Abstract

This study investigated impact-induced strain fields within brain tissue surrogates having different cortical gyrification. Two elastomeric surrogates, one representative of a lissencephalic brain and the other of a gyrencephalic brain, were drop impacted in unison at four different heights and in two different orientations. Each surrogate contained a radiopaque speckle pattern that was used to calculate strain fields. Two different approaches, digital image correlation (DIC) and a particle tracking method, enabled comparisons of full-field and localized strain responses. The DIC results demonstrated increased localized deviations from the mean strain field in the surrogate with a gyrified cortex. Particle tracking algorithms, defining four-node quadrilateral elements, were used to investigate the differences in the strain response of three regions: the base of a sulcus, the adjacent gyrus, and the internal capsule of the surrogates. The results demonstrated that the strains in the cortex were concentrated at the sulcal base. This mechanical mechanism of increased strain is consistent with neurodegenerative markers observed in postmortem analyses, suggesting a potential mechanism of local damage due to strain amplification at the sulcal bases in gyrencephalic brains. This strain amplification mechanism may be responsible for cumulative neurodegeneration from repeated subconcussive impacts. The observed results suggest that lissencephalic animal models, such as rodents, would not have the same modes of injury present in a gyrencephalic brain, such as that of a human. As such, a shift toward representative mild traumatic brain injury animal models having gyrencephalic cortical structures should be strongly considered.

References

References
1.
Taylor
,
C. A.
,
Bell
,
J. M.
,
Breiding
,
M. J.
, and
Xu
,
L.
,
2017
, “
Traumatic Brain Injury-Related Emergency Department Visits, Hospitalizations, and Deaths—United States, 2007 and 2013
,”
MMWR Surveillance Summaries
,
66
(
9
), pp.
1
16
.10.15585/mmwr.ss6609a1
2.
Daneshvar
,
D. H.
,
Nowinski
,
C. J.
,
McKee
,
A. C.
, and
Cantu
,
R. C.
,
2011
, “
The Epidemiology of Sport Related Concussion
,”
Clin. J. Sport Med.
,
30
(
1
), pp.
1
17
.10.1016/j.csm.2010.08.006
3.
Centers for Disease Control and Prevention
, 2015, “
Report to Congress on Traumatic Brain Injury in the United States: Epidemiology and Rehabilitation
,” National Center for Injury Prevention and Control, Division of Unintentional Injury Prevention, Atlanta, GA.
4.
Panzer
,
M. B.
,
Wood
,
G. W.
, and
Bass
,
C. R.
,
2014
, “
Scaling in Neurotrauma: How Do we Apply Animal Experiments to People?
,”
Exp. Neurol.
,
261
, pp.
120
126
.10.1016/j.expneurol.2014.07.002
5.
Xiong
,
Y.
,
Mahmood
,
A.
, and
Chopp
,
M.
,
2013
, “
Animal Models of Traumatic Brain Injury
,”
Nat. Rev. Neurosci.
,
14
(
2
), pp.
128
142
.10.1038/nrn3407
6.
Vink
,
R.
,
2018
, “
Large Animal Models of Traumatic Brain Injury
,”
J. Neurosci. Res.
,
96
(
4
), pp.
527
535
.10.1002/jnr.24079
7.
Patestas
,
M.
, and
Gartner
,
L.
,
2006
,
A Textbook of Neuroanatomy
,
Blackwell Publishing
,
Malden, MA
.
8.
McKee
,
A. C.
, and
Robinson
,
M. E.
,
2014
, “
Military-Related Traumatic Brain Injury and Neurodegeneration
,”
Alzheimer's Dementia
,
10
(
3 Suppl
), pp.
S242
S253
.10.1016/j.jalz.2014.04.003
9.
McKee
,
A. C.
,
Cantu
,
R. C.
,
Nowinski
,
C. J.
,
Hedley-Whyte
,
T.
,
Gavett
,
B. E.
,
Budson
,
A. E.
,
Veronica
,
E.
,
Lee
,
H.-S.
,
Kubilus
,
C. A.
, and
Stern
,
R. A.
,
2009
, “
TDP-43 Proteinopathy and Motor Neuron Disease in Chronic Traumatic Encephalopathy
,”
J. Neuropathol. Exp. Neurol.
,
68
(
7
), pp.
709
735
.10.1097/NEN.0b013e3181a9d503
10.
McKee
,
A. C.
,
Stein
,
T. D.
,
Nowinski
,
C. J.
,
Stern
,
R. A.
,
Daneshvar
,
D. H.
,
Alvarez
,
V. E.
,
Lee
,
H.-S.
,
Hall
,
G.
,
Wojtowicz
,
S. M.
,
Baugh
,
C. M.
,
Riley
,
D. O.
,
Kubilus
,
C. A.
,
Cormier
,
K. A.
,
Jacobs
,
M. A.
,
Martin
,
B. R.
,
Abraham
,
C. R.
,
Ikezu
,
T.
,
Reichard
,
R. R.
,
Wolozin
,
B. L.
,
Budson
,
A. E.
,
Goldstein
,
L. E.
,
Kowall
,
N. W.
, and
Cantu
,
R. C.
,
2013
, “
The Spectrum of Disease in Chronic Traumatic Encephalopathy
,”
Brain
,
136
(
1
), pp.
43
64
.10.1093/brain/aws307
11.
Guo
,
T.
,
Noble
,
W.
, and
Hanger
,
D. P.
,
2017
, “
Roles of Tau Protein in Health and Disease
,”
Acta Neuropathol.
,
133
(
5
), pp.
665
704
.10.1007/s00401-017-1707-9
12.
Horstemeyer
,
M. F.
,
Berthelson
,
P. R.
,
Moore
,
J.
,
Persons
,
A. K.
,
Dobbins
,
A.
, and
Prabhu
,
R. K.
,
2019
, “
A Mechanical Brain Damage Framework Used to Model Abnormal Brain Tau Protein Accumulations of National Football League Players
,”
Ann. Biomed. Eng.
,
47
(
9
), pp.
1873
1888
.10.1007/s10439-019-02294-1
13.
McKee
,
A. C.
, and
Daneshvar
,
D. H.
,
2015
, “
The Neuropathology of Traumatic Brain Injury
,”
Handbook of Clinical Neurology
, Vol.
127
, Elsevier, Amsterdam, The Netherlands, pp.
45
66
.
14.
Sawyer
,
T. W.
,
Josey
,
T.
,
Wang
,
Y.
,
Villanueva
,
M.
,
Ritzel
,
D.
,
Nelson
,
P.
, and
Lee
,
J.
,
2018
, “
Investigations of Primary Blast-Induced Traumatic Brain Injury
,”
Shock Waves
,
28
(
1
), pp.
85
99
.10.1007/s00193-017-0756-2
15.
Sawyer
,
T. W.
,
Ritzel
,
D. V.
,
Wang
,
Y.
,
Josey
,
T.
,
Villanueva
,
M.
,
Nelson
,
P.
,
Song
,
Y.
,
Shei
,
Y.
,
Hennes
,
G.
,
Vair
,
C.
,
Parks
,
S.
,
Fan
,
C.
, and
McLaws
,
L.
,
2018
, “
Primary Blast Causes Delayed Effects Without Cell Death in Shell-Encased Brain Cell Aggregates
,”
J. Neurotrauma
,
35
(
1
), pp.
174
186
.10.1089/neu.2016.4961
16.
Piehler
,
T.
,
Banton
,
R.
,
Zander
,
N.
,
Duckworth
,
J.
,
Benjamin
,
R.
, and
Sparks
,
R.
,
2018
, “
High-Speed Imaging and Small-Scale Explosive Characterization Techniques to Understand Effects of Primary Blast-Induced Injury on Nerve Cell Structure and Function
,”
Shock Waves
,
28
(
1
), pp.
37
50
.10.1007/s00193-017-0744-6
17.
Thielen
,
P.
,
Mehoke
,
T.
,
Gleason
,
J.
,
Iwaskiw
,
A.
,
Paulson
,
J.
,
Merkle
,
A.
,
Wester
,
B.
, and
Dymond
,
J.
,
2018
, “
Exploration of the Molecular Basis of Blast Injury in a Biofidelic Model of Traumatic Brain Injury
,”
Shock Waves
,
28
(
1
), pp.
115
126
.10.1007/s00193-017-0769-x
18.
Bottlang
,
M.
,
Sommers
,
M. B.
,
Lusardi
,
T. A.
,
Miesch
,
J. J.
,
Simon
,
R. P.
, and
Xiong
,
Z.-G.
,
2007
, “
Modeling Neural Injury in Organotypic Cultures by Application of Inertia-Driven Shear Strain
,”
J. Neurotrauma
,
24
(
6
), pp.
1068
1077
.10.1089/neu.2006.3772
19.
Sarntinoranont
,
M.
,
Lee
,
S. J.
,
Hong
,
Y.
,
King
,
M. A.
,
Subhash
,
G.
,
Kwon
,
J.
, and
Moore
,
D. F.
,
2012
, “
High-Strain-Rate Brain Injury Model Using Submerged Acute Rat Brain Tissue Slices
,”
J. Neurotrauma
,
29
(
2
), pp.
418
429
.10.1089/neu.2011.1772
20.
Zhang
,
K.
, and
Sejnowski
,
T. J.
,
2000
, “
A Universal Scaling Law Between Gray Matter and White Matter of Cerebral Cortex
,”
Proc. Natl. Acad. Sci. U. S. A.
,
97
(
10
), pp.
5621
5626
.10.1073/pnas.090504197
21.
Jean
,
A.
,
Nyein
,
M. K.
,
Zheng
,
J. Q.
,
Moore
,
D. F.
,
Joannopoulos
,
J. D.
, and
Radovitzky
,
R.
,
2014
, “
An Animal-to-Human Scaling Law for Blast-Induced Traumatic Brain Injury Risk Assessment
,”
Proc. Natl. Acad. Sci.
,
111
(
43
), pp.
15310
15315
.10.1073/pnas.1415743111
22.
Tallinen
,
T.
,
Chung
,
J. Y.
,
Biggins
,
J. S.
, and
Mahadevan
,
L.
,
2014
, “
Gyrification From Constrained Cortical Expansion
,”
Proc. Natl. Acad. Sci.
,
111
(
35
), pp.
12667
12672
.10.1073/pnas.1406015111
23.
Ganpule
,
S.
,
Daphalapurkar
,
N. P.
,
Cetingul
,
M. P.
, and
Ramesh
,
K. T.
,
2018
, “
Effect of Bulk Modulus on Deformation of the Brain Under Rotational Accelerations
,”
Shock Waves
,
28
(
1
), pp.
127
139
.10.1007/s00193-017-0791-z
24.
Coats
,
B.
, and
Margulies
,
S. S.
,
2006
, “
Material Properties of Porcine Parietal Cortex
,”
J. Biomech.
,
39
(
13
), pp.
2521
836
.10.1016/j.jbiomech.2005.07.020
25.
Hajiaghamemar
,
M.
,
Wu
,
T.
,
Panzer
,
M. B.
, and
Margulies
,
S. S.
,
2020
, “
Embedded Axonal Fiber Tracts Improve Finite Element Model Predictions of Traumatic Brain Injury
,”
Biomech. Model. Mechanobiol.
,
19
(
3
), pp.
1109
1130
.10.1007/s10237-019-01273-8
26.
Lauret
,
C.
,
Hrapko
,
M.
,
van Dommelen
,
J. A. W.
,
Peters
,
G. W. M.
, and
Wismans
,
J. S. H. M.
,
2009
, “
Optical Characterization of Acceleration-Induced Strain Fields in Inhomogeneous Brain Slices
,”
Med. Eng. Phys.
,
31
(
3
), pp.
392
399
.10.1016/j.medengphy.2008.05.004
27.
Raghupathi
,
R.
,
Mehr
,
M. F.
,
Helfaer
,
M. A.
, and
Margulies
,
S. S.
,
2004
, “
Traumatic Axonal Injury is Exacerbated Following Repetitive Closed Head Injury in the Neonatal Pig
,”
J. Neurotrauma
,
21
(
3
), pp.
307
316
.10.1089/089771504322972095
28.
Cloots
,
R. J. H.
,
Gervaise
,
H. M. T.
,
Van Dommelen
,
J. A. W.
, and
Geers
,
M. G. D.
,
2008
, “
Biomechanics of Traumatic Brain Injury: Influences of the Morphologic Heterogeneities of the Cerebral Cortex
,”
Ann. Biomed. Eng.
,
36
(
7
), pp.
1203
1215
.10.1007/s10439-008-9510-3
29.
Ghajari
,
M.
,
Hellyer
,
P. J.
, and
Sharp
,
D. J.
,
2017
, “
Computational Modelling of Traumatic Brain Injury Predicts the Location of Chronic Traumatic Encephalopathy Pathology
,”
Brain
,
140
(
2
), pp.
333
343
.10.1093/brain/aww317
30.
Saikali
,
S.
,
Meurice
,
P.
,
Sauleau
,
P.
,
Eliat
,
P. A.
,
Bellaud
,
P.
,
Randuineau
,
G.
,
Vérin
,
M.
, and
Malbert
,
C. H.
,
2010
, “
A Three-Dimensional Digital Segmented and Deformable Brain Atlas of the Domestic Pig
,”
J. Neurosci. Methods
,
192
(
1
), pp.
102
109
.10.1016/j.jneumeth.2010.07.041
31.
Fedorov
,
A.
,
Beichel
,
R.
,
Kalpathy-Cramer
,
J.
,
Finet
,
J.
,
Fillion-Robin
,
J.-C.
,
Pujol
,
S.
,
Bauer
,
C.
,
Jennings
,
D.
,
Fennessy
,
F.
,
Sonka
,
M.
,
Buatti
,
J.
,
Aylward
,
S.
,
Miller
,
J.
,
Pieper
,
S.
, and
Kikinis
,
R.
,
2012
, “
3D Slicer as an Image Computing Platform for the Quantitative Imaging Network
,”
Magn. Resonance Imaging
,
30
(
9
), pp.
1323
1341
.10.1016/j.mri.2012.05.001
32.
Palchesko
,
R. N.
,
Zhang
,
L.
,
Sun
,
Y.
, and
Feinberg
,
A. W.
,
2012
, “
Development of Polydimethylsiloxane Substrates With Tunable Elastic Modulus to Study Cell Mechanobiology in Muscle and Nerve
,”
PLoS One
,
7
(
12
), p.
e51499
.10.1371/journal.pone.0051499
33.
Kalcioglu
,
Z. I.
,
Mrozek
,
R. A.
,
Mahmoodian
,
R.
,
VanLandingham
,
M. R.
,
Lenhart
,
J. L.
, and
Van Vliet
,
K. J.
,
2013
, “
Tunable Mechanical Behavior of Synthetic Organogels as Biofidelic Tissue Simulants
,”
J. Biomech.
,
46
(
9
), pp.
1583
1591
.10.1016/j.jbiomech.2013.03.011
34.
Ouellet
,
S.
, and
Philippens
,
M.
,
2018
, “
The Multi-Modal Responses of a Physical Head Model Subjected to Various Blast Exposure Conditions
,”
Shock Waves
,
28
(
1
), pp.
19
36
.10.1007/s00193-017-0771-3
35.
Blaber
,
J.
,
Adair
,
B.
, and
Antoniou
,
A.
,
2015
, “
Ncorr: Open-Source 2D Digital Image Correlation Matlab Software
,”
Exp. Mech.
,
55
(
6
), pp.
1105
1122
.10.1007/s11340-015-0009-1
36.
Magnan
,
S.
,
2018
, “
Analysis of Radiographic Contrast Markers for X-Ray Digital Image Correlation of Tissue-Simulants Under Dynamic Load
,”
M.Sc. thesis
,
Carleton University
, Ottawa, ON, Canada.10.22215/etd/2018-13242
37.
Sbalzarini
,
I. F.
, and
Koumoutsakos
,
P.
,
2005
, “
Feature Point Tracking and Trajectory Analysis for Video Imaging in Cell Biology
,”
J. Struct. Biol.
,
151
(
2
), pp.
182
195
.10.1016/j.jsb.2005.06.002
38.
Schindelin
,
J.
,
Arganda-Carreras
,
I.
,
Frise
,
E.
,
Kaynig
,
V.
,
Longair
,
M.
,
Pietzsch
,
T.
,
Preibisch
,
S.
,
Rueden
,
C.
,
Saalfeld
,
S.
,
Schmid
,
B.
,
Tinevez
,
J.-Y.
,
White
,
D. J.
,
Hartenstein
,
V.
,
Eliceiri
,
K.
,
Tomancak
,
P.
, and
Cardona
,
A.
,
2012
, “
Fiji: An Open-Source Platform for Biological-Image Analysis
,”
Nat. Methods
,
9
(
7
), pp.
676
682
.10.1038/nmeth.2019
39.
Schneider
,
C. A.
,
Rasband
,
W. S.
, and
Eliceiri
,
K. W.
,
2012
, “
NIH Image to ImageJ: 25 Years of Image Analysis
,”
Nat. Methods
,
9
(
7
), pp.
671
675
.10.1038/nmeth.2089
40.
Cook
,
R. D.
, and Malkus, D. S.,
2007
,
Concepts and Applications of Finite Element Analysis
,
John Wiley & Sons, Hoboken, NJ.
41.
Margulies
,
S. S.
, and
Thibault
,
L. E.
,
1992
, “
A Proposed Tolerance Criterion for Diffuse Axonal Injury in Man
,”
J. Biomech.
,
25
(
8
), pp.
917
923
.10.1016/0021-9290(92)90231-O
42.
Baugh
,
C.
,
Stamm
,
J.
,
Riley
,
D.
,
Gavett
,
B.
,
Shenton
,
M.
,
Lin
,
A.
,
Nowinski
,
C.
,
Cantu
,
R.
,
McKee
,
A.
, and
Stern
,
R.
,
2012
, “
Chronic Traumatic Encephalopathy: Neurodegeneration Following Repetitive Concussive and Subconcussive Brain Trauma
,”
Brain Imaging Behav.
,
6
(
2
), pp.
244
254
.10.1007/s11682-012-9164-5
43.
Mckee
,
A. C.
,
Stein
,
T. D.
,
Kiernan
,
P. T.
, and
Alvarez
,
V. E.
,
2015
, “
The Neuropathology of Chronic Traumatic Encephalopathy
,”
Brain Pathol
,
25
(
3
), pp.
350
364
.10.1111/bpa.12248
44.
Margulies
,
S. S.
,
Thibault
,
L. E.
, and
Gennarelli
,
T. A.
,
1990
, “
Physical Model Simulations of Brain Injury in the Primate
,”
J. Biomech.
,
23
(
8
), pp.
823
836
.10.1016/0021-9290(90)90029-3
You do not currently have access to this content.