remaining still. Behavioral performances were equivalent to those recorded previously in right-handers and indicated reliance on effector-specific internal representations. In left-handers, however, grip selection decisions for both sides (left, right) and effectors (hand, tool) were associated with bilateral increases in activity within aIPS and vPMC. A direct comparison between left- and right-handers did reveal equivalent increases in left vPMC regardless of hand dominance. By contrast, aIPS and right vPMC activity were dependent on handedness, showing greater activity in the motor-dominant hemisphere. Though showing bilateral increases in both left- and right-handers, greater increases in the motor dominant hemisphere were also detected in the caudal IPS (cIPS), superior parietal lobule (SPL) and dorsal premotor cortex (dPMC). These findings provide further evidence that regions involved in the sensorimotor control of grasp also participate in grasp planning, and that for certain areas hand dominance is a predictor of the cerebral organization of motor cognitive functions.

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