Perinatal stroke: mapping and modulating developmental plasticity

Kirton, Adam; Metzler, Megan J.; Craig, Brandon T.; Hilderley, Alicia J.; Dunbar, Mary; Giuffre, Adrianna; Wrightson, James; Zewdie, Ephrem; Carlson, Helen L.

doi:10.1038/s41582-021-00503-x

Cited by 39 publications

(33 citation statements)

References 305 publications

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“…Perinatal strokes lead to lifelong disability for millions worldwide 1 , 2 . Three types predominate including arterial ischemic stroke (AIS), encompassing both neonatal arterial ischemic stroke and arterial presumed perinatal ischemic stroke, and periventricular venous infarction (PVI) 1 , 3 . Males appear to have a higher prevalence than females for neonatal AIS and PVI, but not arterial presumed perinatal ischemic stroke 1 .…”

Section: Introductionmentioning

confidence: 99%

Structural connectivity of the sensorimotor network within the non-lesioned hemisphere of children with perinatal stroke

Craig

Kinney‐Lang

Hilderley

et al. 2022

Sci Rep

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Perinatal stroke occurs early in life and often leads to a permanent, disabling weakness to one side of the body. To test the hypothesis that non-lesioned hemisphere sensorimotor network structural connectivity in children with perinatal stroke is different from controls, we used diffusion imaging and graph theory to explore structural topology between these populations. Children underwent diffusion and anatomical 3T MRI. Whole-brain tractography was constrained using a brain atlas creating an adjacency matrix containing connectivity values. Graph theory metrics including betweenness centrality, clustering coefficient, and both neighbourhood and hierarchical complexity of sensorimotor nodes were compared to controls. Relationships between these connectivity metrics and validated sensorimotor assessments were explored. Eighty-five participants included 27 with venous stroke (mean age = 11.5 ± 3.7 years), 26 with arterial stroke (mean age = 12.7 ± 4.0 years), and 32 controls (mean age = 13.3 ± 3.6 years). Non-lesioned primary motor (M1), somatosensory (S1) and supplementary motor (SMA) areas demonstrated lower betweenness centrality and higher clustering coefficient in stroke groups. Clustering coefficient of M1, S1, and SMA were inversely associated with clinical motor function. Hemispheric betweenness centrality and clustering coefficient were higher in stroke groups compared to controls. Hierarchical and average neighbourhood complexity across the hemisphere were lower in stroke groups. Developmental plasticity alters the connectivity of key nodes within the sensorimotor network of the non-lesioned hemisphere following perinatal stroke and contributes to clinical disability.

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Section: Introductionmentioning

confidence: 99%

Structural connectivity of the sensorimotor network within the non-lesioned hemisphere of children with perinatal stroke

Craig

Kinney‐Lang

Hilderley

et al. 2022

Sci Rep

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“…Therapeutic approaches to enhance developmental neuroplasticity of children with perinatal stroke have been reviewed recently. 24 In a separate pilot study with no participant overlap with this study, we showed that intensive activity-based rehabilitation for the lower extremity in children with hemiparesis under the age of 2 resulted in large improvements in walking. 25 We hypothesized that early, intensive, child-initiated therapy for the lower extremity in children with perinatal stroke would result in greater improvements in motor function than usual care.…”

Section: Introductionmentioning

confidence: 61%

Early, Intensive, Lower Extremity Rehabilitation Shows Preliminary Efficacy After Perinatal Stroke: Results of a Pilot Randomized Controlled Trial

Hurd

Livingstone

Brunton

et al. 2022

Neurorehabil Neural Repair

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Background Perinatal stroke injures motor regions of the brain, compromising movement for life. Early, intensive, active interventions for the upper extremity are efficacious, but interventions for the lower extremity remain understudied. Objective To determine the feasibility and potential efficacy of ELEVATE—Engaging the Lower Extremity Via Active Therapy Early—on gross motor function. Methods We conducted a single-blind, two-arm, randomized controlled trial (RCT), with the Immediate Group receiving the intervention while the Delay Group served as a 3-month waitlist control. A separate cohort living beyond commuting distance was trained by their parents with guidance from physical therapists. Participants were 8 months to 3 years old, with MRI-confirmed perinatal ischemic stroke and early signs of hemiparesis. The intervention was play-based, focused on weight-bearing, balance and walking for 1 hour/day, 4 days/week for 12 weeks. The primary outcome was the Gross Motor Function Measure-66 (GMFM-66). Secondary outcomes included steps and gait analyses. Final follow-up occurred at age 4. Results Thirty-four children participated (25 RCT, 9 Parent-trained). The improvement in GMFM-66 over 12 weeks was greater for the Immediate than the Delay Group in the RCT (average change 3.4 units higher) and greater in younger children. Average step counts reached 1370-3750 steps/session in the last week of training for all children. Parent-trained children also improved but with greater variability. Conclusions Early, activity-intensive lower extremity therapy for young children with perinatal stroke is feasible and improves gross motor function in the short term. Longer term improvement may require additional bouts of intervention. Clinical trial registration This study was registered at ClinicalTrials.gov (NCT01773369).

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“…The sensorimotor network is one of the earliest developing networks, well-established very early in life but highly refined throughout of development where motor maps may undergo dramatic developmental plasticity (Khazipov and Milh, 2018). How these natural processes are altered after early unilateral injury such as perinatal stroke are increasingly understood from preclinical models (Martin et al, 2007;Wen et al, 2018) and human imaging and brain mapping studies (Kirton et al, 2021). A recent mouse model of perinatal stroke evaluated motor map size and movement latency following cortical stimulation and motor training (Zhang et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Effects of Transcranial Direct Current Stimulation and High-Definition Transcranial Direct Current Stimulation Enhanced Motor Learning on Robotic Transcranial Magnetic Stimulation Motor Maps in Children

Giuffre

Zewdie

Wrightson

et al. 2021

Front. Hum. Neurosci.

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Introduction: Conventional transcranial direct current stimulation (tDCS) and high-definition tDCS (HD-tDCS) may improve motor learning in children. Mechanisms are not understood. Neuronavigated robotic transcranial magnetic stimulation (TMS) can produce individualised maps of primary motor cortex (M1) topography. We aimed to determine the effects of tDCS- and HD-tDCS-enhanced motor learning on motor maps.Methods: Typically developing children aged 12–18 years were randomised to right M1 anodal tDCS, HD-tDCS, or Sham during training of their left-hand on the Purdue Pegboard Task (PPT) over 5 days. Bilateral motor mapping was performed at baseline (pre), day 5 (post), and 6-weeks retention time (RT). Primary muscle was the first dorsal interosseous (FDI) with secondary muscles of abductor pollicis brevis (APB) and adductor digiti minimi (ADM). Primary mapping outcomes were volume (mm2/mV) and area (mm2). Secondary outcomes were centre of gravity (COG, mm) and hotspot magnitude (mV). Linear mixed-effects modelling was employed to investigate effects of time and stimulation type (tDCS, HD-tDCS, Sham) on motor map characteristics.Results: Twenty-four right-handed participants (median age 15.5 years, 52% female) completed the study with no serious adverse events or dropouts. Quality maps could not be obtained in two participants. No effect of time or group were observed on map area or volume. LFDI COG (mm) differed in the medial-lateral plane (x-axis) between tDCS and Sham (p = 0.038) from pre-to-post mapping sessions. Shifts in map COG were also observed for secondary left-hand muscles. Map metrics did not correlate with behavioural changes.Conclusion: Robotic TMS mapping can safely assess motor cortex neurophysiology in children undergoing motor learning and neuromodulation interventions. Large effects on map area and volume were not observed while changes in COG may occur. Larger controlled studies are required to understand the role of motor maps in interventional neuroplasticity in children.

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Perinatal stroke: mapping and modulating developmental plasticity

Cited by 39 publications

References 305 publications

Structural connectivity of the sensorimotor network within the non-lesioned hemisphere of children with perinatal stroke

Structural connectivity of the sensorimotor network within the non-lesioned hemisphere of children with perinatal stroke

Early, Intensive, Lower Extremity Rehabilitation Shows Preliminary Efficacy After Perinatal Stroke: Results of a Pilot Randomized Controlled Trial

Effects of Transcranial Direct Current Stimulation and High-Definition Transcranial Direct Current Stimulation Enhanced Motor Learning on Robotic Transcranial Magnetic Stimulation Motor Maps in Children

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