Obtaining and maintaining cortical hand representation as evidenced from acquired and congenital handlessness

Wesselink, Daan B; Heiligenberg, Fiona M.Z. van den; Ejaz, Naveed; Dempsey-Jones, Harriet; Cardinali, Lucilla; Tarall-Jozwiak, Aurelie; Diedrichsen, Jörn; Makin, Tamar R.

doi:10.7554/elife.37227

Cited by 73 publications

(149 citation statements)

References 85 publications

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“…One would expect cortical remapping to occur in the case of spinal cord injury; however, current models of remapping predict that the immediately adjacent intact body parts (in this case face and head) should become more dominant (Qi, Stepniewska, and Kaas 2000). Instead, we found in participant T5 that arm and leg movements were more strongly represented than face and head movements, suggesting that the extent of remapping may be limited in precentral gyrus; consistent with this, a recent fMRI study also found limited motor cortical remapping in hand amputees (Wesselink et al 2019). The fact that we observed roughly the same proportions of modulation for face, head, arm and leg movements in participant T7, who had ALS, gives further confidence that the broad tuning we observed was not caused by remapping.…”

Section: Discussionsupporting

confidence: 88%

Hand Knob Area of Motor Cortex in People with Tetraplegia Represents the Whole Body in a Modular Way

Willett

Deo

Avansino

et al. 2019

Preprint

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24Decades after the motor homunculus was first proposed, it is still unknown how different body 25 parts are intermixed and interrelated in human motor cortex at single-neuron resolution. Using 26 microelectrode arrays, we studied how face, head, arm and leg movements on both sides of the 27 body are represented in hand knob area of precentral gyrus in people with tetraplegia. Contrary 28 to the traditional somatotopy, we found strong representation of all movements. Probing further, 29 we found that ipsilateral and contralateral movements, and homologous arm and leg 30 movements (e.g. wrist and ankle), had a correlated representation. Additionally, there were 31 neural dimensions where the limb was represented independently of the movement. Together, 32 these patterns formed a "modular" code that might facilitate skill transfer across limbs. We also 33 investigated dual-effector movement, finding that more strongly represented effectors 34 suppressed the activity of weaker effectors. Finally, we leveraged these results to improve 35 discrete brain-computer interfaces by spreading targets across all limbs. 42intermixing between widely distinct areas of the body within any one individual (Leyton and 43 Sherrington 1917; W. Penfield and Boldrey 1937; Wilder Penfield and Rasmussen 1950). fMRI 44 studies also support the existence of an orderly map with largely separate face, arm and leg 45 areas along the precentral gyrus and the anterior bank of the central sulcus (Lotze et al. 2000; computer interface (BCI) that can decode movements across all four limbs. We show that this 86 "full body" BCI improves information throughput relative to a single-effector approach. 87 Results 89Tuning to Face, Head, Arm and Leg Movements 90 91We used microelectrode array recordings from participants T5 and T7 to assess tuning to face, 92 head, arm and leg movements in hand knob area of precentral gyrus. Participant T5 had a C4 93 spinal cord injury and was paralyzed from the neck down; he could move his face and head, but 94 attempted arm and leg movements resulted in little or no overt motion. Participant T7 had ALS 95and could move all joints tested, although some of his arm movements were limited due to 96 weakness. 98In this experiment, T5 and T7 made (or attempted to make) movements in sync with visual cues 99 displayed on a computer screen ( Fig. 1A). T5 completed an instructed delay version of the task 100 where each trial randomly cued one of 32 possible movements spanning the face, head, arm 101 and legs. For face and head movements, T5 was instructed to move normally; for arm and leg 102 movements, T5 was instructed to attempt to make the movement as if he were not paralyzed. 103T7, whose more restricted data was collected earlier in a different study (and who is no longer 104 enrolled), completed an alternating paired movement task with a block design. Each block 105 tested a different movement pair, during which T7 alternated between making each of the paired 106 movements every 3 seconds. 108Despite recording from micr...

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Section: Discussionsupporting

confidence: 88%

Hand Knob Area of Motor Cortex in People with Tetraplegia Represents the Whole Body in a Modular Way

Willett

Deo

Avansino

et al. 2019

Preprint

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“…Traditionally, body representation in the sensorimotor cortex is considered to be highly adaptive even in the adult brain (26,27) however recent research contributes a new perspective on its malleability (12,13). Tools have been suggested to update the biological body representation, for example by tool-body integration (28)(29)(30).…”

Section: Discussionmentioning

confidence: 99%

“…It is highly consistent within (8) and across (9) participants and is preserved even after severe loss of motor functions due to e.g. stroke (9), spinal cord injury (10), disability (11) or even hand amputation (12)(13)(14). Hand representation has been suggested to reflect daily hand use (9), with studies showing that it may be altered under constrained circumstances.…”

Section: Introductionmentioning

confidence: 99%

Neurocognitive consequences of hand augmentation

Kieliba

Clode

Maimon-Mor

et al. 2020

Preprint

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From hand tools to cyborgs, humans have long been fascinated by the opportunities afforded by augmenting ourselves. Here, we studied how motor augmentation with an extra robotic thumb (the Third Thumb) impacts the biological hand representation in the brains of ablebodied people. Participants were tested on a variety of behavioural and neuroimaging tests designed to interrogate the augmented hand's representation before and after 5-days of semi-intensive training. Training improved the Thumb's motor control, dexterity and handrobot coordination, even when cognitive load was increased or when vision was occluded, and resulted in increased sense of embodiment over the robotic Thumb. Thumb usage also weakened natural kinematic hand synergies. Importantly, brain decoding of the augmented hand's motor representation demonstrated mild collapsing of the canonical hand structure following training, suggesting that motor augmentation may disrupt the biological hand representation. Together, our findings unveil critical neurocognitive considerations for designing human body augmentation.

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“…Digit somatotopy is characterised in neuroimaging by two main principles: 1) digit selectivity, meaning separable regions show increased responsiveness to one digit compared to all other digits , and 2) inter-digit overlap, where neighbouring digits are more overlapping in their representation than non-neighbouring digits (Ejaz et al, 2015). The features of these digits maps have been extensively studied separately using either active (Kikkert et al, 2016;Wesselink et al, 2019) or passive tasks (Martuzzi, van der Zwaag, Farthouat, Gruetter, & Blanke, 2014;Sanchez-Panchuelo et al, 2010;Schweizer, Voit, & Frahm, 2008). Recent work by Berlot and colleagues (2019) provided a comparison between active and passive tasks.…”

Section: Introductionmentioning

confidence: 99%

Similar somatotopy for active and passive digit representation in primary somatosensory cortex

Sanders

Wesselink

Dempsey-Jones

et al. 2019

Preprint

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Scientists traditionally use passive stimulation to examine organisational properties of the primary somatosensory cortex (SI). Recent research has, however, emphasised the close and bidirectional relationship between somatosensory and motor systems. This suggests active contributions (e.g., direct inputs from the motor system to SI) should also be considered when studying SI representations. Under such a framework, discrepant results are possible when different tasks are used to study the same underlying somatosensory representation. Here we examined whether SI hand representation is consistent when compared between active and passive tasks. Moreover, we ask whether this holds when task demands and stimulus properties are not directly matched. Using 7T fMRI, we examined three key digit representation features -spatial location, activity gradient profiles and multivariate representational structure. We show that although activity was increased overall in the active task, all key features of digit somatotopy were consistent over tasks, using both traditional univariate (activity-level) and multivariate (pattern structure) measurements. Despite overall comparability, when investigating fine-grained features of somatotopy using multivariate analysis, the active task was superior for individuating the representation across digits. We suggest that the information produced by an active task is more aligned with typical, ecologically relevant patterns of hand sensory input, resulting in more optimal SI activity patterns. Our findings validate the utilisation of active tasks for studying SI somatotopy.

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Obtaining and maintaining cortical hand representation as evidenced from acquired and congenital handlessness

Cited by 73 publications

References 85 publications

Hand Knob Area of Motor Cortex in People with Tetraplegia Represents the Whole Body in a Modular Way

Hand Knob Area of Motor Cortex in People with Tetraplegia Represents the Whole Body in a Modular Way

Neurocognitive consequences of hand augmentation

Similar somatotopy for active and passive digit representation in primary somatosensory cortex

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