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Dyslexia Regional differences in brain electrical activity by topographic mapping.

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ORIGINAL ARTICLES
Dyslexia: Regional
Dfierences in Brain Electrical Activity
by Topographc Mapping
Frank H. Duffy, MD, Martha B. Denckla, M D , Peter H. Bartels, PhD, and Giulio Sandini, P h D
Electroencephalographic (EEG) and evoked potential data were recorded during behavioral testing from 8 dyslexic
and 10 normal boys aged 9 to 11 years. Topographic mapping of their brain electrical activity revealed four discrete
regions of difference between the two groups involving both hemispheres, left more than right. Aberrant dyslexic
physiology was not restricted to a single locus but was found in much of the cortical region ordinarily involved in
reading and speech. Prominent group differences were observed in the bifrontal area in addition to the more
expected left temporal and left posterior quadrant regions. Although activation tests produced more prominent
group difference, dyslexics differed from normal subjects at rest as well. EEG alpha activity was increased for the
dyslexics, suggesting relative cortical inactivity in that group.
Duffy FH, Denckla MB, Bartels PH, Sandini G: Dyslexia: regional differences in brain electrical activity
by topographic mapping. Ann Neurol 7:412-420, 1980
Community surveys have shown that dyslexia affects
3.5 to 6% of school-aged children [23]. Sixty percent
of all children referred to the Learning Disabilities
Clinic at Children’s Hospital Medical Center, Boston, have a measurable degree of reading disability.
Despite this high frequency, not everyone agrees on
the exact boundaries for the definition of dyslexia o r
on its pathophysiological origins. What is agreed is
that “developmental dyslexia” is not due to educational or environmental deprivation, primary
psychiatric disorder, or visual or auditory sensory
handicap.
The occurrence of dyslexia as either an isolated
symptom o r a symptom complex including other evidence of minimal brain dysfunction seems partially
responsible for difficulties in elucidating the underlying pathophysiological mechanism. W e shall
adopt the distinction between “dyslexia-pure” and
“dyslexia-plus” proposed by Hughes and Denckla
[ 131 and limit our considerations to dyslexia-pure;
“plus” refers to the common accompanying symptoms of hyperactivity, dyscalculia, and motor incoordination.
Theories on the physiological cause of dyslexia
have generally lacked neuropathological confirmation. Accordingly, many authors have employed
clinical neurophysiological studies to analyze the
problem [4, 12, 14, 15, 25-27]. Regrettably, the
electroencephalographic (EEG) and evoked potential
(EP) abnormalities in children with dyslexia are too
nonspecific to form useful diagnostic constellations.
With the exception of Hanley and Sklar [12], few
have looked beyond the visual (occipital) or classic
speech (temporoparietal) regions for abnormalities.
Two areas in which electrophysiological data may
prove to be of some importance in dyslexia are: (1)
characterization and localization of the brain system
or component distinctively different in dyslexia, and
(2) establishment of a less culturally variable criterion
for objective diagnosis. In this paper we report evidence suggesting that physiological aberrations in the
brains of dyslexics are more widespread than previously suspected. This evidence is based upon analysis
of topographic maps of EEG and EP activity formed
by brain electrical activity mapping (BEAM) methodology [S].
From the Seizure Unit and Division of Neurophysiology and the
Learning Disabilities Clinic, Department of Neurology, Children’s
Hospital Medical Center and Harvard Medical School, Boston,
MA, and the Departments of Microbiology and Optical Science,
University of Arizona, Tucson, AZ.
Received June 25, 1979, and in revised form Sept 4. Accepted for
publication Sept 9, 1979.
412
Materials a n d Methods
Eight children fulfilling the criteria for “dyslexia-pure”[ 131
were selected from among patients receiving a multidisciplinary workup for “readingdifficulties”in the Learning Disabilities Clinic of Children’s Hospital Medical Center,
Boston. None of these dyslexics had abnormalities on a
traditional neurological examination (by a neurologist);
requests
iddress
tO Dr Duffy, Seizure Unit,
Boston, MA
Hospital Medical Center, 300 Lonwood
02115.
0364-5134/80/050412-09$01.25 @ 1979 by Frank H. Duffy
none demonstrated psychopathology by history or interview (with a psychiatrist). All had oral reading scores at
least 1.5 years below expectation as defined by Rutter [23],
and none had a history of hyperactivity o r received a score
of 16 or above on the Connors rating scales tor parents and
teachers [ S ] . To reduce variability, we chose to examine an
all-male group 9.0 and 10.7 years of age with full-scale I Q
scores ranging from 94 to 114. Two of the dyslexics were
left-handed, two ambidextrous, and four right-handed.
Ten controls were recruited from a population of successful fifth grade suburban Boston students. This all-male
group ranged in age from 9.0 to 10.5 years and came from a
similar socioeconomic class to that of the dyslexics. All
controls were administered the Raven Coloured Progressive Matrices test [22] and the Gray Oral Reading Test
[lo]. To be included in the control group, each subject had
to be above the 50th percentile on the former test and at
fifth grade reading level on the latter. Two controls were
left-handed, one ambidextrous, and seven right-handed.
EEG Tests
Spontaneous EEG was recorded during ten different testing conditions or states. These were designed to permit recording during simple resting brain activity (with eyes open
or closed) and during tests designed to activate the left
hemisphere (speech and reading), the right hemisphere
(music and geometric figures), and both hemispheres together (paired visual-verbal associations). The ten EEG test
states were:
1. Speech (S): to listen carefully to a tape-recorded fairy
tale (“The Elephant and the Butterfly,” e. e. cummings) and answer simple questions about its content
when completed.
2. Music (M): Similarly, to listen to music (“Nutcracker
Suite,” Tchaikovsky).
3. Kimura figures-instruction (KF-I): to remember a set
of six abstract figures on index cards presented by an
examiner [16].
4. Kimura figures-test (KF-T): to select the six previously presented figures from a set of 38 figures, verbally indicating yes or no.
5. Paired associates-instruction (PA-I): to associate each
of four abstract figures on index cards with a particular
artificial name (e.g., “Mog”) spoken by the examiner
(i.e., the sound-symbol-association test [28]).
6. Paired associates-test (PA-T): to name each of the
same four abstract figures when tested by the examiner.
(RT-I): to read silently
7. Reading task-instruction
three previously unread paragraphs [lo] so as to answer questions subsequently.
(RT-T): to identify whether 34
8 . Reading task-test
typed sentences presented by the examiner were previously included in the three paragraphs (verbal yes o r
no response).
9. Eyes open (EO): to relax but remain still with the eyes
open.
10. Eyes closed (EC): to relax but remain still with the eyes
closed.
Approximately three minutes of EEG data were recorded
for each of the ten states in a clinical EEG laboratory.
Evoked Potential Tests
Brain activity and suitable trial markers were tape-recorded
for subsequent off-line formation of average EPs in three
test states. Two (visual and auditory EP) were administered
with no instructions other than to remain alert. O n e
(“tight-tyke” auditory EP) required a difficult phonological
discrimination. These three EP test states were:
1. Visual evoked potential (VEP): over 500 flashes from a
Grass PS-2 strobe stimulator were presented at random
interstimulus intervals always exceeding 1 second; the
unit was set at intensity 8 and placed 20 cm from the
subject’s closed eyes.
2. Auditory evoked potential (AEP): over 500 clicks were
similarly presented via earphones at 92 db sound pressure level.
3. “Tight-tyke’’ auditory evoked potential (TTAEP): over
250 presentations of the tape-recorded word tight were
randomly presented, intermixed with a similar number
of the word tyke; subjects were required to count the
number of tights heard for half the presentation and
tykes for the remainder of the presentation.
Data Processing
For all states, data were recorded from 20 standard EEG
electrodes in the normal 10-20 format. Signals were taperecorded and processed into spectra o r EPs on a PDP-12
computer (Digital Equipment Corp) using the appropriate
programs of the SIGSYS- 12 biomedical software package
(Agrippa Data Systems). A single spectrum (0 to 32 Hz) o r
EP (512 msec) was formed for each electrode and state.
Segments of raw data containing eye movement, muscle
artifact, o r mains interference were eliminated from the
analysis. Next, the set of 20 spectra or EPs representing
one experimental state were processed into topographic
maps of electrical field distribution using the BEAM technology under SIGSYS-12 control. T h e details of this processing have been described previously [8]. Topographic
images of spectral theta (4 to 7.75 Ht) and alpha (8 to
11.75 Hz) activity were retained as images on a display
screen for visual inspection and as 64 x 64 numerical matrices in computer memory for subsequent analysis. A series of 128 images, each representing 4 msec of EP activity,
was similarly retained for display and analysis of the EP
data.
Mean image matrices for each state were formed separately for the control and dyslexic groups with the aim of
locating regions of the image matrix where the normal and
dyslexic groups differed. This was done by comparing each
point of the 64 x 64 image matrix using the standard twosample t statistic [24]. Each t with N degrees of freedom
was then transformed into a percentile index (PI) by the
formula PI = 200 [ 1 - F( t ,n)], where F(t,n) is the cumulative distribution function for the Student t distribution.
The result was a matrix of PI values which was then converted into topographic images in pseudocolor format (e.g.,
Fig 1). Each color represents a particular PI value. Since the
PI is related inversely to a measure of between-group difference (t statistic), a PI of 2 indicates a greater difference
than a PI of 5. W e shall use the phrase “PI at least 2” to
refer to between-group differences at least as great as those
I I
Duffy et al: Brain Electrical Activity Differences in Dyslexia
413
that have a PI of 2. Thus, a PI at least 2 indicates a set of
more extreme differences than a PI of at least 5.
Note that the PI maps are not used to measure the overall
statistical significance of group separation between control
and dyslexic subjects. Rather, they are utilized to permit
graphic localization of regions of maximal between-group
difference, using the t statistic as a measure of separation.
The issue of overall group separation in multivariate space
is addressed in a separate report [8al.
Results
E~ectroenrephalographirFindings
ACTIVITY. Topographic maps of 8 to 11.75
Hz alpha demonstrated, for all subjects, peaks of activity in the occipital, midline vertex, or midcentral
regions such as one might expect from analysis of
classic EEG data. When present, the midcentral
peaks corresponded to mu rhythm on the standard
EEG tracing. The topographic distribution of alpha
activity was usually state dependent. By visual inspection, controls generally showed a great variation
in alpha distribution as a function of state. Dyslexics
usually showed alpha distributions that were less
state dependent and tended to have invariant maxima
in the midline or over the left hemisphere. However,
subject-to-subject variability prevented group or
state identification by visual inspection of individual
maps.
Figure 1 shows state-by-state comparisons between
control and dyslexic subjects using PI maps for alpha.
The degree of between-group difference is indicated
as follows for each state; the location of the difference is shown by L for left hemisphere, R for right
hemisphere, and B for both hemispheres. Numbers
represent PI values.
ALPHA
a-M
5L
...
...
a-KF-T
5L
2L
State: a-PA-T a-RT-I a-RT-T a-EO
PI:
1B
State: 8-S
8-M
8-KF-I
8-KF-T
8-PA-I
...
...
2L
...
...
8-RT-I
0-RT-T
19-EO
0-EC
2L, 5B
...
5L
5R
PI:
State: 8-PA-T
PI:
...
Between-group difference in the left anterolateral
frontal region is prominent for the KF-I state and
minimal for EO. The RT-I state shows marked differences in the left midtemporal region and left medial frontal region as well as a smaller right anterolatera1 frontal difference. A small right posterior
parietal difference is seen in EC. N o left parietal
differences were observed for theta activity. Note
that many fewer differences were detected for theta
than for alpha activity but that the most prominent
delineation of the left anterolateral frontal region was
seen for theta (KF-I). Regions of between-group
difference were associated with higher mean theta
values for the dyslexic group except for the KF-I
state. in which the reverse was true.
Evoked Potentials
State: a-S
PI:
Topographic maps of 4 to 7.75
Hz theta demonstrated peaks of activity almost always maximal along the midline vertex for both control and dyslexic subjects. The topographic distribution of theta activity was not prominently altered by
state change. It was impossible to judge group or
state by visual inspection of theta maps.
Figure 2 shows comparisons by state between
controls and dyslexics using PI maps for theta. The
degree and location of between-group difference for
each state is indicated as it was for alpha activity:
THETA ACTIVITY.
2B
...
5L
a-EC
2L, 5B
In Figure 1, note the prominent between-group difference in the medial frontal region, which is seen
only on the left for the S, PA-I, and EO states but
bilaterally for the PA-T and RT-I states. Note also
the between-group differences in the left midtemporal region (S, EO, EC) and left anterolateral frontal
region (KF-T). Only the EC state shows left parietal
and left posterior central frontal differences. Although differences are more frequent over the left
hemisphere, the greatest between-group difference
(PA-T) is seen bilaterally (medial frontal). Regions of
group difference were always associated with higher
mean alpha activity for the dyslexic group.
414 Annals of Neurology Vol 7 No 5 May 1980
Topographic maps of between-group differences for
the three EP states (VEP, AEP, and TTAEP) are
F i g 1. Maps of state-depevident regional differences between
normal and dyslexic subjects for E E G alpha actiz'ity. Earh
map represents the between-groupdifference of normal and
dyslexic boys f o r ten different states and within the EEG alpha
frequency band (8 t o 12 Hzi. Each map is a pseudocolor plot of
the percentile index (PI) based upon the standard two-sample t
statistic. Next t o each map is a color scale iri which light green
represents a PI of I : blue a PI of 2 , pink a PI of 5 , dark green
a PI of 10, and red-brown a PI of 20: uncolored regions represent a PI greater thari 20. The PI is inimersely related to
between-group difference; thus, light green shows the maximal
between-group difference and red-brown the least.
These maps permit localization of between-group difference.
Note that the greatest differences are predominantly anterior to
the interaural line and are maximal ivi the a-PA-T and
a-RT-I states (the states are defined in the text). Note also that
despite the left-sided bias, differences are seen oziey both hemispheres, especially in the frontal lobe.
Uuffy et al: Brain Elcctri
ences in Dyslexia
415
416 Annals of Neurology Vol 7 No 5
May 1980
speech regions centered about Wernicke’s area and
extending into the adjacent regions of the left
parietal and temporal lobes. Most neurophysiological
studies of dyslexics have been limited to these regions. In agreement with other reports [4, 12, 14, 15,
25-27], our study demonstrates differences between
the left posterior quadrant in boys with dyslexia-pure
[13] and controls (see Fig 4 ) . However, additional
shown in Figure 3. Each map represents the between-group difference over a 12-msec epoch centered about the indicated time.
In the following table the degree of between-group
difference is indicated for each EP condition at the
indicated 12-msec epoch from time of stimulus (latency). The relative polarity of the mean normal (N)
and dyslexic (D) EPs is also shown.
Time (msec)
EP
Condition
78
114
126
150
162
174
186
198
282
VEP
...
...
...
...
...
...
...
...
5 ND+
AEP
...
2 N-
...
...
...
...
...
2N+
...
5 ND+
5N+
IN+
2N+
D+
lN+
D-
lN+
D-
...
...
...
D+
TTAEP
2 ND+
...
D-
D+
For the TTAEP at 150 and 162 msec, the dyslexic
and normal EPs were both positive but the dyslexic
EPs were much more so. In Figure 3 , because all AEP
maps show between-group differences over a very
similar region (left posterior temporoparietal), only
the largest (198 msec) is shown. Similarly, although
six TTAEP maps showed regions with a PI of at least
5, only four representative maps are illustrated.
Summary Maps
Figure 4 presents two maps that summarize Figures
1, 2, and 3 and show substantial regions of betweengroup difference as indicated by occurrence of the
indicated PI at least once during all EEG or EP states
or both. The map of differences with PI of at least 2
delineates four regions: (1) bilateral medial frontal
(supplementary motor area)-EEG;
(2) left anterolateral frontal (Broca’s area)-EEG; ( 3 ) left midtemporal (auditory associative area)-EEG; and (4)
left posterolateral quadrant (Wernicke’s area, parietal
associative areas, and visual associative areas-EP.
The map of differences with PI of at least 5 delineates
the same four regions, but the area enlarges. In addition, the left (EEG) and right (EP) midfrontal regions
and right Broca’s area (EEG) become involved.
Discussion
Concepts of dyslexia based upon analogues to traditional aphasiology implicate the classic posterior
F i g 2. Maps of state-dependent regional differences between
normal and dyslexic subjects for EEG theta activity. All display, scaling, and state factors are the same as in Figure 1 except for the EEG theta frequency band (4 to 8 Hz). Note that
jiwer regions reach high PI levels for theta than for alpha activity. Note, however, the dgference in the left anterior region
for the 8-KF-1 state, which is seen only for theta.
342
...
areas of between-group difference are also found
over both hemispheres, especially over the frontal
lobes. The subjects summary maps in Figure 4 demarcate four distinct regions of difference between
dyslexic and normal subjects, including the medial
frontal lobe (supplementary motor area), the left lateral frontal lobe, the left midtemporal lobe, and the
left posterior quadrant (including Wernicke’s area,
the left posterior lobe, and the left posterior parietal
lobe).
In recent publications Lassen and his colleagues
[17, 181, using cerebral blood flow studies with
xenon labeling, have demonstrated a pattern of cortical activation during speech, oral reading, and silent
reading in normal subjects that appears similar to the
regions demarcated in Figure 4. These in turn correspond to brain regions which, when stimulated [20],
interfere with a patient’s speech. So the regions that
we have shown to differ electrophysiologically between the brains of dyslexic and normal boys appear
to be among the regions normally involved in speech
and reading. Thus, dyslexia-pure may represent dysfunction within a complex and widely distributed
brain system, not a discrete brain lesion.
Regions of between-group differences demarcated
by analysis of alpha activity (Fig 1) were always associated with greater mean alpha in the dyslexic group.
Many investigators interpret relative increases in
alpha to represent relative inactivity or “idling” of
underlying cortex [9]; conversely, decreases in alpha
activity are taken to represent cortical activation [6].
Thus, the increased dyslexic alpha anteriorly may
signify relative underactivation of frontal systems in
dyslexic as compared to control boys.
Test conditions were chosen to permit examination of brain electrical activity during neutral states o r
during relative activation of the left and right hemi-
Duffy et al: Brain Electrical Activity Differences in Dyslexia
417
F i g 3 . Maps o f regional differelires between tiorrizul mid ~+slexic subjects for e1,okt.dpotential stutes. Displaj apid sculiwg
conasentions art. the J a m as for Figure 1 : the stutes ure explaitied iiz the tmt. Numbers represent the tivie from .rtitiiufus
onset t o the center of the indicated 12-tti~eeepoch. Note that
maximal dryfererms ure predominantly posierior to the iiiteranral line. Also ttote the left-sided predorttllinance but occur.
retzce of beiweeri-group dif;fretices w e r both hemiiphere.i.
PI s 2
418
Annals of Neurology
Vol 7
PI < 5
No 5
May 1980
spheres. In general, the highly activated states requiring sound-symbol association (EEG a-PA-I,
a-PA-T) and a phonetic discrimination (TTAEP)
produced the greatest differences between groups.
Nonetheless, sizeable regions of group difference
were demarcated during simpler conditions, e.g.,
alpha EO and EC, AER. Thus, demonstration of differences between the brains of normal and dyslexic
boys does not necessarily require special o r complex
test conditions.
In contrast to Hanley and Sklar’s [12] finding that
“the most recurring difference between dyslexic and
normal children is . . . 3-7 H t theta,” in our study the
largest regions delineated by EEG were in the alpha
spectral band. This may well be attributed to the fact
that those authors did not utilize midline electrodes
(FZ, CZ) and could not have delineated the large
medial frontal region which was found by our analysis
(Fig 1)of the alpha band. O n the other hand, had we
not also evaluated the theta band, we would not have
delineated the differences overlying Broca’s area (see
Fig 2). This emphasizes the importance of not limiting oneself, on the basis of an a priori hypothesis, to a
single spectral band o r to a limited set of electrodes
when attempting to correlate brain electrical activity
with underlying brain function.
Involvement of the supplementary motor area of
the frontal lobe in linguistic tasks has been suggested
by many observers. Focal seizures emanating from lesions in this region have been reported to interfere
with speech [I 1, 121 o r produce palilalia [I]. Penfield
and Roberts [20] have reported both speech arrest
and vocalization from stimulation of this region.
Most recently, Masdeu et a1 [I91 reported aphasia
following infarction of the left supplemmtary motor
region. Following a two- to three-week recovery period, the patient’s residua consisted of a mild anomia
with “marked impairment to both spontaneous writing and writing to dictation which persisted to . . .
death.” This was accompanied by “a tendency to give
up in language tasks, particularly writing.” Since iso~
~~
Fig 4. Summary maps of between-group differences of normal
and dyslexic subjects. Colored areas represent regions of
between-group differences reaching a PI of at least 2 (lej9 map)
or 5 (right map) at least once during all EEG and EP states.
Solid red represents the contribution from the ten EEG states
(alpha plus theta); the dashed red represents the contribution
from the three EP states. The blue region represents overlapping
contributions from both EEG and EP states. Note fourprominent between-group regions of difference at PI = 2: bilateral
frontal, left anterolateral frontal, left midtemporal, and left
posterolateral quadrant. I t is suggested that dyslexia represents
dysjiunction of much of the cortex normally znvolved in speech
and reading (see text). Note the bilaterality of the betweengroup difference. Note also that differences shown by E E G lie
anterior t o the interaural line, wnereaJ EP dzffwences lie posterior to that line.
Duffy et
lated vascular accidents are less common in the anterior cerebral than the middle cerebral territory, it
may be that this region, prominently demarcated in
our PI maps, plays a previously underemphasized
role in aphasia and in concepts of dyslexia and dysgraphia. The known clinical overlap and statistical association of dyslexia with the “hyperactive syndrome” [3] and “attentional deficits” [71 might be
explained on the basis of some yet unspecified frontal
lobe dysfunction.
Figure 4 illustrates that the EEG states demonstrated between-group differences largely anterior to
the interaural line. In contrast, the EP states showed
differences largely posterior to that line. The reasons
for this finding are not immediately evident. Perhaps
the between-group differences in the left posterior
region demonstrated by the AEP and TTAEP reflect
a limitation to auditory and auditory association cortex. Although demanding auditory attention, the
phonetic discrimination, TTAEP, was largely a
modality-specific task requiring little memory and no
overt cross-modal association o r motor response. In
contrast, all EEG tasks (except E O and EC) required
some form of learning, cross-modal association,
complex decoding of oral or written material, and
some sort of response. Indeed, the test designed to
activate both hemispheres (PA-T) was the most effective in showing bihemispheral between-group
difference (see Fig 1: a-PA-T). Because the regions
of group difference may vary as a function of the
testing paradigm, one cannot exclude the possibility
that more extensive regions of cortical difference
might exist between dyslexic and control subjects
under other conditions. Arguing against this possibility is the recurring similarity of the regional difference noted throughout all EEG states, even if the
trends failed to reach a PI of at least 5 for a particular
state.
There are many reports of EEG and EP abnormalities in children with specific reading disability [4,
12, 14, 25-27]. In most cases the findings have been
relativelv nonspecific and have failed to form useful
diagnostic constellations. Although our sample size
does not permit evaluation of effects due to handedness or dyslexic inhomogeneity (subtypes), the current findings of distinct regional differences between
dyslexics and normal subjects raises the possibility
that specific diagnostic rules may be developed.
We gratefully acknowledge the financial support of the Jeffrey A.
Brous Memorial Fund, Mental Retardation Core Grant HD 06276
held by Children’s Hospital Medical Center (Dr C. F. Barlow), and
National Institutes of Health Grants R1 H D 13420-01 and R1 NS
14767-01.
We thank D r C. T. Lombroso for helpful consultation, Dr Y . Matsumiya for use of his “tight-tyke” stimulus tapes, and Mr D.
MacIver and Ms C. Chapman for their flawless technical assistance.
al:
Brain Electrical Activity Differences in Dyslexia 419
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mapping, regional, differences, dyslexia, activity, electric, brain, topography
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