Shear Properties of Human

B. R. Donnelly
Principal Engineer,
Calspan-University at Buffaio
Research Center,
Box 400,
Buffalo, NY 14225
J. Medige
Associate Professor,
Department of IVIecfianical Engineering,
State University of New Yori< at Buffaio,
Buffalo, NY 14260
Brain Tissue
The objective of this study was to determine a relationship between shear stress and
strain for human brain tissue by performing transient, single-pulse, high-rate, shear
displacement tests. A constant velocity, parallel plate shear test device was designed
and fabricated. This equipment generated constant rate shear strains in cylindrical
tissue samples mounted between the shear plates. The transverse reaction force at
the upper end of the sample was measured during the event with a sensitive quartz
piezoelectric force transducer, thus obtaining the force associated with the displace-
ment versus time ramp. Shear tests were performed on 125 tissue samples taken from
twelve fresh cadaver brain specimens. The average true shear stress and finite strain
were calculated. A nonlinear, viscoelastic, standard solid model was fit to the constant
rate test data and the material constants were determined.

Introduction velocity time history providing sample shear deformation with-

The existing body of knowledge concerning the mechanical
properties of human brain tissue has been derived primarily
from oscillatory testing of tissue samples and the measurement
of the frequency-dependent complex shear moduli. Debilitating
or fatal injury resulting from deformation of the brain is usually
caused by head impact with an unyielding surface. The most
common causes of injurious head impacts are automobile acci-
dents, although falls are also significant (Harris et al., 1983).
These events result in abrupt deceleration of the moving head
and the deformation of the brain due, primarily, to inertial
forces. These events are transient and nonperiodic: essentially
a single pulse. Oscillatory tissue testing may cause tissue dam-
age that alters the material response before, or while, force
measurements are made. Transient testing is more representa-
tive of the deformation that brain tissue undergoes in injury
producing head impacts. The development of inexpensive and
powerful microcomputers, high-speed digital data acquisition,
and servo-controlled linear motors has made the performance
of high strain rate, transient, translational, single-pulse shear
tests of human brain tissue possible.
Review of Previous Worli
The determination of the mechanical properties of human brain
tissue has been recognized as an important part of understanding
and modehng brain injury for many years. A series of studies
quantifying the mechanical properties of human brain tissue were
performed between 1954 and 1975 (Table 1). In all of these
studies it was assumed that human brain tissue is incompressible
(Stalnaker 1969; McElhaney et al, 1976) and the results were
usually presented in the form of frequency-dependent storage and
loss shear moduli. The ranges in the magnitudes measured for the
shear moduli in these studies are considerable.
Test Equipment
A parallel-plate shear testing system was designed and fabri-
cated (Donnelly, 1993; Donnelly and IVIedige, 1993) to provide
a constant-velocity shear displacement between a stationary up-
per horizontal shear plate and a moving lower horizontal shear
plate (Fig. 1). The lower plate is struck by an impacting cart
driven by a linear motor and undergoes a square wave, constant
Contributed by the Bioengineering Division for publication in the JOURNAL
OF BiOMECHANiCAL ENQINEERING. Manuscript received by the Bioengineering
Division, June 12, 1994; revised manuscript received April 16, 1997. Associate
Technical Eiditor: A. I. King.
out inertial stress due to acceleration. Primary instrumentation
consists of a piezoresistive crystal force transducer (Kistler In-
strument Corp. 9251 A) to measure the reaction force at the
upper shear plate and a velocity transducer (Trans-tek 100-001)
to record the lower shear plate velocity with respect to the upper
shear plate. The relative displacement versus time of the lower
shear plate with respect to the upper shear plate is obtained
by integrating the velocity versus time data obtained from the
velocity transducer. The maximum displacement of the lower
plate was set at the natural length of each sample, as measured
while submerged in saline, to give a maximum engineering
shear strain of 1.
Metliodology
Brain specimens were obtained from fresh human cadavers,
usually within 48 hours of death, which were kept under re-
frigeration during as much of that period as was possible. Sub-
jects were accepted only if there was no known pathology of
the head and brain.
A brain specimen consisted of the cerebrum of the brain
removed whole from the cadaver. The brain was exposed using
the standard technique for removal of the calvaria. The dura
and arachnoid were cut away, the brain stem was severed, the
cerebellum was removed, and the cerebrum was lifted out of
the skull. The brain specimen was immediately submerged in
stabilized isotonic saline at room temperature.
Samples were excised from the brain specimens immediately
after the specimens were removed from the cadaver. The cere-
brum was first split into right and left halves by cutting through
the corpus callosum and midbrain while the specimen was sub-
merged in saline solution. Samples were excised from the sub-
merged cerebral halves using stainless steel boring tools. The
submerged specimen was supported in one hand and the boring
tool was pushed slowly through the tissue with an oscillatory
rotary motion. All samples were cut from the cerebral halves
in a medial to lateral direction beginning at the corpus callosum
and midbrain and cutting outward to the cerebral surface. In
most cases six samples were obtained from each cerebral half
in the pattern shown in Fig. 2.
Trimming and measurement of the samples took place as
soon as possible after sample excision: in most cases within
three hours. IVIeasurements of the natural sample length and
diameter were performed while the samples were submerged in
saline solution at room temperature using a divider and a vernier
caliper. The samples were then refrigerated to 4C. Samples
were randomly assigned to groups for testing at the various
conditions.

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 Table 1 Summary of brain tissue shear properties* Samples were removed from refrigeration approximately one
hour prior to mounting and allowed to attain room temperature.
G'
Storage
G-
Loss
The selected sample was affixed to the shear plates using a methyl-
Modulus Modulus 2-cyanoacrylate adhesive (Measurements Group Inc. M-Bond 200
(kPa) (kPa-seo) Reference
adhesive). The final spacing between the upper and lower shear
Franke [19541
plates was set equal to the natural length of the sample after
1.5 oscillating glass sphere trimming. The transverse displacement in all tests was the same
125 - 500 Hz
as the sample natural length, resulting in a maximum engineering
Koeneman {1966] shear strain of 1 (assumed to be independent of axial position).
2.7 - 5.0 0.5-3.2 compiession
80 - 350 Hz Each brain tissue sample was tested once. The majority of tests
Galford and McElhaney [1969] were performed at four nominal engineering strain rates of 0, 30,
22.2 8.7 free axial vibration
34 Hz
60, and 90 s"' with several additional tests performed at 120 and
180 s"'. The actual strain rates were measured during testing and
Fallenslein, Hulce and
0 . 6 - I.l 0.35 - 0.60 Melvin [1969a, 19e9b] used in all subsequent calculations. All samples were shear tested
oscillating shear plates
10 Hz
to an engineering strain of 1, i.e., to an angle of 45 deg. The intent
of the experimental design was to develop a sufficientiy complete
Melz, McElhaney and
3 . 3 - 17.0 Ommaya [19701
matrix of tests at die 0, 30, 60, and 90 s"' strain rates to demon-
pressurized rubber probe strate the effect of sti-ain rate on sample stress response. Approxi-
compression
mately 30 tests were performed at each of these strain rates. Addi-
Estes and McElhaney [1970J
4.7 2.8-0.28 constant strain rate
tional tests were performed at the higher strain rates to determine
compression whether the expected dependency of stress on strain rate was
Shuck and Advani [1972] occurring at those higher rates.
8.0- 16.0 3.2-8.6 osciitatuig torsion
1 0 - 6 0 Hz The transverse displacement of the lower end of the sample
Shuck and Advani [1972]
versus time was obtained from the integration of the lower shear
7.0 7.0 oscillating torsion plate velocity. This displacement was divided by the natural
yielded, >60 Hz
length of the sample to obtain the engineering shear strain. The
19.5 11.2 Wang and Wineman [1972]
in vivo probe data
finite, or Lagrangian, shear strain for these displacements is one
half of the engineering shear strain (Fung, 1965; Sokolnikoff,
Ljung [1975]
1.7 0.92 transient rotation of a cylinder
1983). The average true shear stress in the incompressible de-
0.06 sec duration formed sample was calculated by dividing the measured force
by the reduced area of the sample due to stretching:
* In some cases moduli have b n calculated from reported quantities and unils have been converted to a
comparison.

Go + yt
A subjective descriptor of sample quality was assigned to each
where
sample. A sample that was solid, had a good cylindrical shape,
square ends, and a length of approximately one centimeter was a true shear stress
assigned a quality rating of good. A sample with a portion of a F shear force
sulcus in it, that was irregular in shape, or had a length of less a actual area of sample
than three quarters of a centimeter, was given a rating of poor. oo natural area of sample
Samples that were not clearly in either category were given a \ stretch ratio
rating of fair. 7^ engineering shear strain

Fig. 1 Drawing of the high rate shear test device: {A) upper fixed shear plate, (B) lower moving shear
plate, (C) impacting cart, (D) test cart, {E) sample cart with removable side plates

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 The stress response of the linear standard solid (Fliigge, 1967)
subjected to a constant rate strain is

a{t) = eo(<?, - p^qa){\ - e*-""!") + q^eot (2)

where

shear stress
time
constant shear strain rate
2aia2/(ai + 0^2)
2ai^/(ai + 02)
?/(: + ^2)
independent elastic shear constant
combined elastic shear constant
viscous shear constant.

This equation can be made nonlinear by attaching an exponent

to the right-hand side (Shames and Cozzarelli, 1992; Lockett,
1972)
Fig. 2 Sample locations
a{t) = {^eod - e"") + qotatV (3)

where

= (^1 - p^qa)
= Mp^
True stress was used in all calculations. Finite shear strain and
shear stress histories were calculated for each sample. The shear A quasi-static stress versus strain equation for the standard
stress versus finite strain responses from each test of each sam- solid can be found by considering the first term on the right-
ple were plotted and analyzed. hand side of Eq. (3) to be negligible for small eo and large ;
In order to make the stress versus strain results amenable to when compared to the second term, leaving
statistical analysis, each curve was fit with a two-parameter
power curve using weighted least squares: CT(0 = [qatat]" = {qae{t)] (4)
r7 = Ae (1) The result is a power equation very similar to the power equa-
tions (Eq. ( I ) ) developed for statistical analysis.
where A least-squares power curve fit of the quasi-static test data
(Eq. (4)), similar to that performed for statistical analysis,
e = finite shear strain provided the exponent, b, and the coefficient, qo, for each test.
A = coefficient The exponents and the coefficients for all of the quasi-static
B = exponent. tests were averaged to obtain the exponent and coefficient that
best represented all of the test results.
The stress value at each point was employed as a weighting The dynamic test data obtained from the higher rate shear
factor to give a better fit at higher stress levels. This procedure tests of 15, 30, 45, 60, and 90 s"' (engineering strain rates of
resulted in an exponent and a coefficient for each stress versus 30, 60, 90, 120, and 180 s"', respectively) were used to find
strain curve. The exponents were then averaged and each data the remaining parameters tfj and a. The last term on the right-
set was fit with a single-parameter least-squares power curve hand side of the nonlinear stress versus strain equation (Eq.
having the average exponent as the exponent in each case. This (3)) was obtained previously from the quasi-static curve fitting.
procedure yielded a set of power curves, all having the same This term was subtracted from both sides to obtain an exponen-
exponent, and each having a coefficient that represented the tial function for the time dependent response of the tissue alone:
amplitude of the corresponding stress versus strain curve. The
amplitude, which was used in statistical analysis, is a single a(0' goe(0 = 'Aeo(] - e - " ' ) . (5)
number that characterizes the stress versus strain curve from
which it is derived.
The amplitudes of each of the stress versus strain curves
obtained from all of the tests were analyzed statistically.
Initially, the means, standard deviations, and coefficients of
variation were calculated and compared. The amplitudes were
then examined in a two-factor analysis of variance. Addi-
tional analyses were performed to examine the effects of
sample location and sample quality. Finally, strain rate effect
was examined in a multiple comparison test to ascertain
whether a strain rate effect existed between and among all
of the rates tested.
a
A nonlinear standard viscoelastic solid model provided a bet-
ter representation of the stress versus strain response of brain
tissue than did several other models considered. The linear stan-
dard solid viscoelastic model is comprised of an elastic element
in series with a two-element Kelvin-Voigt model (Fig. 3). Fig. 3 Standard solid linear viscoelastic model

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 The stress versus strain data were manipulated into the form of
Eq. (5) by raising the measured stress, a(t), to the power, l/b,
and subtracting from it the modeled quasi-static stress response.
This remaining stress was considered to be the dynamic contri-
bution. Plots of this dynamic stress as a function of time yield
exponential curves consistent with model predictions. The mod-
ified stress curves at each strain rate were averaged by summing
the stress values at each time point and dividing by the number
of tests contributing to that sum. The resulting average dynamic
stress versus time history curve was divided by the finite strain
rate to obtain a data set that represented a normalized time
function applicable to all tests at all rates. This data set was fit
to an exponential equation having the form of Eq. (5) to find
ij/ and a.
The constants, a, b, ip, and qo, found by fitting the stress
versus strain curves obtained from the brain tissue testing to
the constant strain rate equation (Eq. (3)) were then used to
calculate the material constants, a^, a2, and ^, for a nonlinear
viscoelastic solid similar to that shown in Fig. 3.
Results
Twelve human brain specimens were obtained from fresh
human cadavers over a nine month period. The subjects ranged
from 49 to 95 years of age with an average age of 77 years.
Seven subjects were female and five were male. All but two
subjects were obtained within two days of death with two being
obtained within three days of death. Sample testing occurred
within one day of subject acquisition except in two cases when
sample testing occurred within two days of subject acquisition.
No attempt was made to quantify the effects of sex or age on
the results.
The twelve fresh human brain specimens yielded 143 brain
tissue samples. Due to losses during the mounting and testing
operations it was possible to generate useful results from a total
of 125 samples. Sample lengths ranged from 0.53 to 2.64 cm
with a mean of 1.20 and a standard deviation of 0.15. The cross-
sectional area of the samples ranged from 1.19 to 2,85 cm^ with
a mean of 2.32 and a standard deviation of 0.10.
All samples shrunk slightly upon excision from the brain
specimen. The reduction in diameter was approximately 12 per-
cent of the boring tool diameter.
The samples obtained from the midbrain region (location
number one in Fig. 2) contained mixed white and gray tissue.
Samples obtained from the other locations were predominantly
white tissue with occasional bits of gray tissue from the cerebral
cortex randomly included. The gray tissue from the cerebral
cortex expanded after cutting while the gray tissue from the
midbrain remained smooth and conformed to the cylindrical
shape of the sample. No attempt to quantify effects of gray and
white tissue was made.
The shear force versus time curves generally increased mono-
tonically from zero newtons (at time zero) to approximately
two newtons at maximum displacement. The smallest shear
force measured at maximum displacement was 0.07 newtons
for a sample tested at 0.34 s^' while the largest was 2.16 new-
tons for a sample tested at 59.5 s~'. The maximum shear dis-
placement for each sample was always the length of the sample.
Figure 4 presents plots of typical quasi-static and dynamic
shear stress versus strain response. The two-step power curve
fitting process (Eq. (1)) resulted in an average exponent of
1.28 that provided the best fit for all of the stress versus strain
curves. The amplitudes (Eq. (1)) ranged from 1070 pascals for
a quasi-static test to 33,500 pascals for a dynamic constant rate
test. A summary of the power curve fit statistics is presented
in Table 2, including means, standard deviations, and coeffi-
cients of variation of the sample population. It can be seen that
the average of the first power curve exponent is greater than
1.0 in all cases except the 30 s"' tests where the power curve
is almost a straight line. It can also be seen that the coefficients
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of variation of the second power curve coefficients are smaller
than the coefficients of variation of the first power curve coeffi-
cients in all cases. The standard error of the fit was calculated
for each case and the error for the second power curve fit was
not appreciably larger than that of the first power curve fit. The
second set of fitted power curves with the common exponent
of 1.28 and a coefficient representing the amplitude of the stress
versus strain response for each test are a good representation
of the test results and provide a single number measure of the
entire stress versus strain curve that is amenable to analysis of
variance.
The summary statistics presented in Table 2 indicate that
the mean amplitudes (second coefficients) for each strain rate
generally increase as the strain rate increases. The mean ampli-
tude for the 120 s~' tests does not follow this trend. Only a
few samples were tested at the higher strain rates of 120 and
180 s~' and the mean amplitudes are not as reliable as those
calculated for the other strain rates. The mean amplitude in-
creases substantially as strain rate increases from 0 to 90 s^'
and exhibits only a small additional increase as the strain rate
increases from 90 to 180 s~'. As is common with biological
tissue, there is a considerable amount of variance in the results
with coefficients of variation ranging from 0.25 to 0.66.
Plots of the stress versus strain curves from the tests at each
strain rate are shown in Figs. 5, 6, 7, and 8 along with the mean
power curves and the plus and minus one standard deviation
curves.
A two-way analysis of variance was performed on a matrix
of the amplitudes (second power curve coefficients) associated
with each stress versus strain curve. The stress amplitude was
the dependent variable and the strain rate and brain specimen
were the main factors in this analysis. The criterion of signifi-
cance for this experiment was set at 0.05 and the null hypotheses
were: (1) The amplitude does not increase when the strain rate
increases, (2) the amplitude does not vary with respect to the
brain specimen and (3) the amplitude does not vary with respect
to a combination of the brain specimen and the strain rate. The
results of this analysis indicated that the first two null hypothe-
ses should be rejected while the third should be accepted: The
stress amplitude is related to strain rate and to brain specimen
but not to the interaction of the two factors.
The proportion of the variance in the dependent variable that
is due to each of the main effects of strain rate and brain speci-
men was examined using a procedure for estimating the magni-
tude of experimental effects (Winer, 1962; Fleiss, 1969). This
procedure indicated that 47 percent of the variance was due to
the strain rate effect and that 30 percent of the effect was due
to the brain specimen effect. The remaining 23 percent of the
variance is assumed to be due to experimental error.
The power of this experiment was assessed using the tech-
niques and tables of Cohen (1988). For both the brain specimen
effect and the strain rate effect the power was found to be
greater than 0.94. For the interaction effect, a power of 0.34
was calculated.
There were no trends in the results due to sample quality and
location. The multiple comparison testing indicated that a strain
rate effect existed between 0 s~' rate and each of the higher
rates and between the 30 s"' rate and the 90 s"' rate. No rate
effect was found between the 60 s~' rate and the 90 s"' rate.
The higher rates were not tested due to an insufficient number
of tests at those rates.
The parameters resulting from curve fitting the quasi-static
data sets to the nonlinear quasi-static stress versus strain equa-
tion (Eq. (4)) were the stress power, b = 1.45, and the long-
term elastic modulus qo = 381. The parameters resulting from
curve fitting the dynamic test data to the nonlinear dynamic
stress versus strain equation (Eq. (5)) were the retardation con-
stant, a = 89.5, and the viscous coefficient, i/f = 8.06. The
shear stress versus strain equation for a constant rate strain
displacement derived from a three element nonlinear viscoelas-
Transactions of the ASME
 Shear Stress versus Strain

5000
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4000

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yH^ ^^
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Finite Shear Strain

Fig. 4 Test data from brain specimen BOS

tic solid model (Eq. (4)) and the shear test response of human State University of New York at Buffalo through a willed body
brain tissue is program. It generally took one or two days for the subjects to
become available. Specimen removal, sampling, and testing
a{t) = [8.06 eo(l - e-^"") + 381 (?)]''*' (6)
took place as soon as possible after subject acquisition; how-
Figure 9 shows the nonlinear model representation of the stress ever, several days inevitably passed between death and testing.
versus strain response for each of the strain rates employed in When two subjects became available simultaneously an extra
this study overplotted with the average power curves shown in day was required before testing could take place. Testing oc-
Figs. 5, 6, 7, and 8. curred between two and five days after death in all cases. Sub-
Returning to the phenomenological model (Fig. 3) the con- jects, specimens, and samples were kept refrigerated and in
stants associated with each element were determined from the saline, as appropriate, at all times.
parameters found by curve fitting. The model constants are The approach of coring cylindrical samples from the midbrain
a, = 550 Pa and corona radiata regions of the brain was selected as the
optimum method for obtaining a sufficient number of reason-
a2 = 291 Pa ably sized and dimensionally stable samples to perform a good
, = 9.40 Pa-s (7) experiment. The reasons for selecting this approach were (1)
the need to obtain a large number of samples from a limited
Discussion number of specimens, (2) the need for a physical sample size
The subjects from which the brain specimens were obtained that would generate a measurable force response, and (3) the
were donated by the Department of Anatomical Sciences of the need for a regular sample shape with dimensions that could be
accurately measured. The cored cylindrical sample approach
has been used successfully in many previous studies (Metz et
Table 2 Summary statistics for a power curve fit of stress versus strain
a l , 1970; Estes and McElhaney, 1970; Galford and McElhaney,
A'
1969; Koeneman, 1966).
Test No. Measure B* B* A"
(1st flt) (1st nt) (2nil fit) (2na nt) Samples were generally of a good right circular cylindrical
Quasi- 30 Mean 1.43 6015 1,28 4697 shape and predominantly made up of white tissue. Some sam-
static St. Dev. 0.48 4885 3100 ples contained gray matter from the cerebral cortex, which ex-
Coet. ofVar. 0.34 0.81 0,66
panded after excision and gave the sample a somewhat irregular
3ft sec'* 27 Mean 0.98 8473 1,28 11707
St. Dev. 0.27 4447 5835 shape. This phenomenon resulted in that sample receiving a
Coef. of Var. 0.28 0.52 0,50 poor quality rating. Some samples contained gray matter from
60 sec' 31 Mean 1.16 14926 1.28 14880 the basal ganglia, which did not affect the sample shape at all.
St. Dev. 0.29 13464 7267
Coef. of Var. 0.25 0.90 0.49 Many samples contained a part of a sulcus somewhere along
90 sec"' 26 Mean 1.50 20377 1,28 17049 the surface of the sample. It was not possible to avoid all sulci
St. Dev. 0.66 10371 6303 and still obtain samples of a physical size large enough for
Coef of Var. 0.44 0.51 0.37
testing. The inclusion of a part of a sulcus in a sample resulted
120 sec' 7 Mean 1.50 17027 1,28 12596
St. Dev. 0,49 8055 3195 in that sample receiving a poor quality rating.
Coef of Var. 0.32 0.47 0,25
The human brain is not a homogeneous structure and the
180 sec' 4 Mean 1.12 20057 1,28 18665 tissue of the brain is, most likely, not isotropic. This study
St. Dev. 0.55 19691 8741
Coef of Var. 0.49 0,98 0.47 intended to determine the average shear properties of human
* A and B efer to t he parameters of equation (1) brain tissue for purposes of mathematical modeling of the head

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 Shear Stress vs Finite Strain

Fig. 5 Quasi-static stress versus strain curves overplotted with average power curves

undergoing an abrupt acceleration. The assumptions of homoge-
neity and isotropy were made with an understanding of the
shortcomings that were inherent in the experimental design. The
sampling that was done in this study was intended to provide
sufficient diversity in location that the results, when averaged,
would be representative of all brain tissue without modeling
any particular type of tissue exactly. The fact that all samples
were cut in a medial to lateral direction may have biased results;
however, samples were mounted randomly and the direction of
the shear displacement, while always in a sagittal plane, was
otherwise random.
The brain tissue tested in this experiment was a very soft solid
that could be easily damaged while handling. When immersed in
saline, a tissue sample had a clearly defined shape that it would
return to after being slightly deformed. This characteristic of a
solid was not so evident when the tissue sample was removed
from the liquid. Out of liquid the tissue deformed considerably
under its own weight and would tear if not supported uniformly.
The brain tissue was slippery when the surface was wet and cut
easily with only very slight pressure; however, when the surface
dried the tissue became very sticky and would adhere to almost
any other dry surface. All tools and gloves were wetted before
handling the tissue.
In the Shuck and Advani (1972) study of the shear material
properties of brain tissue the maximum strain rate was 77 s"'
and the maximum strain was 0.35. At the University of Pennsyl-
vania (Thibault and Gennarelli, 1987) studies have been per-
formed with giant squid axons that suggest a strain of 0.05 at

Shear Stress vs Finite Strain

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i ; i j I i ^. 1: .;.".....;....

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.
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:
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Finite Strain

Fig. 6 Stress versus strain curves from 30 s ' tests overplotted with average power curves

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 Shear Stress vs Finite Strain

Fig. 7 Stress versus strain curves from 60 s ' tests overplotted with average power curves

a strain rate of 45 s"' and a strain of 0.30 at a strain rate of
90 s"' are thresholds of concussion and diffuse axonal injury,
respectively. A subsequent study (Margulies et al., 1990) uti-
lized silicone gel brain models in human and baboon skulls to
photographically measure strains larger than 0.2 when the head
was exposed to an angular acceleration pulse. Bycroft (1973)
performed an analytical study based on the work of Thomas
(1970) that suggests a strain of 0.05 at a strain rate of 18 s"'
is the threshold for concussion. Troseille et al. (1992) modeled
head impacts experienced by boxers using a finite element
model developed at General Motors (Lighthall et al., 1989) and
estimated that strain above 0.15 would result in serious brain
injury and strain above 0.20 would be fatal. The strain and
strain rates chosen for this experiment were comfortably larger
than these values found in the literature. It was assumed that
testing to a strain of 1.0 would provide a valid force response for
all strain values less than 1.0. If evidence of yielding appeared in
the force data, the curves could be truncated accordingly. This
proved not to be the case and all of the data up to and including
a strain of 1.0 were utilized for model development.
Because the material is nearly incompressible, the cross-sec-
tional area of the sample is reduced as the transverse displacement
increases and the sample is stretched. At the sample ends the
adhesive attaching the sample to the end plates prevents this reduc-

Shear Stress vs Finite Strain

.250

Finite Strain

Fig. 8 Stress versus strain curves from 90 s ' tests overplotted with average power curves

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 tion in area from occurring by applying a radial stress over the
cross section. The transverse reaction force measured at the upper
sample end is the same as the shear force at every cross section
of the sample due to equilibrium. The shear stress over the cross
section varies with location (Donnelly, 1993; Donnelly and Med-
ige, 1993) and, therefore, is affected by the changing area of the
cross section near the end plates. It is assumed that the end effects
are rapidly diminished as the distance from the end of the sample
increases due to the principle of St. Venant, and that the calculated
average true shear stress at every cross section is constant over
most of the sample length. Similarly, the shear strain is related to
the shear stress and varies over the cross section of the sample.
The shear strain is also affected by the end conditions with a
maximum shear strain occurring at the trailing edge of the sample
cross section on the upper plate and the leading edge of the sample
cross section on the lower plate. Again, due to the principle of St.
Venant, it is assumed that the end effects diminish rapidly and the
average finite shear strain is constant at every cross section over
most of the length. Because the stress and strain found in this
experiment are average values over the cross section of the sample,
the effects that the end conditions have on the stress and strain
are thought to be insignificant.
A review of the stress versus strain curves obtained from the
shear tests indicated a trend of increasing slope with increasing
strain. This characteristic shape has been noted by other investi-
gators (Metz et al., 1970; Estes and McElhaney, 1970; Galford
and McElhaney, 1969). This curve shape suggested a polyno-
mial, an exponential, or a power curve as being likely candidate
functions for curve fitting. All of these function types were
fitted to the data and the standard errors calculated. In general,
all of these functions fit the data reasonably well. The power
curve has the advantage of naturally passing through zero, as
do the data. It was also known that the form of the power curve
equation was the same as the form of the quasi-static stress
versus strain equation for the three-element nonlinear standard
viscoelastic solid model subjected to a constant rate strain.
Examination of the stress versus strain curves, for all samples
at all strain rates, revealed that all of the curves had approxi-
mately the same shape with the major difference being in the
amplitude. This observation indicated that a single exponent
might fit all of the stress versus strain curves fairly well with
only the coefficient varying for each curve. This approach was
ideally suited to the analysis of variance where a single number
measure that is characteristic of the entire stress versus strain
curve could be studied.
Each stress versus strain curve was fit with a power curve in
a two-step, ordinate weighted, least-squares curve fitting process
as discussed previously. The standard errors calculated from
the second step fit were similar in size to the standard errors
calculated from the first step fit. This indicates that the curve
fits obtained using the common exponent were nearly as good
a representation of the data as were the curve fits obtained from
the first step of curve fitting. The resulting coefficients found
for each stress versus strain curve are characteristic of the entire
curve and are used for statistical analysis of the data. These
characteristic amplitudes are useful for calculating means, stan-
dard deviations, and coefficients of variation, and are direct
inputs to the analysis of variance.
The statistical analysis indicated that although there was con-
siderable variance in the data, the stress versus strain response
of human brain tissue is dependent on the strain rate. No effects
were found for sample location or sample quality. The fact that
the multiple comparison test was unable to differentiate between
the 60 s ' rate and the 90 s~' rate may be due, in part, to the
decreasing size of the effect at the higher rates causing the
effect to be obscured by the brain to brain differences.
The characteristic amplitudes are also useful for comparisons
to previous brain tissue studies where investigators report the shear
storage and loss moduli. The average amplitude of the quasi-static
stress versus strain data can be used to approximate the slope of
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a straight line representing the shear storage modulus. A least-
squares fit of a straight line yields an approximate shear storage
modulus of 1810 pascals for this study after adjusting to engi-
neering strain rather than finite strain. Fallenstein et al. (1969a, b)
reported a shear storage modulus ranging from 600 to 1100 pas-
cals. Shuck and Advani (1972) reported an average shear storage
modulus of 7170 pascals for low-frequency tests at low strain. At
strains greater than 0.035, Shuck and Advani suggest yielding
occurs and the shear storage modulus is reduced to approximately
5000 pascals. Ljung (1975) found an elastic shear modulus of
1700 pascals in an unusual transient rotation experiment in which
data were obtained by digitizing high-speed film. The approximate
value of elastic shear modulus found from this testing of 1800
pascals is in the middle of the range of reported values.
Comparison of the amplitudes obtained from the dynamic
shear tests and the reported dynamic loss moduli obtained from
oscillatory tests is more difficult because the two-element Kel-
vin-Voigt viscoelastic model does not fit these transient data
very well. If the average quasi-static slope is subtracted from
the average dynamic slopes of the higher rate tests, the result
would be the stress versus strain response due to the viscous
nature of the material. Integration of this stress versus strain
curve with respect to strain yields an estimate of the energy
dissipated per unit volume during the event. For a Kelvin-
Voigt model, the energy dissipated in a constant rate strain test
is the product of the viscous constant, the strain rate, and the
strain. Equating these two energy expressions and solving for
the viscous constant provides an estimate of a viscous constant
for the transient tests performed in this study that can be com-
pared to loss modulus results from other studies when they are
multiplied by the appropriate test frequency.
Table 3 shows the estimated viscous constants for the 30, 60,
90, 120, and 180 s"' strain rate tests. As before, these values
have been adjusted to reflect the use of the engineering strain.
The fact that the values obtained for the viscous constant are
not the same at the different strain rates indicates that a linear
Kelvin-Voigt model is not representative of the brain tissue
shear response found in this study.
Shuck and Advani (1972) reported an average loss modulus
of 2280 pascals at frequencies from 2 to 10 hertz. This is compa-
rable to a viscous constant ranging from 182 to 36 paScal-
seconds. These investigators also reported a loss modulus of
approximately 7500 pascals for tissue strained more than 0.035
that was fairly constant at all frequencies from 100 to 350 hertz.
This value is comparable to a viscous constant ranging from 12
to 4 pascal-seconds. Fallenstein et al. (1969a, b) reported a loss
modulus ranging from 350 to 600 pascals at 10 hertz. This is
comparable to a viscous constant ranging from 6 to 10 pascal-
seconds. Ljung (1975) found a viscous constant ranging from
7.6 to 12.4 pascal-seconds in his transient rotation test, which
encompassed strain rates from 0 to 180 s ~'. As with the storage
moduli, the loss moduli from the various studies show a range
of values with the results from this study being comfortably
within that range.
A nonlinear viscoelastic standard solid model was formulated
that fit the basic characteristics of the stress versus strain curves
generated from the shear tests performed in this program. Only
Table 3 Estimated viscous constants
Engineering Estimated Viscous
Strain Rate Constant
(.sec-') (pascal-sec.)
30 45
60 33
90 26
120 13
180 15
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 Shear Stress versus Strain
6500
5000
3500
2500
Fig. 9 Average power curves and modeled curves:
solid models were considered because the material behaved like
a solid in the laboratory. Liquid models would most likely fit
the dynamic data fairly well but would be unlikely to model
the quasi-static results. The first and simplest model considered
was the two-element solid (Kelvin-Voigt). It quickly became
apparent that the stress versus strain response of human brain
tissue did not increase linearly with strain rate as this model
would predict. The three-element standard solid also has the
desirable characteristic of zero stress at zero strain regardless
of the strain rate. Because the nonlinear standard solid model
was found to fit the data well, more complicated models such
as generalized Kelvin-Voigt models (Shames and Cozzarelli,
1992) were not considered.
Comparison of the average power curves at each strain rate
and the nonlinear viscoelastic model curves at each strain rate
(Fig. 9) indicate that the model is a good representation of the
shear stress versus strain response of human cadaver brain tissue
over the range of strain rates tested.
The determination of the model parameters that were depen-
dent on the quasi-static response of the tissue were found
through a straightforward exercise in fitting power curves to
the test results. The validity of neglecting the dynamic portion
of the stress for quasi-static tests can be verified by calculating
the dynamic stress, from Eq. (5), for a typical quasi-static strain
rate of 0.3 s ' and a test duration of 3 s. It can be seen that the
dynamic part of the stress is less than 1 percent of the static
part of the stress under these conditions.
The determination of the model parameters that were depen-
dent on the dynamic response of the tissue were found by fitting
an exponential curve to the dynamic data less the quasi-static
data using the Fung (1984) technique of fitting the first deriva-
tive of stress with respect to time as a linear function of stress
over the duration of the event.
Conclusion
The human brain is a complex structure made up gray
matter, white matter, blood vessels, membranes, fissures, and
voids surrounded by, or filled with, cerebrospinal fluid. The
quantification of mechanical properties for each of these tis-
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power curves; model curves
sues would be an enormous undertaking equaled only by the
effort required to develop a mathematical model capable of
utilizing these disparate mechanical properties. In order to
develop a brain tissue stress versus strain relationship that is
useful for modeling the head with state-of-the-art finite ele-
ment models, and to further the process of relating brain
deformation and injury to head impact, the brain was assumed
to be a continuous, isotropic, homogeneous entity that be-
haves according to the theory of viscoelastic materials.
Because the bulk modulus of brain tissue aXK = 2100 MPa
(Stalnaker, 1969; McElhaney et al., 1976) is approximately
10' times larger than the shear modulus, brain tissue is nearly
incompressible and the deformation of brain tissue can be
assumed to depend on the shear modulus only. This behavior
is common with viscoelasric materials (Shames and Cozzarel-
li, 1992). Determination of a phenomenological model for the
viscoelastic shear response will completely characterize the
stress versus strain behavior of human brain tissue when gener-
alized to three dimensions.
The stress versus strain results from the tests performed in
this study were not significantly dependent on the sample loca-
tion within the brain or on the sample condition. There was;
however, significant variance among samples obtained from
different subjects. A strain rate effect was clearly evident for
brain tissue over the range of loading rates tested in this study.
The stress versus strain relationship is nonlinear with increasing
slope as strain increased and increasing slope as strain rate
increased. The stress versus strain results from this study are
within the range of results reported from previous studies.
The stress versus strain data from this study were fitted to a
single nonlinear viscoelastic solid model that can aid in under-
standing the response of brain tissue.
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Transactions of the ASME