Arts & Sciences Brown School McKelvey School of Engineering School of Medicine Weekly Publications

WashU weekly Neuroscience publications: November 13, 2022

Bi-allelic CAMSAP1 variants cause a clinically recognizable neuronal migration disorder” (2022) American Journal of Human Genetics

Bi-allelic CAMSAP1 variants cause a clinically recognizable neuronal migration disorder
(2022) American Journal of Human Genetics, 109 (11), pp. 2068-2079. 

Khalaf-Nazzal, R.a , Fasham, J.b c , Inskeep, K.A.d e , Blizzard, L.E.f , Leslie, J.S.b , Wakeling, M.N.b , Ubeyratna, N.b , Mitani, T.h , Griffith, J.L.i , Baker, W.j , Al-Hijawi, F.k , Keough, K.C.l m , Gezdirici, A.n , Pena, L.f g , Spaeth, C.G.f g , Turnpenny, P.D.b c , Walsh, J.R.o , Ray, R.p , Neilson, A.q , Kouranova, E.q , Cui, X.q , Curiel, D.T.r s t , Pehlivan, D.h u x , Akdemir, Z.C.h , Posey, J.E.h , Lupski, J.R.h v w x , Dobyns, W.B.y , Stottmann, R.W.d e f g , Crosby, A.H.b , Baple, E.L.b c

a Biomedical Sciences Department, Faculty of Medicine, Arab American University of Palestine, Jenin, P227, Palestine
b Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, ExeterEX2 5DW, United Kingdom
c Peninsula Clinical Genetics Service, Royal Devon University Healthcare NHS Foundation Trust (Heavitree Hospital), Gladstone Road, ExeterEX1 2ED, United Kingdom
d Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, United States
e Institute for Genomic Medicine at Nationwide Children’s Hospital, The Ohio State University College of Medicine, Columbus, OH 43205, United States
f Division of Human Genetics, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, United States
g Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229, United States
h Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, United States
i Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, United States
j Paediatrics Department, Dr. Khalil Suleiman Government Hospital, Jenin, Palestine
k Paediatrics Community Outpatient Clinics, Palestinian Ministry of Health, Jenin, Palestine
l Department of Pediatrics, Dell Medical School, 1400 Barbara Jordan Boulevard, Austin, TX 78723, United States
m Child Neurology Consultants of Austin, 7940 Shoal Creek Boulevard, Suite 100, Austin, TX 78757, United States
n Department of Medical Genetics, Başakşehir Çam and Sakura City Hospital, Istanbul, 34480, Turkey
o Department of Neurological Surgery, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, United States
p Departments of Pediatrics and Medical Genetics, Boston Children’s Hospital and Harvard Medical School, Boston, MA 02115, United States
q Genome Engineering & Stem Cell Center, Department of Genetics, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, United States
r Department of Biomedical Engineering, McKelvey School of Engineering, Washington University in Saint Louis, St. Louis, MO 63130, United States
s Division of Cancer Biology, Department of Radiation Oncology, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, United States
t Biologic Therapeutics Center, Department of Radiation Oncology, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, United States
u Division of Neurology and Developmental Neuroscience, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, United States
v Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX 77030, United States
w Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, United States
x Texas Children’s Hospital, Houston, TX 77030, United States
y Departments of Pediatrics and Genetics, University of Minnesota, Minneapolis, MN, United States

Abstract
Non-centrosomal microtubules are essential cytoskeletal filaments that are important for neurite formation, axonal transport, and neuronal migration. They require stabilization by microtubule minus-end-targeting proteins including the CAMSAP family of molecules. Using exome sequencing on samples from five unrelated families, we show that bi-allelic CAMSAP1 loss-of-function variants cause a clinically recognizable, syndromic neuronal migration disorder. The cardinal clinical features of the syndrome include a characteristic craniofacial appearance, primary microcephaly, severe neurodevelopmental delay, cortical visual impairment, and seizures. The neuroradiological phenotype comprises a highly recognizable combination of classic lissencephaly with a posterior more severe than anterior gradient similar to PAFAH1B1(LIS1)-related lissencephaly and severe hypoplasia or absence of the corpus callosum; dysplasia of the basal ganglia, hippocampus, and midbrain; and cerebellar hypodysplasia, similar to the tubulinopathies, a group of monogenic tubulin-associated disorders of cortical dysgenesis. Neural cell rosette lineages derived from affected individuals displayed findings consistent with these phenotypes, including abnormal morphology, decreased cell proliferation, and neuronal differentiation. Camsap1-null mice displayed increased perinatal mortality, and RNAScope studies identified high expression levels in the brain throughout neurogenesis and in facial structures, consistent with the mouse and human neurodevelopmental and craniofacial phenotypes. Together our findings confirm a fundamental role of CAMSAP1 in neuronal migration and brain development and define bi-allelic variants as a cause of a clinically distinct neurodevelopmental disorder in humans and mice. © 2022 The Authors

Author Keywords
agyria;  autosomal recessive;  lissencephaly;  MARK2;  neurodevelopmental disorder;  pachygyria;  patronin;  tubulinopathy

Funding details
National Heart, Lung, and Blood InstituteNHLBIUM1 HG006542
National Human Genome Research InstituteNHGRI
National Institute of Dental and Craniofacial ResearchNIDCRR01 DE027091
Wellcome TrustWT216279/Z/19/Z
Baylor-Hopkins Center for Mendelian GenomicsBHCMG
Medical Research CouncilMRCG1001931, G1002279, MC-PC-18047, MC_PC_15047, MC_PC_15054
University of Exeter
National Heart and Lung InstituteNHLI
Medical Research FoundationMRF-145-0006-DG-BAPL-C0788

Document Type: Article
Publication Stage: Final
Source: Scopus

Return to Full Participation Following Concussion in the National Football League, 2015 Through 2020” (2022) Clinical Journal of Sport Medicine: Official Journal of the Canadian Academy of Sport Medicine

Return to Full Participation Following Concussion in the National Football League, 2015 Through 2020
(2022) Clinical Journal of Sport Medicine: Official Journal of the Canadian Academy of Sport Medicine, 32 (6), pp. e605-e613. 

Mack, C.D.a , Herzog, M.M.a , Solomon, G.b c , Putukian, M.d , Lee, R.Y.a , Matava, M.J.e , Cárdenas, J.f , Theodore, N.g , Sills, A.c

a Real World Solutions, Research Triangle ParkNC, United States
b Department of Neurological Surgery and Vanderbilt Sports Concussion Center Vanderbilt University School of Medicine, Nashville, TN, United States
c National Football League Player Health and Safety DepartmentNY, United States
d Massachusetts General Hospital, Harvard University, Boston, MA, United States
e Department of Orthopedic Surgery, Washington University, St. Louis, MO, United States
f Department of Neurology, Barrow Neurological Institute, Phoenix, Arizona; and
g Department of Neurological Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, Liberia

Abstract
OBJECTIVE: Quantify days missed, games missed, injury burden, and time to return to full participation (RTFP) among National Football League (NFL) players who sustained a concussion. DESIGN: Retrospective cohort study. SETTING: 2015 through 2020 NFL seasons. PARTICIPANTS: National Football League players diagnosed with a concussion from 2015 to 2020. INTERVENTIONS: National Football League-mandated graduated RTFP protocol. MAIN OUTCOME MEASURES: Days missed, games missed, burden, and time to RTFP, overall and by position. RESULTS: An annual average of 3639 player-days of participation and 255 games were missed across NFL because of concussion. Concussed players missed a median of 9 days (mean = 15.0), a relatively stable metric over 6 years, with slight variation by position. Offensive linemen, tight ends, running backs, and linebackers missed the most days per concussion; defensive secondary, offensive linemen, and wide receivers sustained the highest injury burden. Postconcussion, 59% of players missed one or more scheduled games. Among players concussed in a Sunday game, 38% played in a Sunday game one week later. CONCLUSIONS: The 9-day median time missed post-concussion may be related to emphasis on graduated phase-based concussion management. No concussed player returned to competition on the day of injury, and less than 40% participated in games the following week. Further work is needed to better understand characteristics of concussions that take longer to return and movement through stages of return. Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.

Document Type: Article
Publication Stage: Final
Source: Scopus

Spinal stimulation for motor rehabilitation immediately modulates nociceptive transmission” (2022) Journal of Neural Engineering

Spinal stimulation for motor rehabilitation immediately modulates nociceptive transmission
(2022) Journal of Neural Engineering, 19 (5), . 

Bandres, M.F.a b , Gomes, J.L.a , McPherson, J.G.a b c d e

a Program in Physical Therapy, Washington University School of Medicine, 4444 Forest Park Avenue, St. Louis, United States
b Department of Biomedical Engineering, Washington University in St. Louis, 1 Brookings Drive, St. Louis, MO 63130, United States
c Department of Anesthesiology, Washington University School of Medicine, 660 S Euclid Avenue, St. Louis, MO 63110, United States
d Washington University Pain Center, Washington University School of Medicine, 660 S Euclid Avenue, St. Louis, United States
e Program in Neuroscience, Washington University School of Medicine, 660 S Euclid Avenue, St. Louis, MO 63110, United States

Abstract
Objective. Spinal cord injury (SCI) often results in debilitating movement impairments and neuropathic pain. Electrical stimulation of spinal neurons holds considerable promise both for enhancing neural transmission in weakened motor pathways and for reducing neural transmission in overactive nociceptive pathways. However, spinal stimulation paradigms currently under development for individuals living with SCI continue overwhelmingly to be developed in the context of motor rehabilitation alone. The objective of this study is to test the hypothesis that motor-targeted spinal stimulation simultaneously modulates spinal nociceptive transmission.Approach. We characterized the neuromodulatory actions of motor-targeted intraspinal microstimulation (ISMS) on the firing dynamics of large populations of discrete nociceptive specific and wide dynamic range (WDR) neurons. Neurons were accessed via dense microelectrode arrays implantedin vivointo lumbar enlargement of rats. Nociceptive and non-nociceptive cutaneous transmission was induced before, during, and after ISMS by mechanically probing the L5 dermatome.Main results. Our primary findings are that (a) sub-motor threshold ISMS delivered to spinal motor pools immediately modulates concurrent nociceptive transmission; (b) the magnitude of anti-nociceptive effects increases with longer durations of ISMS, including robust carryover effects; (c) the majority of all identified nociceptive-specific and WDR neurons exhibit firing rate reductions after only 10 min of ISMS; and (d) ISMS does not increase spinal responsiveness to non-nociceptive cutaneous transmission. These results lead to the conclusion that ISMS parameterized to enhance motor output results in an overall net decrease n spinal nociceptive transmission.Significance. These results suggest that ISMS may hold translational potential for neuropathic pain-related applications and that it may be uniquely suited to delivering multi-modal therapeutic benefits for individuals living with SCI. © 2022 IOP Publishing Ltd.

Author Keywords
motor control;  neural plasticity;  neuromodulation;  neuropathic pain;  rehabilitation;  spinal cord injury;  spinal stimulation

Document Type: Article
Publication Stage: Final
Source: Scopus

Temporal Construal Effects Are Independent of Episodic Future Thought” (2022) Psychological Science

Temporal Construal Effects Are Independent of Episodic Future Thought
(2022) Psychological Science, . 

Rosenbaum, R.S.a b , Halilova, J.G.a b , Kwan, D.a b , Beneventi, S.c , Craver, C.F.d , Gilboa, A.b e , Ciaramelli, E.c f

a Department of Psychology, York University, Canada
b Rotman Research Institute, Baycrest, Toronto, Canada
c Dipartimento di Psicologia, Università di Bologna, Italy
d Department of Philosophy, Washington University in St. Louis, United States
e Department of Psychology, University of Toronto, Canada
f Centro Studi e Ricerche in Neuroscienze Cognitive, Università di Bologna, Italy

Abstract
Human thought is prone to biases. Some biases serve as beneficial heuristics to free up limited cognitive resources or improve well-being, but their neurocognitive basis is unclear. One such bias is a tendency to construe events in the distant future in abstract, general terms and events in the near future in concrete, detailed terms. Temporal construal may rely on our capacity to orient toward and/or imagine context-rich future events. We tested 21 individuals with impaired episodic future thinking resulting from lesions to the hippocampus or ventromedial prefrontal cortex (vmPFC) and 57 control participants (aged 45–76 years) from Canada and Italy on measures sensitive to temporal construal. We found that temporal construal persisted in most patients, even those with impaired episodic future thinking, but was abolished in some vmPFC cases, possibly in relation to difficulties forming and maintaining future intentions. The results confirm the fractionation of future thinking and that parts of vmPFC might critically support our ability to flexibly conceive and orient ourselves toward future events. © The Author(s) 2022.

Author Keywords
episodic memory;  future imagining;  hippocampus;  patient-lesion method;  temporal orientation;  ventromedial prefrontal cortex

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Neurodevelopmental patterns of early postnatal white matter maturation represent distinct underlying microstructure and histology” (2022) Neuron

Neurodevelopmental patterns of early postnatal white matter maturation represent distinct underlying microstructure and histology
(2022) Neuron, . 

Nazeri, A.a , Krsnik, Ž.b , Kostović, I.b , Ha, S.M.a , Kopić, J.b , Alexopoulos, D.c , Kaplan, S.c , Meyer, D.c , Luby, J.L.d , Warner, B.B.e , Rogers, C.E.d , Barch, D.M.a d f , Shimony, J.S.a , McKinstry, R.C.a , Neil, J.J.c , Smyser, C.D.a c e , Sotiras, A.a g

a Mallinckrodt Institute of Radiology, Washington University School of Medicine, Saint Louis, MO 63110, United States
b Croatian Institute for Brain Research, School of Medicine, University of Zagreb School of Medicine, Zagreb, 10000, Croatia
c Department of Neurology, Washington University School of Medicine, Saint Louis, MO 63110, United States
d Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO 63110, United States
e Department of Pediatrics, Washington University School of Medicine, Saint Louis, MO 63110, United States
f Psychological & Brain Sciences, Washington University School in St. Louis, Saint Louis, MO 63130, United States
g Institute for Informatics, Washington University School of Medicine, Saint Louis, MO 63108, United States

Abstract
Cerebral white matter undergoes a rapid and complex maturation during the early postnatal period. Prior magnetic resonance imaging (MRI) studies of early postnatal development have often been limited by small sample size, single-modality imaging, and univariate analytics. Here, we applied nonnegative matrix factorization, an unsupervised multivariate pattern analysis technique, to T2w/T1w signal ratio maps from the Developing Human Connectome Project (n = 342 newborns) revealing patterns of coordinated white matter maturation. These patterns showed divergent age-related maturational trajectories, which were replicated in another independent cohort (n = 239). Furthermore, we showed that T2w/T1w signal variations in these maturational patterns are explained by differential contributions of white matter microstructural indices derived from diffusion-weighted MRI. Finally, we demonstrated how white matter maturation patterns relate to distinct histological features by comparing our findings with postmortem late fetal/early postnatal brain tissue staining. Together, these results delineate concise and effective representation of early postnatal white matter reorganization. © 2022 Elsevier Inc.

Author Keywords
data-driven parcellation;  histology;  MRI;  Neurodevelopment;  newborn;  subplate remnant;  tissue microstructure;  topography;  unsupervised machine learning;  white matter maturation

Funding details
RR1953, RSNA R&E
National Institutes of HealthNIHP50 HD103525, R01AG067103
BrightFocus FoundationBFF
University of WashingtonUW
American Society of NeuroradiologyASNR
Engineering Research CentersERC319456, R01MH113883
European CommissionEC
European Research CouncilERC
Hrvatska Zaklada za ZnanostHRZZ
European Social FundESF1S10OD018091-01, 1S10RR022984-01A1, PSZ-2019-02-4710
Seventh Framework ProgrammeFP7FP/2007-2013

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Deferoxamine Prevents Neonatal Posthemorrhagic Hydrocephalus Through Choroid Plexus-Mediated Iron Clearance” (2022) Translational Stroke Research

Deferoxamine Prevents Neonatal Posthemorrhagic Hydrocephalus Through Choroid Plexus-Mediated Iron Clearance
(2022) Translational Stroke Research, . 

Ramagiri, S.a , Pan, S.a , DeFreitas, D.a , Yang, P.H.a , Raval, D.K.a , Wozniak, D.F.b c d , Esakky, P.a , Strahle, J.M.a e f

a Department of Neurosurgery, Washington University School of Medicine, St. Louis, MO 63110, United States
b Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110-1093, United States
c Intellectual and Developmental Disabilities Research Center, Washington University School of Medicine, St. Louis, MO 63110-1093, United States
d Taylor Family Institute for Innovative Psychiatric Research, Washington University School of Medicine, St. Louis, MO 63110-1093, United States
e Department of Orthopedic Surgery, Washington University School of Medicine, St. Louis, MO 63110, United States
f Department of Pediatrics, Washington University School of Medicine, St. Louis, MO 63110, United States

Abstract
Posthemorrhagic hydrocephalus occurs in up to 30% of infants with high-grade intraventricular hemorrhage and is associated with the worst neurocognitive outcomes in preterm infants. The mechanisms of posthemorrhagic hydrocephalus after intraventricular hemorrhage are unknown; however, CSF levels of iron metabolic pathway proteins including hemoglobin have been implicated in its pathogenesis. Here, we develop an animal model of intraventricular hemorrhage using intraventricular injection of hemoglobin at post-natal day 4 that results in acute and chronic hydrocephalus, pathologic choroid plexus iron accumulation, and subsequent choroid plexus injury at post-natal days 5, 7, and 15. This model also results in increased expression of aquaporin-1, Na+/K+/Cl- cotransporter 1, and Na+/K+/ATPase on the apical surface of the choroid plexus 24 h post-intraventricular hemorrhage. We use this model to evaluate a clinically relevant treatment strategy for the prevention of neurological sequelae after intraventricular hemorrhage using intraventricular administration of the iron chelator deferoxamine at the time of hemorrhage. Deferoxamine treatment prevented posthemorrhagic hydrocephalus for up to 11 days after intraventricular hemorrhage and prevented the development of sensorimotor gating deficits. In addition, deferoxamine treatment facilitated acute iron clearance through the choroid plexus and subsequently reduced choroid plexus iron levels at 24 h with reversal of hemoglobin-induced aquaporin-1 upregulation on the apical surface of the choroid plexus. Intraventricular administration of deferoxamine at the time of intraventricular hemorrhage may be a clinically relevant treatment strategy for preventing posthemorrhagic hydrocephalus and likely acts through promoting iron clearance through the choroid plexus to prevent hemoglobin-induced injury. © 2022, The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Author Keywords
Deferoxamine;  Germinal matrix hemorrhage;  Hydrocephalus;  Intraventricular hemorrhage;  Preterm

Funding details
National Institutes of HealthNIHR01 NS110793
McDonnell Center for Systems Neuroscience
Washington University School of Medicine in St. LouisWUSM
Center for Cellular Imaging, Washington UniversityWUCCI
Hydrocephalus AssociationHA
St. Louis Children’s HospitalSLCH

Document Type: Article
Publication Stage: Article in Press
Source: Scopus