Alterations in Motor Cortical Representation of Muscles Following Incomplete Spinal Cord Injury in Humans

Fassett, Hunter J.; Turco, Claudia V.; El-Sayes, Jenin; Nelson, Aimee J.

doi:10.3390/brainsci8120225

Cited by 8 publications

(9 citation statements)

References 39 publications

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“…These studies demonstrated that the representations of less impaired muscles shift and expand following a complete or incomplete SCI, whereas representations of more impaired muscles retract or are absent. 14,71–75 However, our fMRI results showed that SCI patients had a similar level of finger-related movement activity in M1 as controls, and preserved somatotopic hand representations in S1. It is possible that reorganisation and preservation of the original function could co-occur within cortical areas.…”

Section: Discussionmentioning

confidence: 59%

Finger somatotopy is preserved after tetraplegia but deteriorates over time

Kikkert

Pfyffer

Verling

et al. 2021

Preprint

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Following spinal cord injury (SCI), the motor output flow to the limb(s) and sensory input to the brain is largely lost. While attempted movements with the paralysed and sensory deprived body part can still evoke signals in the sensorimotor system, this task-related 'net' brain activity of SCI patients differs substantially from healthy controls. Such reorganised and/or altered activity is thought to reflect abnormal processing. It is however possible that this altered net sensorimotor activity in SCI patients conceals preserved somatotopically-specific representations of the paralysed and sensory deprived body parts that could be exploited in a functionally meaningful manner (e.g. via neuroprosthetics). In this cross-sectional study, we investigated whether a functional connection between the periphery and the brain is necessary to maintain somatosensory representations. We used functional MRI and an (attempted) finger movement task to characterise the somatotopic hand layout in the primary somatosensory cortex and structural MRI to assess spared spinal tissue bridges. We tested 14 tetraplegic SCI patients (mean age, s.e.m.=55, 3.6; 1 female) who differed in terms of lesion completeness, retained sensorimotor functioning, and time since injury, as well as 18 healthy control participants (mean age, s.e.m.=56, 3.6 years; 1 female). Our results revealed somatotopically organised representations of patients' hands in which neighbouring clusters showed selectivity for neighbouring fingers in contralateral S1, qualitatively similar to those observed in healthy controls. To quantify whether these representations were normal in tetraplegic SCI patients we correlated each participant's intricate representational distance pattern across all fingers (revealed using representational similarity analysis) with a canonical inter-finger distance pattern obtained from an independent sample. The resulting hand representation typicality scores were not significantly different between patients and controls. This was even true when considering two individual patients with no sensory hand functioning, no hand motor functioning, and no spared spinal tissue bridges. However, a correlational analysis revealed that over years since SCI the hand representation typicality in primary somatosensory cortex deteriorates. We show that somatosensory representations can be maintained for several years following SCI even in the absence of perhiperhal inputs. Such preserved cortical hand representations could therefore be exploited in a functionally meaningful way by rehabilitation approaches that attempt to establish new functional connections between the hand and the brain after an SCI (e.g. through neuroprosthetics). However, time since injury may critically influence the somatotopic representations of SCI patients and might thereby impact the success of such rehabilitation approaches.

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Section: Discussionmentioning

confidence: 59%

Finger somatotopy is preserved after tetraplegia but deteriorates over time

Kikkert

Pfyffer

Verling

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…TMS studies similarly induce current in localised areas of M1 to induce a peripheral muscle response of cortically neighbouring body parts. These studies demonstrated that the representations of less impaired muscles shift and expand following a complete or incomplete SCI ( Fassett et al, 2018 ; Freund et al, 2011a ; Levy et al, 1990 ; Streletz et al, 1995 ; Topka et al, 1991 ; Urbin et al, 2019 ). Our fMRI results showed that tetraplegic patients had a preserved somatotopic hand representation in S1, though this deteriorated over time.…”

Section: Discussionmentioning

confidence: 92%

“…Transcranial magnetic stimulation (TMS) studies induced current in localised areas of SCI patients’ primary motor cortex (M1) to induce a peripheral muscle response. They found that representations of more impaired muscles retract or are absent while representations of less impaired muscles shift and expand ( Fassett et al, 2018 ; Freund et al, 2011a ; Levy et al, 1990 ; Streletz et al, 1995 ; Topka et al, 1991 ; Urbin et al, 2019 ). Similarly, human fMRI studies have shown that cortically neighbouring body part representations can shift towards, though do not invade, the deprived M1 and S1 cortex ( Freund et al, 2011b ; Henderson et al, 2011 ; Jutzeler et al, 2015 ; Wrigley et al, 2018 ; Wrigley et al, 2009 ).…”

Section: Introductionmentioning

confidence: 99%

Finger somatotopy is preserved after tetraplegia but deteriorates over time

Kikkert

Pfyffer

Verling

et al. 2021

eLife

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Previous studies showed reorganised and/or altered activity in the primary sensorimotor cortex after a spinal cord injury (SCI), suggested to reflect abnormal processing. However, little is known about whether somatotopically-specific representations can be activated despite reduced or absent afferent hand inputs. In this observational study we used functional MRI and an (attempted) finger movement task in tetraplegic patients to characterise the somatotopic hand layout in primary somatosensory cortex. We further used structural MRI to assess spared spinal tissue bridges. We found that somatotopic hand representations can be activated through attempted finger movements in absence of sensory and motor hand functioning, and no spared spinal tissue bridges. Such preserved hand somatotopy could be exploited by rehabilitation approaches that aim to establish new hand-brain functional connections after SCI (e.g., neuroprosthetics). However, over years since SCI the hand representation somatotopy deteriorated, suggesting that somatotopic hand representations are more easily targeted within the first years after SCI.

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“…SCI largely damages both sides of the spinal cord resulting in asymmetrical deficits in sensory and motor function 54 , 74 . Thus, the handedness of SCI participants is affected by the injury 76 . Thirteen SCI subjects were right-handed before the injury and this arm corresponded to the “more affected arm” after the injury.…”

Section: Methodsmentioning

confidence: 99%

Cerebellar contribution to sensorimotor adaptation deficits in humans with spinal cord injury

Lei

Perez

2021

Sci Rep

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Humans with spinal cord injury (SCI) show deficits in associating motor commands and sensory feedback. Do these deficits affect their ability to adapt movements to new demands? To address this question, we used a robotic exoskeleton to examine learning of a sensorimotor adaptation task during reaching movements by distorting the relationship between hand movement and visual feedback in 22 individuals with chronic incomplete cervical SCI and 22 age-matched control subjects. We found that SCI individuals showed a reduced ability to learn from movement errors compared with control subjects. Sensorimotor areas in anterior and posterior cerebellar lobules contribute to learning of movement errors in intact humans. Structural brain imaging showed that sensorimotor areas in the cerebellum, including lobules I–VI, were reduced in size in SCI compared with control subjects and cerebellar atrophy increased with increasing time post injury. Notably, the degree of spared tissue in the cerebellum was positively correlated with learning rates, indicating participants with lesser atrophy showed higher learning rates. These results suggest that the reduced ability to learn from movement errors during reaching movements in humans with SCI involves abnormalities in the spinocerebellar structures. We argue that this information might help in the rehabilitation of people with SCI.

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Alterations in Motor Cortical Representation of Muscles Following Incomplete Spinal Cord Injury in Humans

Cited by 8 publications

References 39 publications

Finger somatotopy is preserved after tetraplegia but deteriorates over time

Finger somatotopy is preserved after tetraplegia but deteriorates over time

Finger somatotopy is preserved after tetraplegia but deteriorates over time

Cerebellar contribution to sensorimotor adaptation deficits in humans with spinal cord injury

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