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Epilepsia, 49(2):189200, 2008
doi: 10.1111/j.1528-1167.2007.01378.x
CRITICAL REVIEW AND INVITED COMMENTARY
Diffusion-based magnetic resonance imaging and
tractography in epilepsyMahinda Yogarajah and John S. Duncan
Department of Clinical and Experimental Epilepsy and National Society for Epilepsy, Institute of Neurology,
University College London, Queen Square, London, United Kingdom
SUMMARYDiffusion-based imaging is an advanced MRI tech-
nique that is sensitive to the movement of water
molecules, providing additional information on the
micro-structural arrangement of tissue. Qualita-tive and quantitative analysis of peri, post and in-
terictal diffusion images can aid the localization of
seizure foci. Diffusion tensor tractography is an ex-
tension of diffusion-based imaging, and can provide
additional information about white matter path-
ways. Both techniques are able to increase under-
standing of the effects of epilepsy on the structural
organization of the brain, and can be used to opti-
mize presurgical planning of patients with epilepsy.
This review focuses on the basis, applications, lim-
itations, and future directions of diffusion imagingin epilepsy.
Literature search strategy: We searched Pubmed
using the terms diffusion MRI or diffusion tensor
MRI or tractography and epilepsy.
KEY WORDS: Diffusion, Diffusion tensor, MRI,
Tractography, Ictal, Postictal.
Magnetic resonance imaging (MRI) is central to the as-
sessment of individuals with refractory epilepsy, enabling
the identification of the underlying epileptogenic substrate,and if surgical treatment is considered, depicting the rela-
tionship of the epileptogenic lesion and zone to eloquent
areas of the brain such as the motor, language, or memory
areas.
Diffusion-based MRI and tractography can provide valu-
able information in the evaluation of an individual with
epilepsy. Diffusion-based MRI has the potential to identify
potentially epileptogenic abnormalities, including those
that appear normal on standard MRI sequences. Tractog-
raphy may be used to map white matter tracts, and their
relationship to epileptogenic tissue and eloquent cortex.
This information may be used to improve surgical plan-ning in order to minimize postoperative deficits including
memory, language, and visual field loss. Furthermore, it
also has the potential to aid understanding of the acute
Accepted August 31, 2007; Online Early publication October 18, 2007.
Address correspondence to Prof J. S. Duncan, Department of Experi-mental and Clinical Epilepsy, Institute of Neurology, University CollegeLondon, Queen Square, London WC1N 3BG, United Kingdom E-mail:
j.duncan@ion.ucl.ac.uk
Blackwell Publishing, Inc.C 2008 International League Against Epilepsy
and chronic pathophysiological effects of seizures on the
brain.
THE BIOLOGICAL AND PHYSICALBASIS OF DIFFUSION IMAGING
In a free medium the molecular diffusion of water refers
to the random translational motion (Brownian motion)
of molecules resulting from the thermal energy carried
by these molecules. In the brain, diffusion is restricted
by intra- and extracellular boundaries, and represents the
effects of several variable, independent factors. These
include the presence of impermeable or semipermeable
membranes (Hansen, 1971), macromolecules that hinderthe diffusion of small molecules, and intra- and extracel-
lular microcirculatory effects (Le Bihan et al., 1992; Le
Bihan & Turner, 1992). The measurement of water dif-
fusion therefore provides a means of probing cellular in-
tegrity and pathology (Le Bihan, 2003).
The principles of diffusion MRI were first developed in
vivo in the mid 1980s (see Le Bihan, 1995 for review).
In diffusion-weighted imaging (DWI), images are sensi-
tized to the diffusional properties of water by the incorpora-
tion of pulsed magnetic field gradients into a standard spin
echo sequence (Merboldt et al., 1985; Taylor & Bushell,
1985). By taking measurements in at least three directions,
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M. Yogarajah and J. S. Duncan
it is possible to characterize the mean diffusion properties
within a voxel in the image by way of a single scalar ap-
parent diffusion coefficient (ADC). Early diffusion studies
discovered that ADC measurements depended on a sub-
jects orientation relative to the magnet and gradient coils
(Hajnal et al., 1991). White matter tracts parallel to an ap-plied gradient had the greatest ADC whereas those lying
oblique or transverse to a gradient had smaller ADC val-
ues. This gave rise to the concept of asymmetry of diffusion
of molecules in three directions, or anisotropy (Basser,
1995).
Diffusion tensor imaging (DTI) enables not only the
quantification of water molecule diffusion, but also the
characterization of the degree and direction of anisotropy
(see Le Bihan et al., 2001 for review). The diffusion tensor
is a mathematical construct that can be calculated from a
nondiffusion-weighted image plus six or more diffusion-
weighted measurements along noncollinear directions. Thetensor can be diagonalized to give three eigenvectors, 1,2, and 3 representing the principal directions of diffu-
sion, and three eigenvalues 1, 2, and 3 representing the
magnitude of diffusion (or the corresponding ADC values)
along these directions. Furthermore, a number of diffusion
parameters can be derived in each voxel, which are insensi-
tive to subject positioning and fiber tract alignment within
the diffusion gradients of the MRI scanner (Basser et al.,
1994; Pierpaoli et al., 1996). Mean diffusivity (MD) is a
summary measure of the average diffusion properties of a
voxel and is equivalent to the estimated ADC over three
Figure 1.
(A) Axial diffusion-weighted image. The dark end of the gray scale represents areas of increased diffusion, and the
bright end areas of restricted diffusion. Diffusion is greatest in the CSF, which therefore appears dark. Diffusion-
weighted images are T2 sensitive, such that bright regions of high T2 signal that are not diffusion restricted persist
in the diffusion-weighted images (T2 shine through). For this reason the calculation of an ADC map that is
independent of this effect is useful. Bright T2 signal and decreased ADC drive DWI signal intensity up whereas low
T2 signal and high ADC drive DWI signal intensity down. (B) Axial ADC map describing the ADC value in each
voxel. The bright end of the gray scale represents increased diffusion, and the dark end areas of decreased diffusion.
Diffusion is greatest in the CSF, which therefore appears bright. (C) Fractional anisotropy map describes the degree
of diffusion anisotropy in each voxel. In white matter where anisotropy is high the bright end of the gray scale is
assigned. In gray matter where anisotropy is low, the dark end of the gray scale is applied.
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orthogonal directions. Fractional anisotropy (FA) on the
other hand is an estimate of what proportion of the mag-
nitude of the diffusion tensor is due to anisotropic diffu-
sion. Quantitative maps of these parameters can also be
constructed, and used to make comparisons between indi-
viduals or populations (Fig. 1).Diffusion anisotropy in cerebral tissue is highly hetero-
geneous due to several factors including, the concentration
of macromolecules and intracellular organelles, regional
differences in the density of nerve fibers, the degree of
myelination, fiber diameter and the density of neuroglial
cells (Beaulieu, 2001). Anisotropy in white matter results
from the organization of tissue as bundles of axons and
myelin sheaths run in parallel, and the diffusion of water
is freer and quicker in the long axis of the fibers, than in
the perpendicular direction (Beaulieu, 2001). Malforma-
tions or acquired insults cause disruption to the microstruc-
tural environment, and more often than not, a subsequentreduction in anisotropy. Such abnormalities may also lead
to a reduction in cell density and/or expansion of the extra
cellular space, resulting in an increase in MD/ADC.
PER I- AN D POSTICTAL CHANGES INDIFFUSION
Seizure-associated changes in diffusion parameters are
not static, but have a dynamic profile. These changes are
observed in both animal and human studies, and generally
show a pattern of early postictal depression, followed by
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Diffusion-based MRI and Tractography in Epilepsy
normalization, and then transient or chronic elevation of
the ADC/MD (Righini et al., 1994).
Animal studies
A considerable body of animal data has shown that
diffusion-weighted MRI can visualize the histopathologi-cal changes that result from seizures in animal models. The
first reported study, by Zhong et al., demonstrated a fall of
15% in the ADC in bicuculline-induced status epilepticus
in rats (Zhong et al., 1993). Other models have shown sim-
ilar reductions in ADC values that are in proportion to the
severity of seizure activity (Prichard et al., 1995; Zhong
et al., 1995, 1997).
The ictal and postictal changes seen in the ADC are sim-
ilar to those seen in cerebral ischaemia, and both share a
common biological basis, namely the loss of membrane
function and ion homeostasis. Cerebral ischaemia leads
to a failure of energy metabolism, membrane dysfunction,and cell death. Sustained seizures on the other hand lead
to an increased metabolic rate. This is coupled to an in-
crease in cerebral blood flow (Szabo et al., 2005), so that
cellular energy values are close to normal, though in pro-
longed ictal activity, the increased metabolic activity may
not be matched by enhanced blood flow (Bruehl et al.,
1998). The early ADC decline seen in prolonged seizures
is thought to reflect cytotoxic oedema (Wang et al., 1996),
and a decrease in the extra cellular space volume frac-
tion of up to 30% at the area of maximum neuronal activ-
ity in the cortex (Lux et al., 1986). This in turn leads to
increased extracellular tortuosity and decreased diffusiv-
ity. Seizures cause increased membrane ion permeability
(McNamara, 1994) leading to an influx of sodium, cal-
cium, and water along the osmotic gradient (Wang et al.,
1996), which cannot be compensated for by an energy de-
ficient sodiumpotassium ion ATP pump. Intracellular cy-
toskeletal fragmentation that increases intracellular tortu-
osity and viscosity, may also contribute to restricted diffu-
sion (van der Toorn et al., 1996).
While cytotoxic oedema is the most common patho-
physiological effect of seizures found in cortical gray mat-
ter, vasogenic oedema has also been reported less com-
monly in subcortical white matter (Tanaka et al., 1992).
Animal studies have demonstrated that seizures can alsotrigger acidosis and the breakdown of the blood brain bar-
rier (Nitsch & Klatzo, 1983). This, together with local va-
sodilatory effects, can give rise to vasogenic oedema and
an increase in intercellular space and diffusivity (Nedelcu
et al., 1999).
Though cytotoxic oedmatous changes are not necessar-
ily irreversible, with prolonged seizures, diffusivity and the
ADC can change permanently (Nedelcu et al., 1999). Ex-
citotoxic mechanisms mediated by excitatory amino acids,
calcium influx, ATP depletion, and lactate accumulation
eventually lead to cell atrophy and death (Wasterlain et al.,
1993). This cell lysis results in an increase in extracellu-
Figure 2.
(Adapted with permission from Wieshmann et al., 1997)
DWI in a patient with complex partial status epilepticus
affecting the right leg. Decreased diffusion is visible in
the motor cortex, and increased diffusion is visible inthe subcortical white matter. This corresponded to
a relative decrease in ADC of 27% and increase in
ADC of 31% in the cortical and subcortical tissue,
respectively.
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lar space and an increase in diffusion above normal values,
which correlates with histopathological changes in both the
seizure focus and secondarily affected areas (Pitkanen et
al., 2002; Hasegawa et al., 2003).
Clinical studies
Status epilepticus
Early clinical studies assessed diffusion-weighted imag-
ing in patients with status epilepticus. In a patient with
focal motor status epilepticus consisting of clonic jerking
of the right leg, a 27% relative decrease in the ADC was
demonstrated in the motor cortex of the right leg (Wiesh-
mann et al., 1997). There was also a 31% relative increase
in the ADC of the subcortical white matter (Fig. 2). This
finding was thought to represent a shift of water into corti-
cal cells at the seizure focus, and a shift of water into ex-
tracellular space in remote white matter due to vasogenicoedema (Lux et al., 1986). Similar findings in other case
reports hint at the complex osmotic relationship between
epileptogenic and surrounding areas, and cytotoxic and va-
sogenic oedema (Kim et al., 2001; Hong et al., 2004).
Other studies have broadly corroborated these results in-
cluding a small case series, where cortical ADC reductions
of up to 36% were found during partial status epilepticus
(Lansberg et al., 1999).
Early clinical reports also suggested that there were
significant correlations between the areas of diffusion
abnormalities, and increased perfusion and electrocortico-
graphic abnormalities (Diehl et al., 1999; Flacke et al.,Epilepsia, 49(2):189200, 2008
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M. Yogarajah and J. S. Duncan
2000; Calistri et al., 2003). In a study of 10 patients with
complex partial status epilepticus there was correlation
between focal swelling and hyperintensity on T2-weighted
images and increased signal on DWI images (Szabo et
al., 2005). ADC values were reduced by 11 to 37%, and
there was a close spatial correlation of diffusion weightedand perfusion imaging (PI) changes, hyperperfusion on
SPECT, and localization of EEG focus. These abnormal-
ities normalized in most patients by day 14. In many cases
however, DWI revealed abnormalities in several different
regions, and it was problematic to differentiate changes in
areas of seizure focus, and changes in the epileptic corti-
cal and subcortical networks that underlie seizure spread
(Lansberg et al., 1999; El Koussy et al., 2002). The authors
therefore concluded that it would be difficult to locate the
epileptogenic focus using DWI and PI alone.
Single seizuresThere have also been several studies of diffusion imag-
ing following single seizures (Table 1). The interpretation
of these studies is limited by a number of factors. These
include, small numbers of heterogeneous patients, varying
methods of analysis (including a priori region of interest
(ROI) and whole brain voxel-based methods), lack of con-
trol groups or follow-up scanning, and wide variability in
the duration of both seizure, and interval from seizure to
scan.
Salmenpera et al. (2006b) used DWI to study changes
in diffusivity after single seizures. In 21 patients with in-
tractable focal epilepsy, postictal decreases were found in
52% seizures, but in 17% of seizures there were increases
Table 1. Postictal diffusion studies
Authors Findings
Diehl et al., 2001 1/7 had significant ADC compared with contralateral side after a single seizure
Areas of diffusion change maximal adjacent to hippocampus (unclear if seizure onset or seizure spread zone)
Hufnagel et al., 2003 2/9 patients had significant ADC postictally compared to interictally
Changes colocalized with postulated seizure focus
Konermann et al., 2003 10 patients with TLE scanned before and after injection with flumazenil
Significant ADC in all patients postictally compared with interictally
Changes colocalized with postulated seizure focusOh et al., 2004 9/14 patients had significant ADC postictally compared to interictally
Changes colocalized with postulated seizure focus
Significant difference seen only in patients with neocortical ictal onset zones or in neocortical portion of temporal
lobeauthors hypothesize this is due to interictal chronic ADC in hippocampus of mTLE patients masking any
postictal decrease
Diehl et al., 2005 8/18 patients had significant MD postictally compared with interictally which were focal in seven patients
(including one with MD)
In 3 patients presumed epileptogenic zone colocalized with the area of MD decrease
No changes in FA seen suggesting that single short seizures cause changes in cell hydration but not the
directionality of diffusion
Salmenpera et al., 2006b 21 patients scanned after 23 seizures
Focal diffusion changes (significant or in MD) seen in 52% of seizures postictally compared with interictally
Changes colocalized with postulated seizure focus in 4 patients
in MD. The analysis used voxel-based methods to include
data from the whole brain, and the resulting spatial dis-
tribution of diffusion changes was complex, with postictal
changes in MD often being found distant to the putative
seizure focus. This implied involvement of a widespread
epileptic network, and not a single focus (Fig. 3). Theincreases in MD, which were detected together with the
decreases in postictal scans that were acquired soon af-
ter seizures, were thought to be due to vasogenic oedema.
Concordance with the presumed epileptogenic focus was
seen in only four patients, all of whom had postictal scans
within 45 min of seizure onset. Repeated postictal scans
showed a gradual return to baseline for both the increases
and decreases in MD.
In an effort to minimize the delay between seizure and
scan, Konermann et al. administered intravenous flumaze-
nil, during scanning. They consistently demonstrated sig-
nificantly reduced ADC in hippocampi and parahippocam-pal gyri, ipsilateral to the seizure onset, in a series of 10 pa-
tients with refractory TLE (Konermann et al., 2003). Fur-
ther work by the same group without the use of flumazenil,
identified diffusion changes postictally in only two out of
nine patients, in whom complex partial seizures were of du-
ration greater than 60 s, and seizure to scan time was less
than 15 min. Generalized seizures were associated with
global ADC change (Hufnagel et al., 2003).
These studies suggest that the diffusion changes visu-
alized with MRI after single seizures are more transient
than those after status epilepticus, and are complex in terms
of their distribution and evolution of change. The inher-
ent difficulties in scanning patients directly after seizures,
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Figure 3.
(Adapted with permission from
Salmenpera et all. 2006b)
Difference analysis (areas of de-creased diffusivity postictally are
compared with interictal values) of
a patient with left temporal lobe
epilepsy scanned 40 min after a
complex partial seizure. The areas
of change are overlaid in color on
the patients normalized b0 image,
and this shows decreased mean
diffusivity postictally in the bilat-
eral cingulate cortex compared to
the interictal image. Red arrows
refer to the mean diffusivity val-ues measured from the areas of
change at different time points
(II = interictal, PI = postictal).
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the evident involvement of a cerebral network and not of
a single focus, and the physical limitations of spatial res-
olution limit the sensitivity of the technique in the local-
ization of seizure foci. Technological advancements such
as, real time motion correction, open access scanners, and
fast acquisitions may overcome these limitations and re-sult in postictal diffusion MRI becoming a useful clinical
tool.
Interictal studies
Early interictal diffusion imaging studies of patients
with epilepsy concentrated on temporal lobe epilepsy
(TLE) and hippocampal Sclerosis (HS) and found in-
creased average ADC values in sclerotic hippocampi, com-
pared with the contralateral side and control subjects. This
suggested structural disorganization and an expansion of
extra cellular space, and was thought to reflect neuronal
loss, reduction of dendritic branching, and microstruc-tural changes associated with epileptogenesis (Hugg et al.,
1999; Wieshmann et al., 1999a; Kantarci et al., 2002; Yoo
et al., 2002; Assaf et al., 2003; Hakyemez et al., 2005).
Furthermore, in those patients who undergo surgery, ADC
measures may be a useful postoperative prognostic indi-
cator (Goncalves Pereira et al., 2006). Studies using high-
resolution DTI have also found abnormal anisotropy val-
ues in the hippocampus compared to healthy control sub-
jects, though to a lesser magnitude than mean diffusivity
changes (Salmenpera et al., 2006a). Abnormalities in the
diffusion parameters of hippocampi ipsilateral to seizure
onset, which are normal on conventional MRI have also
been found. This suggests that diffusion MRI may be more
sensitive in identifying abnormal cerebral tissue than stan-
dard MRI sequences (Assaf et al., 2003; Londono et al.,
2003). Wehner et al. assessed 22 patients with TLE, and
found that in the 14 patients with MRI defined hippocam-
pal sclerosis, the ADC was significantly greater in the ipsi-lateral HC compared with the contralateral side, and could
be used to lateralize the seizure focus (Wehner et al., 2007).
In the remaining patients without HS, the ADC of the hip-
pocampi were not significantly different to the contralateral
side, but were significantly less than in controls. Analysis
of the resected specimens confirmed hippocampal sclero-
sis in those MR positive patients, but revealed gliosis only
without any apparent neuron loss or hippocampal sclerosis
in the MR negative group. The authors postulated that bi-
lateral temporal lobe abnormalities in some patients with
TLE might explain why diffusivity did not provide later-
alizing information in patients with nonlesional MRI, andthis appears to be have been borne out by other studies (Lee
et al., 2004). Diffusion-based studies that have specifically
assessed normal looking tissue, beyond ipsilateral mesial
temporal lobe structures in TLE patients, have demon-
strated bilateral changes together with extratemporal ab-
normalities (Arfanakis et al., 2002; Thivard et al., 2005b;
Gross et al., 2006). This suggests that structural or func-
tional abnormalities (metabolic changes, subtle structural
lesions) may extend beyond the seizure onset zone in uni-
lateral mesial TLE associated with HS.
Diffusion imaging is also sensitive to patients with
epilepsy and nonprogressive acquired lesions such as
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Figure 4.
(Adapted with permission from Dumas et al., 2005)
(AC) Frontal lobe dysplasia in a 31-year-old patient. (A) FLAIR sequences showing subtle hyperintensity of the
left frontal lobe (arrow). (B) Fractional anisotropy (FA) map. Area of decreased FA of the left frontal lobe, more
extensive than the area of FLAIR signal abnormality. (C) Superposition of FA (using a color scale) and FLAIR images.
Epilepsia C ILAE
cerebral ischaemic lesions and perinatal hypoxia (Wiesh-
mann et al., 1999b, 1999c, Rugg-Gunn et al., 2001). Ar-
eas of increased MD and decreased FA correlate with
abnormalities identified on visual inspection of conven-
tional MR imaging, and are concordant with neuronal loss,
gliosis, and structural disorganization. Moreover, diffusion
imaging can often pick up areas of pathology beyond the
conventional margins of acquired lesions seen on stan-
dard MRI, again suggesting additional sensitivity from DTI
(Rugg-Gunn et al., 2001).
Patients with epilepsy and malformations of cortical de-velopment (MCD) have also been studied with diffusion-
based MRI (Wieshmann et al., 1999b). Eriksson et al. used
a voxel-based method to assess the whole brains of 22 pa-
tients with several types of MCD (Eriksson et al., 2001).
Fifteen and eight patients had reduced anisotropy and in-
creased diffusivity within the MCD respectively, which
suggests a loss of directional organization and relatively
preserved cell density. Moreover, diffusion abnormalities
were also found beyond the margins of the evident MCD
in areas that appeared normal on conventional MRI. Con-
sistent with these findings, Dumas et al. used a ROI-based
method to assess both areas of MR visible abnormality, and
normal appearing cerebral tissue in 15 patients (Dumas etal., 2005). They identified significantly reduced anisotropy
in normal appearing white matter adjacent to, and 23
cm distant from several types of cerebral lesion, includ-
ing MCDs (Fig. 4). Histological examination of resected
normal looking tissue revealed the presence of occult ab-
normalities such as gliosis, infiltrative tumor cells, and ax-
onal loss. Together these findings suggest that diffusion
imaging can often pick up areas of pathological abnormal-
ity beyond the conventional margins seen on standard MR
images, which has implications for the surgical resection
margins of these areas.
Interictal DTI is also able to identify focal abnormali-
ties in patients with focal epilepsy, and unremarkable con-
ventional MRI (Fig. 5). In one of the earliest studies, in-
creased diffusivity was found in eight patients and reduced
anisotropy was found in two patients out of a total of 30
patients with refractory focal epilepsy, and unremarkable
conventional MRI (Rugg-Gunn et al., 2001). In seven, the
areas of abnormal diffusion corresponded with the local-
ization of EEG focus. A group analysis of the nine patients
with electroclinical seizure onset localizing to the left tem-
poral region revealed a significant increase in diffusivity,and reduction in anisotropy within the white matter of the
left temporal lobe. The areas of abnormal diffusion were
postulated to be caused by disruption in the microstruc-
tural environment due to etiological factors such as occult
dysgenesis, or acquired damage, or as a result of repeated
seizures leading to neuron loss, gliosis, and expansion of
the extra cellular space. This study suggested that diffu-
sivity is a more sensitive diffusion index than anisotropy
for identifying occult abnormalities in patients with nor-
mal, conventional MRI. This may represent expansion of
the extra cellular space but retention of the overall struc-
tural organization of the white matter tracts. A patient from
this study, with cryptogenic frontal lobe epilepsy, had fo-cally increased MD in the right frontal lobe. Subsequent in-
tracranial EEG concluded that this was the area of seizure
onset, and led to a resection. Histopathologic examination
of the resected specimen showed marked white matter glio-
sis, associated with structural disorganization, and expan-
sion of the extra cellular space (Rugg-Gunn et al., 2002).
Six years following surgery, seizures have been reduced by
more than 50% the preoperative rate.
Subsequent studies have corroborated these findings,
and investigated the correlation between DTI mea-
surements and stereo-electroencephalographic (SEEG)
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Figure 5.
(Adapted with permission from Thivard et al., 2006)
View of a 3D representation of the brain of a patient with occipital lobe epilepsy and reported normal conven-
tional MRI. Diffusion imaging revealed a region of increased ADC (red) in the left temporo-occipital junction. This
corresponded to the onset zone (blue) and irritative zone (green) as delineated by intracranial EEG.
Epilepsia C ILAE
recordings in patients with cryptogenic focal epilepsy
(Thivard et al., 2006; Guye et al., 2007). These studies havefound good spatial concordance between epileptiform ac-
tivity on EEG and diffusion abnormalities in nearly 50%
(6/13 and 4/9, respectively) patients. They also found that
diffusivity, rather than anisotropy measures, correlated bet-
ter with electroclinical data. Furthermore, in those patients
who have undergone surgery for their epilepsy, this has of-
ten translated into a good postoperative outcome, suggest-
ing that DTI can provide additional information over con-
ventional MRI in the identification of occult abnormalities.
Despite the encouraging nature of these results, it is
important to note that in several of the aforementioned
studies, details of the conventional MRI sequences used
were not available. Tertiary referral centers can increasetheir diagnostic yield in patients with refractory epilepsy,
with the use of epilepsy-specific, high-resolution volumet-
ric imaging (Von Oertzen et al., 2002). In those cases that
remain MR negative after such imaging, interictal diffu-
sion imaging has a role to play. The derivation of quanti-
tative ADC/MD/FA maps and their analysis either by ROI
or VBM methods provides a useful tool in the localiza-
tion of subtle structural abnormalities, as part of a multi-
modality evaluation that should include interictal and ictal
EEG recordings, neuro psychiatric and psychological eval-
uations and other imaging modalities such as PET, SPECT,
or magnetoencephalography (MEG).
TRACTOGRAPHY AND EPILEPSY
Knowledge of the anatomy of white matter connections
is crucial to the understanding of normal and abnormal
brain function (Ffytche & Catani, 2005). With conventional
MRI variations in white matter signal are subtle, and white
matter tracts cannot be accurately parcellated. In most stud-
ies, DTI quantitative measures have been assessed using
either region of interest or voxel-based analysis. The for-
mer has limitations in that it is user dependent, and has a
possibility of error that other fiber tracts, gray matter and
CSF or other white matter structures may be included. The
latter, though observer independent, has problems associ-
ated with the need for spatial normalization and smoothingdue to anatomical variations in ventricular size, gyral pat-
terns, etc. Both methods have limited ability to quantify
specific white matter pathways along their entire trajecto-
ries. Tractography is an extension of DTI, whereby the di-
rectional information obtained in each voxel is used to gen-
erate virtual, three-dimensional white matter maps. These
maps are based on similarities between the diffusion prop-
erties of neighboring voxels in terms of shape (quantita-
tive diffusion anisotropy measures) and orientation (princi-
pal eigenvector map), and several mathematical algorithms
have been devised to generate white matter tracts (Mori &
van Zijl, 2002).Epilepsia, 49(2):189200, 2008
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Tractography does not therefore trace fibers in the sense
that injected tracers do; rather it demonstrates the path of
least resistance to water diffusion. The size of typical imag-
ing voxels is a 23 mm3 so a single voxel could contain
thousands of axons. In addition most methods assume that
fibers at each voxel are well described by a single orienta-tion estimate. This can lead to tracking difficulties in areas
of fiber kissing or crossing. As methodological develop-
ments occur in orientational (Tuch et al., 2002) and spatial
resolution (Nunes et al., 2005), and in diffusion model-
ing (Tournier et al., 2004; Tuch, 2004; Alexander, 2005;
Perrin et al., 2005) and tractography algorithms (Parker &
Alexander, 2005), these limitations should prove less of a
problem.
Despite these limitations tractography is the only tech-
nique available for tracing the white matter pathways in the
living brain. By isolating specific pathways from adjacent
gray and white matter and CSF, tract-specific qualitativeand quantitative information such as volume, anisotropy,
and connectivity indices can also be derived (Ciccarelli
et al., 2003a). Tracts can also be normalized and combined
to generate group maps that indicate how reproducible a
given tract or connection is across a group of subjects (Ci-
ccarelli et al., 2003b). This information can be used to lo-
cate and assess the pathophysiological effects of chronic
epilepsy on the white matter anatomy, including the struc-
tural reorganization of higher cortical functions such as
language and memory. The technique can also be used
to investigate white matter anatomy (Catani et al., 2002),
which can aid preoperative planning, and prevent damage
to eloquent cortical functions, particularly when combined
with functional activation studies (Guye et al., 2003).
Reorganization of language and memory networks
Refractory TLE due to HS has a good outcome follow-
ing anterior temporal lobe resection (ATLR). TLE may be
associated with disrupted lateralization of language and
material specific memory, and these functions may be fur-
ther impaired by ATLR. Significant, selective language
deficits have been reported in up to 40% of patients fol-
lowing dominant ATLR (Davies et al., 1998). Patients un-
dergoing unilateral ATLR for refractory TLE also typically
show a decline in verbal memory following surgery involv-ing the language-dominant hemisphere (Ivnik et al., 1987)
and deficits in topographical memory following nondom-
inant temporal lobe resection (Spiers et al., 2001). Func-
tional MRI studies have demonstrated the reorganization
of both memory (Powell et al., 2007b) and language func-
tions in TLE patients (Adcock et al., 2003; Thivard et
al., 2005a). DTI tractography has the potential to demon-
strate the structural reorganization of networks involved in
memory and language, which mirror changes in cerebral
function.
Powell et al. (Powell et al., 2007a) combined fMRI
and tractography in patients with unilateral TLE, and
in controls. Verb generation and reading comprehension
paradigms were used to define functional regions that were
used to generate starting regions for tractography. Trac-
tography was carried out using diffusion images acquired
with a high angular resolution technique, and a proba-
bilistic algorithm. This technique is thought to cope betterwith crossing or kissing fibers (Parker & Alexander, 2003).
Controls and right TLE patients had a left-lateralized pat-
tern of both language-related activations, and associated
white matter organization. Left TLE patients showed more
symmetrical language activations, along with reduced left
hemisphere and increased right hemisphere white matter
pathways, in comparison with both controls and right TLE
patients (see Fig. 6). Correlations between measures of
structure and function in both groups were found, with
subjects with more lateralized functional activation having
more lateralized white matter pathways.
Other tractography studies have assessed memory-related structures within the limbic system. Concha et
al. found that patients with unilateral TLE have bilateral
changes in the fornix and cingulum bundle, characterized
by impaired tracking of these pathways, and increased
mean diffusivity and reduced FA along them. This was
thought to be consistent with the degeneration of path-
ways connecting to the hippocampus (Concha et al., 2005).
Other studies have assessed the progression of Wallerian
degeneration in the limbic structures in patients with re-
fractory epilepsy who have undergone surgical procedures
such as corpus callostomy (Concha et al., 2006) and tem-
poral lobe resections (Concha et al., 2007). Together, these
results suggest that the use of tractography-derived quanti-
tative measures may have a significant role to play in the
longitudinal evaluation of the effects of epilepsy on the
brain, and on cognitive functions such as memory and lan-
guage, particularly when correlated with neuropsychologi-
cal measures (Lui et al., 2005).
Visual pathways and preoperative planning
ATLR can also cause visual field defects (VFD) in up
to 10% of patients. Indeed, in 5% it can be severe enough
to render the patient ineligible for a driving license, de-
spite being seizure-free (Manji & Plant, 2000). Typically,
VFDs after ATLR occur in the superior homonymous fieldcontralateral to the resection and are due to disruption of
fibers of Meyers loop. The anterior extent of the Meyer
loop is not visualized on conventional imaging and varies
from person to person (Ebeling & Reulen, 1988). As a con-
sequence the occurrence and extent of a postoperative VFD
cannot be accurately predicted by conventional MRI, or
from the extent of resection performed. Tractography has
been used to demonstrate the optic radiation in normal sub-
jects (Yamamoto et al., 2005), and has been applied to pre-
and postoperative surgical patients with AV malformations
and tumors in and around the visual pathways. Kikuta et
al. (Kikuta et al., 2006) carried out pre- and postoperativeEpilepsia, 49(2):189200, 2008doi: 10.1111/j.1528-1167.2007.01378.x
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Figure 6.
(Adapted with permission from Powell et al., 2007a)
Group variability maps of the connecting paths tracked
from left and right functionally defined frontal ROIs for
each of the three groups controls, left TLE and right
TLE patients. Each image shows the maximum inten-
sity of the commonality maps in each plane of view
as a brain surface rendering. The color scale indicates
the degree of overlap among subjects (expressed as
commonality value); for example, a value of 1 (pure
red) represents 100% subject overlap (i.e., every sub-
jects identified tract contains the voxel in question).
Controls and right TLE patients show a similar pattern
of connections with greater SLF connections to the
temporal lobe on the left (arrowed) than the right. In
the left TLE group the opposite pattern is seen with
greater temporal lobe connections on the right.Epilepsia C ILAE
tractography in 10 such patients, and were able to predict
the magnitude of pre- and postoperative visual field loss
from the geometrical relationship between the optic radi-
ation and AV malformation. A recent study demonstrated
application to temporal lobe surgery for epilepsy (Fig. 7).
The optic radiation was visualized before and after ATLR,
and disruption of Meyers loop was demonstrated in a pa-
tient who developed a quadrantanopia (Powell et al., 2005).
In a similar vein, other studies have demonstrated the util-
Figure 7.
(Adapted with permission from Powell et al., 2005)
Tractography of the optic radiation in two patients
who underwent anterior temporal lobe resections,
superimposed on each subjects sagittal non diffusion
weighted (b = 0) MR image. Preoperative images on
the left and postoperative images on the right. Patient
A suffered a quadrantic field deficit postoperatively due
to surgical interruption of the optic radiation (arrow).
The visual fields of patient B remained intact.
Epilepsia C ILAE
ity of tractography in the resection of neoplasms that are in
close proximity to eloquent subcortical white matter tracts
(Yu et al., 2005). There are, however, technical challenges
to be overcome to enable the coregistration of preopera-
tive tractography with the T1-weighted MR images used
to guide neurosurgical interventions. When these are sur-
mounted, preoperative tractography of the optic radiation
and other vital white matter connections, will be able to
be displayed when planning and undertaking surgical pro-
cedures (Kamada et al., 2005). Further, the advent of per-
operative MRI will allow the correction of the movement
of tracts caused by craniotomy, and will improve the ac-
curacy of the data, to aid surgical planning and result in a
lower risk of postoperative deficits.
CONCLUSION
The advent of diffusion-based MRI and tractography
heralds an exciting period in the neuroimaging of epilepsy
patients. The interpretation of peri- and postictal diffusion
changes remains complex, but has the potential to improve
understanding of seizure physiology. Interictal diffusion
MRI studies have some localizing value in patients with fo-
cal epilepsy, but normal conventional MRI scans. The use
of quantitative maps derived from diffusion imaging, es-
pecially within the context of a multimodality assessment,
is a powerful tool to search for subtle lesions. Furthermore
this technique may also have advantages for delineating theEpilepsia, 49(2):189200, 2008
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M. Yogarajah and J. S. Duncan
extent of a structural abnormality, and have a particularly
important role in the planning of intracranial EEG and tis-
sue resection.
The place of tractography in the imaging armory avail-
able to epileptologists remains to be determined. Its find-
ings need to be interpreted with a degree of caution due tothe limitations described above. Despite this, it has already
demonstrated its potential in increasing our understand-
ing of the structural and functional plasticity that occurs
in chronic TLE. Further studies are needed to evaluate the
role of tractography in presurgical planning, particularly
studies incorporating postoperative findings. We anticipate
that as data acquisition and tracking algorithms improve,
and tractography data are combined with EEG and fMRI
data, these improvements will be forthcoming. Ultimately,
it may be possible to visualize white matter organization
with tractography, such that potentially novel approaches
to functionally disconnect the seizure focus from the sur-rounding brain can be developed.
ACKNOWLEDGEMENTSWe are grateful to the Welcome Trust for supporting our work (Pro-
gramme Grant No 067176) and The Big lottery Fund, Wolfson Trust, andthe National Society for Epilepsy for supporting The NSE MRI scanner.
Conflict of interest: We confirm that we have read the Journals positionon issues involved in ethical publication and affirm that this report is con-sistent with those guidelines.
M. Yogarajah nilJ. Duncan nil
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