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Significance of Planum Temporale and Planum Parietale Morphologic Features in Neurofibromatosis Type 1
Rebecca L. Billingsley, PhD;
Gregory W. Schrimsher, PhD;
Edward F. Jackson, PhD;
John M. Slopis, MD;
Bartlett D. Moore III, PhD
Arch Neurol. 2002;59:616-622.
ABSTRACT
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Background Neurofibromatosis type 1 (NF-1) is associated with learning disabilities
and cognitive impairment in childhood and adolescence. Individuals with NF-1
have a propensity for brain hyperintensities on T2-weighted magnetic resonance
images, macrocephaly, and optic gliomas. Few clear relationships between these
central nervous system abnormalities and cognitive function, however, have
been found in this population.
Objectives To determine whether planum temporale (PT) and planum parietale (PP)
morphologic features are associated with learning disabilities in NF-1.
Patients and Methods We measured and compared the surface area, gray matter volume, and asymmetry
of the PT and PP on T1-weighted MRIs from 24 children and adolescents with
NF-1 and an equal number of controls. Relationships between these measurements
and cognitive and academic achievement scores were examined.
Results The left PT in boys with NF-1 was significantly smaller in both surface
area and gray matter volume compared with girls with NF-1 and controls. Boys
with NF-1 also showed greater symmetry between the left and right hemispheres
in this region compared with girls with NF-1 and controls, who showed a pattern
of left greater than right asymmetry of the PT. Intelligence-based discrepancy
scores of reading and math achievement, which are commonly used to define
learning disabilities, were significantly related to PT asymmetry in the NF-1
group as a whole. Less leftward asymmetry of the PT was associated with poorer
reading and math achievement in relation to intellectual test scores.
Conclusions The high susceptibility of individuals with NF-1 to develop reading
and other learning disabilities seems to be related to the development of
the sylvian fissure. These results provide further support for the hypothesized
association between sylvian fissure morphologic features and learning disabilities.
INTRODUCTION
NEUROFIBROMATOSIS TYPE 1 (NF-1) is an autosomal dominant genetic disorder
that affects approximately 1 in 4000 people.1
It is associated with a mutation on chromosome 17 and has highly variable
phenotypic expression. Children with NF-1 have a high incidence of central
nervous system anomalies. Areas of abnormal signal intensity in the brain,
typically visualized using T2-weighted or fluid attenuation inversion recovery
magnetic resonance imaging (MRI) protocols, are observed in approximately
70% of children with NF-1. These hyperintensities are most frequently observed
in the brainstem, cerebellum, basal ganglia, and thalamus.2
Cognitive impairment is also frequently described, and whereas some studies
have shown no relationship between the presence of hyperintensities and neuropsychological
deficits,3-4 others have demonstrated
associations between the presence or absence,5
number,6-7 or location8 of hyperintensities and cognitive impairment.
Macrocephaly and optic gliomas are also commonly observed in children
with NF-1.9-10 Presence of an
optic glioma has not been found to be predictive of cognitive deficits,2, 11-12 but quantitative imaging
studies have revealed increased brain size and gray matter volume to be associated
with degree of learning disability (LD).2 Larger
corpus collosa are also associated with poorer visuospatial skills and academic
achievement.2
Reports of the incidence of LDs in patients with NF-1 vary from 25%
to 61%, whereas 5% to 15% of the general population is estimated to have LDs.13-14 Originally, LDs in patients with
NF-1 were thought to be nonverbal in nature.15-16
More recent evidence suggests that both verbal and nonverbal deficits are
common.6, 16-17 To
date, however, no definitive relationship between central nervous system anomalies
and reading or other LDs has been demonstrated in patients with NF-1. Reading
disability in the general population has been found to be associated with
several cortical abnormalities. Studies of individuals with dyslexia have
shown macroscopic hemispheric symmetry of the planum temporale (PT). An absence
of the usual left greater than right asymmetry that is typically found in
healthy individuals is a well-documented finding in postmortem studies of
dyslexia.18 Early MRI studies also tended to
show left-right symmetry of the PT or rightward asymmetry in reading-impaired
populations, with notable exceptions.19-20
The superior extension of the sylvian fissure, the planum parietale
(PP), has also been associated with reading disability. Robichon and colleagues21 have suggested that phonologic impairment in dyslexia
may be associated with greater PP asymmetry. In addition, PP morphologic features
have been hypothesized to be associated with visuospatial function.22 Although neuroimaging23-26
and lesion27-28 evidence suggests
that this region supports visuospatial processing, few direct correlations
between visuospatial function and PP morphologic features have been reported.
One reason for inconsistency in studies that have examined associations
between sylvian fissure symmetry and reading disability may be heterogeneity
in the genotypes of the samples studied. Some investigators have attempted
to associate specific phenotypic expression of reading disability (eg, dyslexic
patients with vs without phonologic impairments) with neuroanatomic variants.18-19 Others have performed genetic linkage
analysis to identify genomic regions that contribute to LDs.29-32
Our approach was to examine the brains of children who met diagnostic criteria
for NF-1 to assess the hypothesized morphometric-functional relationships
of the sylvian fissure in a population specifically at risk for LDs.
We measured the surface area and gray matter volume of the PT and PP
in children and adolescents with NF-1 and matched controls. Given the incidence
of reading disabilities and other LDs in NF-1, we hypothesized that patients
would show less hemispheric asymmetry of the PT and PP, as has been observed
for individuals with dyslexia in the general population.18
We hypothesized that less PT asymmetry would be associated with poorer performance
on reading and phonologic processing tests. We expected that PT surface area
and gray matter volume would be larger in the patient group, because previous
investigations have shown greater total gray2
and white33 matter volume in NF-1. Finally,
given the tendency of individuals with NF-1 to have visuospatial processing
deficits and the possible association of PP morphologic features with visuospatial
skills, we hypothesized that morphometric differences in this region would
be related to performance on tasks that require visuospatial analysis.
PARTICIPANTS AND METHODS
PARTICIPANTS
Twenty-four individuals diagnosed as having NF-1 and 24 controls were
included (Table 1). Participants
were not preselected based on reading ability but were a subsample of individuals
who received an MRI as part of a larger study of cognitive impairment in NF-1.
One control was a sibling of a participant with NF-1 who had no family history
of the disorder; the control showed no NF-1 characteristics. The patient and
control groups did not differ significantly in age or education level. The
Institutional Review Board (University of Texas, M. D. Anderson Cancer Center)
approved all procedures. Informed consent was obtained from participants'
parents, and assent was obtained from the participants themselves.
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Table 1. Participant Characteristics*
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Eleven participants with NF-1 had hyperintensities visible on T2-weighted
and FLAIR MRI images. No participant had a hyperintensity in the lateral temporal
or parietal lobe (regions of interest for the brain tracings). One participant
with NF-1 had an optic glioma that was untreated and presumed to be nonprogressive.
No control had evidence of abnormalities on MRI.
MRI PROCEDURE
All participants underwent scanning with a 1.5-T EchoSpeed scanner (GE
Medical Systems, Milwaukee, Wis). Sagittal T1-weighted MRI images were obtained
from contiguous sections (2.0-3.0 mm) covering the entire brain using a 3-dimensional
fast spoiled gradient recalled echo sequence (echo time, 4.2 milliseconds;
repetition time, 13 milliseconds; flip angle, 25°; 256 x 192 matrix;
60 sections; field of view [FOV], 220-240 mm; 1 excitation). This protocol
was chosen because it is short enough (<3 minutes) that children as young
as 6 years can tolerate the procedure with minimal motion.
BRAIN MEASUREMENTS
To ensure that comparable regions were examined in each brain, particularly
given the tendency of individuals with NF-1 toward macrocephaly,2, 9
a proportional grid method was used.22 We divided
each hemisphere into 4 equal units and measured sections between 2.25 and
3.25 units from midline, determined as the midsagittal section containing
the anterior and posterior commissures, mammillary bodies, and infundibulum.
The anterior border of the PT was defined as the most anterior Heschl's sulcus
(including cases in which more than 1 Heschl's gyrus was evident).34-35 The posterior termination of the
PT and the starting point of the PP were determined as the bifurcation into
a posterior ascending and descending ramus.19
When the posterior ascending ramus originated before the termination of the
sylvian fissure, the portion of the fissure posterior to the posterior ascending
ramus was included in the PT measurement. Termination of the PP was defined
as the dorsal tip of the posterior ascending ramus.19, 35
In cases where the sylvian fissure merged with occipital and parietal sulci,
termination of the measurements was at the merging point.
Surface contours were manually traced with a computer mouse and ImageJ
software (National Institutes of Health, Bethesda, Md). The sum of the contour
lengths in each hemisphere was multiplied by the slice thickness and pixel
size for surface area estimates. Gray matter area in each slice was subsequently
traced, and volume estimates were obtained by multiplying the sum of the areas
by slice thickness and square pixel size.
Given the potential variability in estimating the anterior and posterior
points of the PT and PP, interrater class correlations were calculated for
the tracers (R.L.B. and G.W.S.). These individuals were blinded to the identity
of the participants' scans. In the 2 hemispheres, interrater class correlations
were each 0.90. Examples of PT and PP tracings are presented in
Figure 1.
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Figure 1. Planum temporale (white) and planum
parietale (black) tracings of a single slice from one participant. The sum
of the surface contours (A) and the areas of gray matter (B) in each slice
were used to estimate the hemispheric surface area and gray matter volume,
respectively, for each region.
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COGNITIVE AND ACADEMIC TESTS
Each participant underwent comprehensive neuropsychological testing
in 5 different domains: reading, math, spelling, phonologic processing, and
visual-spatial processing. The reading domain consisted of Letter-Word Identification
and Passage Comprehension.36 The math domain
consisted of Calculation and Applied Problems.36
The spelling domain consisted of the Spelling subtest from the Wide Range
Achievement Test.37 Phonologic processing tests
included the Test of Auditory Analysis Skills38
and Word Attack.36 The visuospatial processing
domain consisted of the Judgment of Line Orientation39
and Recognition Discrimination40 tests. Scores
for Letter-Word Identification, Passage Comprehension, and Word Attack were
not available for one patient. In addition to examining mean scores, we examined
group differences in discrepancy scores between full-scale IQ41
and academic achievement in reading, math, and spelling. Discrepancy scores
are commonly used to define LDs.42
REGRESSION METHOD
Linear regression analyses were conducted to determine whether PT and
PP asymmetry, surface area, or volume measurements were predictive of performance
on each of the tests. We assessed whether brain measurements accounted for
significant variance in performance above what was accounted for by the group
and sex factors. Group was entered first in each regression analysis, followed
by sex and asymmetry quotient, surface area, or volume measurement.
RESULTS
BRAIN MEASUREMENTS
Surface Area and Volume
Table 2 gives the surface
area and gray matter volume of the PT and PP. A 2 (group) x 2 (sex)
analysis of variance revealed a main effect of group (F1,44 = 10.49, P = .002) and a group-by-sex interaction (F1,44
= 7.04, P = .01) for surface area of the left PT.
Post hoc tests showed that this area was smaller for boys with NF-1 compared
with controls. A main effect of group and a group-by-sex interaction were
also found for gray matter volume of the left PT (F1,44 = 8.23, P = .006, and F1,44 = 5.99, P = .02, for the main effect and interaction, respectively), which
was smaller for boys with NF-1. No significant group differences were observed
in the right PT or the PP of either hemisphere.
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Table 2. Mean (SE) Brain Measurements by Group and Sex*
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Asymmetry
Hemispheric asymmetry ratios were calculated for the PT and PP separately
as (R - L)/[0.5(R + L)].34-35
Controls showed greater leftward PT asymmetry than the NF-1 group in surface
area (F1,44 = 12.24, P = .001) and gray
matter volume (F1,44 = 7.26, P = .01).
Group-by-sex interactions, however, modified these differences (F1,44 = 14.89, P<.001, and F1,44 =
12.38, P = .001, for surface area and volume, respectively).
Boys with NF-1 tended to show less asymmetry than girls with NF-1 and controls.
The PT asymmetry scores are presented in Figure 2. No group differences were found for PP asymmetry.
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Figure 2. Planum temporale (PT) volume asymmetry
score by group and sex. The hemispheric asymmetry score was calculated as
(R - L)/[0.5(R + L)]. NF-1 indicates neurofibromatosis type 1.
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READING AND COGNITIVE PERFORMANCE
Test Scores
Neuropsychological and academic scores are listed in Table 3. Two (group) x 2 (sex) analyses of variance showed
that the NF-1 group performed marginally worse than controls on Recognition
Discrimination (F1,44 = 3.56, P = .07)
and Applied Problems (F1,44 = 3.26, P
= .08). Main effects of sex were observed for the Test of Auditory Analysis
Skills (F1,44 = 6.71, P = .01) and Letter-Word
Identification (F1,44 = 6.13, P = .02).
Girls in both groups outperformed boys on these tests.
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Table 3. Mean (SE) Cognitive Domain Standard Scores by Group and Sex*
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Discrepancy Scores
A main effect of sex was found for the IQ-based discrepancy score for letter-word identification (F1,44 = 11.91, P = .001). Girls in both groups tended to perform above
IQ expectations on this test. A group-by-sex interaction was found for the
IQ-based discrepancy score for Applied Problems (F1,44 = 4.96, P = .03). Girls with NF-1 performed above IQ expectations
on this test, whereas boys tended to perform below expectations (mean ±
SD difference scores, 3.3 ± 13.7 for boys and -9.7 ± 10.3
for girls); male and female control participants tended to perform above their
full-scale IQ test scores (mean ± SD difference scores, -8.4
± 11.0 for boys and -5.6 ± 13.9 for girls).
Regression Analyses
Planum temporale surface area asymmetry accounted for a marginal increase
in predicted variance (R2 change = 0.06)
in Letter-Word Identification discrepancy scores (F1,43 = 3.44, P = .07). Significant correlations were found between PT
surface area asymmetry scores and Letter-Word Identification discrepancy scores
for the NF-1 but not the control group (r23 = 0.43, P = .04, and r24 = 0.04, P = .85, for NF-1 and controls,
respectively). Direct group comparisons of the slopes of the regression lines,
however, were not significant.
Planum temporale gray matter volume asymmetry accounted for a significant
increase in the predicted variance (R2
change = 0.09) of discrepancy scores for Passage Comprehension (F1,43 = 4.87, P = .03). Correlations between PT
volume asymmetry and Passage Comprehension discrepancy scores were significant
for the NF-1 group but not for controls (r23 = 0.46, P = .03, and r24 = 0.17, P = .42, for NF-1 and controls,
respectively); a direct group comparison of the slopes of the regression lines,
however, was not significant (Figure 3).
Surface area and volume of the right PP also accounted for a significant increase
in the predicted variance (R2 change =
0.08 for both surface area and volume) of Passage Comprehension discrepancy
scores (F1,43 = 4.39, P = .04, and F1,43 = 4.07, P = .05, for surface area and
volume, respectively). Negative correlations between these measures, however,
failed to reach significance.
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Figure 3. IQ-based discrepancy scores for
reading comprehension by planum temporale (PT) volume asymmetry in the neurofibromatosis
type 1 (NF-1) (dashed line, Pearson r23
= 0.46, P = .03) and control
(solid line, Pearson r24 = 0.17, P = .42)
groups.
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Planum temporale surface area and volume asymmetry accounted for a significant
increase in the predicted variance (R2
change = 0.11 and 0.08 for area and volume, respectively) of discrepancy scores
for Applied Problems (F1,44 = 6.11, P
= .02, and F1,44 = 4.16, P = .05, respectively).
Correlations between PT surface area and volume asymmetry and the Applied
Problems discrepancy score were significant only in the NF-1 group (surface
area: r24 = 0.47, P = .02; volume: r24 = 0.45, P = .03) (Figure 4).
Direct group comparisons of the slopes of the regression lines did not reach
significance.
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Figure 4. IQ-based discrepancy scores for
applied arithmetic by planum temporale (PT) volume asymmetry in the neurofibromatosis
type 1 (NF-1) (dashed line, Pearson r24
= 0.45, P = .03) and
control (solid line, Pearson r24 = 0.15,
P = .48)
groups.
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COMMENT
We expected to find larger surface area and gray matter volume measurements
of the PT and PP in our sample because we previously demonstrated greater
total gray matter volume in children with NF-1.2
However, we found that both the surface area and volume of the left PT were
smaller in boys with NF-1 compared with controls. Boys with NF-1 also had
less left-right PT asymmetry, similar to what has been reported for reading-impaired
individuals in the general population.18 Although
previous NF-1 studies have measured total brain volume by hemisphere,2, 33 our results suggest that macrocephaly
is not a uniform characteristic across cortical regions.
Comparisons of PT and PP asymmetry in non–reading-disabled populations
have revealed a greater tendency toward leftward asymmetry of the PT and rightward
asymmetry of the PP.35, 43 One
report of PT asymmetry in children without reading disabilities found greater
leftward asymmetry in girls, suggesting that sex may be a significant factor
in the development of hemispheric asymmetry.35
Sex differences in PT asymmetry, however, have not been uniformly observed.44 Although our results showed that boys with NF-1 tended
to have less PT asymmetry than girls with NF-1, we failed to find differences
between boys and girls in our control group.
Overall, the neuropsychological profile of the participants with NF-1
in this study differed in several ways from that described by Cutting et al.13 Although the NF-1 group included herein tended to
perform worse on a visuo-spatial analysis test,40
as has been reported in many investigations,6, 8, 11, 45
as a group they did not differ from controls in reading or phonologic processing.
Nonetheless, we found that in the NF-1 group, IQ-based discrepancy scores
for reading comprehension and applied arithmetic were significantly related
to PT asymmetry. Less asymmetry in the PT was associated with poorer performance
relative to full-scale IQ in the NF-1 group. These relationships suggest that
the susceptibility of individuals with NF-1 to develop LDs is associated with
greater symmetry of the left and right PT.
Larsen and colleagues20 were the first
to suggest that PT symmetry is associated with phonologic processing deficits
in dyslexia. We did not find asymmetry scores to predict phonologic processing
skills, but our ability to detect a relationship between these variables may
have been restricted by the fact that few participants in this sample had
a phonologic deficit. Leonard et al19 suggested
that phonologic dyslexia is associated with cumulative anatomic risk factors,
including the number of perisylvian abnormalities. None of their participants
with a phonologic deficit, however, showed rightward asymmetry or a symmetrical
PT. The potential relationship of PT asymmetry and phonologic skills in the
NF-1 population awaits further investigation, particularly of individuals
who show greater phonologic deficits than those studied herein.
Previous investigations3-4,8
of NF-1 have failed to identify neuroanatomic abnormalities, including hyperintensities
on MRI, that are consistently correlated with the visuospatial deficits commonly
observed in this population. Investigators studying correlates of sylvian
fissure measurements have predicted a relationship between visuospatial skills
and the morphologic features of the PP,22 but
we failed to find one. Furthermore, unlike Robichon and colleagues,21 we did not observe a relationship between phonologic
processing and PP morphologic features. However, we did find that the surface
area and volume of the right PP accounted for significant variance in the
IQ-based discrepancy score for reading comprehension. Greater area and volume
were marginally associated with better reading comprehension relative to IQ.
The advantage of studying relationships between brain morphologic features
and LDs in individuals with a common genetic disorder is that assumptions
can be made about the presumed pathologic condition underlying cognitive impairments.
The prevalence of LDs in NF-1 is much greater than in the general population.
Despite this prevalence, few participants in this sample could be classified
as reading disabled according to discrepancies between academic and intelligence
scores. This lack of phenotypic variability may have therefore limited our
power to detect some morphometric-functional relationships. Nonetheless, the
relationships observed suggest that the high susceptibility of individuals
with NF-1 for reading and math disabilities is related to sylvian fissure
development. Previous studies have demonstrated a relation between other neuroanatomic
and neurocognitive features of NF-1. These include macrocephaly2
and the presence,5 number,6
or location8 of hyperintensities. This study
provides additional evidence of brain-behavior relationships in children and
adolescents with NF-1, specifically sylvian fissure morphologic features and
LDs.
AUTHOR INFORMATION
Accepted for publication November 5, 2001.
Author contributions: Study concept and design (Drs Billingsley and Moore); acquisition of data (Drs Billingsley, Schrimsher, and Moore); analysis and
interpretation of data (Drs Billingsley, Schrimsher, Jackson,
Slopis, and Moore); drafting of the manuscript (Drs
Billingsley and Moore); critical revision of the manuscript for important
intellectual content (Drs Billingsley, Schrimsher, Jackson,
Slopis, and Moore); statistical expertise (Drs Billingsley
and Schrimsher); obtaining funding (Dr Moore);
administrative, technical, and material support (Dr Jackson); study supervision (Dr Moore).
This work was supported by grant R01 NS31950 from the National Institute
of Neurological Disorders and Stroke, Bethesda, Md, and with funding from
the Texas Neurofibromatosis Foundation, Dallas.
We thank Murlidhar Tekchandani, MS, for his meticulous work in the acquisition
and processing of the MRI scans and Bernadette Levy, MEd, for her skill and
dedication in performing most of the neuropsychological evaluations.
Corresponding author and reprints: Bartlett D. Moore III, PhD, Division
of Pediatrics (Box 87), University of Texas, M. D. Anderson Cancer Center,
1515 Holcombe Blvd, Houston, TX 77030 (e-mail: bmoore{at}mdanderson.org).
From the Division of Pediatrics (Drs Billingsley, Schrimsher, Slopis,
and Moore) and the Departments of Neuro-Oncology (Drs Slopis and Moore) and
Diagnostic Imaging (Dr Jackson), University of Texas, M. D. Anderson Cancer
Center, Houston.
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