Children with developmental dyslexia show a left visual

Transcription

Children with developmental dyslexia show a left visual
ARTICLE IN PRESS
Vision Research xxx (2005) xxx–xxx
www.elsevier.com/locate/visres
Brief communication
Children with developmental dyslexia show a left visual
‘‘minineglect’’
Ruxandra Sireteanu a,b,c,*, Ralf Goertz a,b, Iris Bachert a, Timo Wandert a
b
a
Department of Neurophysiology, Max-Planck-Institute for Brain Research, Deutschordenstrasse 46, 60528 Frankfurt, Germany
Department of Biological Psychology, Institute for Psychology, Johann Wolfgang Goethe-University, Mertonstrasse 17, 60054 Frankfurt, Germany
c
Department for Biomedical Engineering, College of Engineering, Boston University, Cumming Street, Boston, USA
Received 20 December 2004; received in revised form 19 July 2005
Abstract
We investigated the performance of children with developmental dyslexia on a visual line bisection task. Dyslexic children did not
show the overestimation of the left visual field (pseudoneglect) characteristic of normal adult vision. These results suggest that children with developmental dyslexia present selective deficits in visual attention, probably involving neural structures located in the
right posterior parietal cortex.
Ó 2005 Elsevier Ltd. All rights reserved.
Keywords: Developmental dyslexia; Attention; Pseudoneglect
1. Introduction
Developmental dyslexia, a neurological condition
afflicting about 5–10% of the school-age population, is
characterized by a selective deficit in reading and writing
abilities, in spite of normal or above average general
intelligence (for reviews, see Shaywitz, 1998; Snowling,
2000). It is generally accepted that children with developmental dyslexia present deficits in phonological processing—the awareness of the sound structure of
words (Shaywitz, 1998). Several neuroimaging studies
showed that, when tested with tasks involving phonological processing, both juvenile and adult dyslexics
have reduced activity in cortical areas in the temporoparietal lobe on the left side of the brain (reviewed in
Habib, 2000). In addition to the phonological impairment, dyslexic subjects show deficits in the processing
of rapidly changing auditory information, implying that
*
Corresponding author. Tel.: +49 69 96769 277; fax: +49 69 96769
742.
E-mail address: [email protected] (R. Sireteanu).
0042-6989/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.visres.2005.07.030
the phonological impairment might result from this
more fundamental deficit. This deficit is correlated with
a severe disturbance in the left inferior prefrontal cortex,
a region known to be specialized for semantic and phonological processing. Both behavioural performance
and cortical activity in the regions involved in the processing of rapid auditory stimuli are improved by intensive, specific training (Temple et al., 2003). The results of
these studies suggest that disruptions in neural responses
occur in the posterior temporo-parietal junction and the
prefrontal left language brain areas of dyslexic subjects.
Based on this disturbed processing in frontal and posterior language networks, it was suggested that developmental dyslexia could be described as a
‘‘disconnection’’ syndrome (Paulesu et al., 1996).
Recent studies reported that developmental dyslexics
show attentional deficits, including prolonged attentional dwell time (Hari, Valta, & Uutela, 1999), a tendency
not to focus visual attention as much as normal readers
(Facoetti, Paganoni, & Lorusso, 2000; Facoetti, Paganoni, Turatto, Marzola, & Mascetti, 2000) and a general
attentional deficit across visual and auditory modalities,
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related to ‘‘sluggish attentional shifts’’ (Hari & Renvall,
2001). Attentional deficits were also related to the syntactic deficits of poor readers (Deutsch & Bentin,
1996), to their contrast sensitivity deficits (Stuart, McAnally, & Castles, 2001) and to their impaired visual
search (Casco & Prunetti, 1996; Vidyasagar, 2001; Vidyasagar & Pammer, 1999).
Visual attention involves the activity of a network of
cortical areas, including areas in the right posterior parietal and dorsolateral prefrontal cortex, known to be involved also in working memory tasks (Kastner &
Ungerleider, 2000; Mangun, 1995; Mesulam, 1999).
Attention can be differentiated between stimulus-driven
(exogenous, automatic, or bottom-up) and goal-directed
(endogenous, voluntary, or top-down). Separate neural
circuits were proposed for the two kinds of attention,
with goal-directed attention involving a dorsal network
including regions in the dorsolateral prefrontal and the
dorsal parietal cortex on the right side of the brain
and stimulus-driven attention involving areas in the prefrontal cortex and the lower parietal and upper occipital
cortex, selective for the attended stimulus properties
(Corbetta & Shulman, 2002). Improvements of activity
in the ventral attentional network are very likely to originate from a top-down propagation of activity from the
fronto-parietal attentional network (Corbetta & Shulman, 2002; Kastner & Ungerleider, 2000).
Here, we addressed the possibility that developmental
dyslexia might reflect a subtle weakness in a string of
cortical areas on the dorsal pathway on both sides of
the brain. Previous studies have suggested that developmental dyslexics show a left ‘‘minineglect’’, suggestive of
a lesion on the right side of the brain (Hari, Renvall, &
Tanskanen, 2001). By using tasks known to be effectuated by specific regions in the dorsal cortical attentional
network on the right side of the brain, we hoped to be
able to gain additional information about the brain circuits affected in developmental dyslexia.
In the neurological condition known as ‘‘hemineglect’’ (or simply ‘‘neglect’’), patients disregard the left
side of their extrapersonal space (cf. Heilman, 1979;
Heilman, Watson, & Valenstein, 1985). When asked to
bisect a horizontal line, the perceived middle is set too
far to the right (Halligan & Marshall, 1992; Schenkenburg, Bradford, & Ajax, 1980); when asked to copy a
visual figure, their drawings are missing the left side.
The condition is most often associated with focal lesions
of the right parietal cortex, usually in the temporo-parietal junction (inferior parietal lobule: Vallar & Perani,
1986) or the superior temporal region (Karnath, Ferber,
& Himmelbach, 2001; for a recent review, see Pisella &
Mattingley, 2004), and is interpreted as a deficit in the
orienting of spatial attention.
Normal adult observers display a reverse asymmetry
of more modest proportions, in that they consistently
overestimate their left extrapersonal space: when asked
to bisect a horizontal line, the left ‘‘half’’ is set shorter
(cf. Bowers & Heilman, 1980; Halligan & Marshall,
1992; von Helmholtz, 1896). This asymmetry is also
found in purely tactile or kinesthetic tasks (Bowers &
Heilman, 1980; Halligan, Manning, & Marshall, 1991).
Bowers and Heilman (1980) were the first to call this
asymmetry ‘‘pseudoneglect’’. Visual pseudoneglect is
dependent on reading habits (Chockron & Imbert,
1993). The overestimation of the left visual field was
interpreted as a bias towards the most attended (usually
left) side of the extrapersonal space. A visual pseudoneglect was described in children as young as 4.5 years of
age (Chockron & De Agostini, 1995).
We investigated whether dyslexic school-age children
show a left ‘‘minineglect’’. We reasoned that, if dyslexic
children show a selective deficit in spatial visual attention, they ought to show a reduced attentional bias towards the left extrapersonal space, suggesting an
involvement of neural structures located in the right
posterior parietal cortex.
2. Methods
2.1. Recruitment of the subjects, inclusion criteria
The subjects were recruited through leaflets sent to
nearby schools and by word-of-mouth. The subjects
had to satisfy the following criteria: no known neurological or psychiatric abnormalities; no ophthalmological
disorders; fully corrected refraction; no medication taken during the 24 h preceding the examinations. Prior to
each experimental session, the subjects were given a
complete orthoptic and psychometric examination.
They were reimbursed 10, -€ for each experimental session as a travel compensation (psychometric and
orthoptic examinations were not reimbursed). Written
informed consent was obtained from all subjects or their
parents after the procedure was fully explained. The
experimental procedures were performed in accordance
with the tenets of the Declaration of Helsinki.
2.2. Observers
The experiments were performed with 30 subjects: 10
non-dyslexic adult observers aged between 21 and 31
years (3 male, 7 female), 10 children diagnosed for developmental dyslexia (aged 8–12 years; 5 girls and 5 boys)
and 10 non-dyslexic children matched to the dyslexic
children for age, gender, general intelligence, and socio-economic status. To avoid the possible influence of
handedness (Bradshaw, Nettleton, Wilson, & Bradshaw,
1977; Scarisbrick, Tweedy, & Kulanski, 1987), only
right-handed subjects were included in the study. Handedness was tested using the Edinburgh test battery. Prior
to the study, the parents of the children were asked to
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complete a questionnaire regarding previous diagnoses
and/or medications of the children. Subjects whose native language was not German as well as children diagnosed or suspected of having an attention deficithyperactivity syndrome (ADHS) were excluded from
the study (n = 2).
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Their task was to indicate, by using two keys on the
computer board, which of the sides of the pretransected
line was perceived as longer. Point of subjective equivalence was assessed by a logistic regression. Transector
location was varied according to a weighted up-down
method (Kaernbach, 1991). Testing was always
binocular.
2.3. Psychometric examination
2.4. Orthoptic examination
Orthoptic examination consisted in the measurement
of: eye alignment, using a cover-uncover test; stereopsis,
tested with the Titmus, Randot, and TNO tests; objective refraction, measured with a Rodenstock refractometer; Snellen corrected visus for single and crowded
optotypes, tested at near and far with a C-test after
Haase and Hohmann; colour vision, assessed with the
Ishihara test; and contrast sensitivity, tested for near
and far with the Vistech Contrast Sensitivity Charts
(VCTS 600). All tests were performed by a professional
orthoptist (I.B.). The results of these tests show that
there are no deficits in basic visual functions in the dyslexic children. The children did not show an increased
incidence of refraction errors or of errors in eye alignment. Their visual acuities and contrast sensitivities were
within the normal range.
2.5. Material and procedure
The procedure was adapted from McCourt (2001).
The subjects were presented with horizontal lines of
two different lengths (14.8° or 22.2°) on a computer
screen. The lines were 0.3° high, and they were pretransected, with the two parts having different black-andwhite polarities on a gray background. Mean luminance
of the computer screen was 30 cd/m2. The luminance of
the white portion of the lines was 125.3 cd/m2, that of
the black portion 19.4 cd/m2, thus yielding a Michelson
contrast of 0.73. The lines could be presented for either
100 or 1000 ms. The subjects were seated at a distance of
57 cm from the screen, in an otherwise darkened room.
3. Results
Consistent with previous findings, the adult observers
showed an overestimation of the left part of the pretransected line, which means that the transector was set too
far to the left (see Fig. 1). The leftward bias varied with
the length of the line and with presentation duration: it
was larger for longer lines and shorter durations, but it
was highly statistically significant for all conditions. The
overall averaged bias was 0.24°, its averaged standard
deviation 0.14° (t (9) = 5.41, p < 0.001; one-sided Student t test).
Non-dyslexic children showed a similar leftward bias
(see Fig. 2) but more shallow slopes of the averaged psychometric curves in all conditions than the adult observers (t (18) = 4.06, p < 0.001). The non-dyslexic children
showed the same tendency as adult observers to show
higher leftward biases for longer lines and shorter durations, but only the individual biases for the longer line
(22.2°) were statistically significant (t (9) = 3.3094,
p < 0.01 for the shorter stimulus duration and
t (9) = 6.32, p < 0.001 for the longer stimulus duration).
The average bias was again 0.24°, the average standard
Visual pseudoneglect
Adult observers (N = 10)
1.00
Probability of answering “left“
Psychometric examination of the subjects consisted
of: intelligence tests, assesed with the CFT 1 and CFT
20 tests (Weiß, 1997); vocabulary and arithmetic tests
(WS, ZF-test); writing proficiency, assessed with the
DRT 2, DRT 3 (Mu¨ller, 1990, 1991), DRT 4-5 (Meis,
1970), WRT 4/5 tests (Rathenow, 1980), and the Westermann tests (Rathenow, Laupenmu¨hlen, & Vo¨ge,
1980); reading proficiency, assessed with the Zu¨rcher
Lesetest (ZLT; Linder & Grisseman, 1996); sustained
attention, assessed with the concentration d2 test (Brickenkamp, 1994), short-term memory tests (HAWIK-R,
HAWIE-R), and a test for phonological discrimination
(syllable sequences, after Mottier).
0.75
0.50
0.25
100 ms, 14.8˚
100 ms, 22.2˚
1.000 ms, 14.8˚
1.000 ms, 22.2˚
0.00
- 1.5
- 1.0
- 0.5
0.0
0.5
1.0
1.5
Transector location (degrees)
Fig. 1. Visual pseudoneglect in normal adult observers (n = 10
subjects). Psychometric curves relate the cumulated probability of
the subjects to answer ‘‘left’’ to the actual position of the transector.
Red curves, shorter lines (14.8°); green curves, longer lines (22.2°).
Continuous lines, stimuli are presented for a shorter duration (100 ms);
dotted lines, stimuli are presented for a longer duration (1000 ms).
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Visual pseudoneglect
Visual pseudoneglect
Adults, control and dyslexic children (N = 10/group)
Control children (N = 10)
1.00
Probability of answering “left“
Probability of answering “left“
1.00
0.75
0.50
0.25
0.75
0.50
0.25
100 ms, 14.8˚
100 ms, 22.2˚
1.000 ms, 14.8˚
1.000 ms, 22.2˚
0.00
- 1.5
- 1.0
- 0.5
0.0
0.5
1.0
1.5
Adults
Controls
Dyslexics
0.00
- 1.5
Transector location (degrees)
- 1.0
- 0.5
0.0
0.5
1.0
1.5
Transector location (degrees)
Fig. 2. Visual pseudoneglect in control children (n =10 subjects).
Symbols as in Fig. 1.
Fig. 4. Averaged visual pseudoneglect in adult control subjects,
control children, and dyslexic children matched for age (n = 10
subjects/group). For each group, the psychometric curves are averaged
over the four stimulus conditions.
Visual pseudoneglect
Dyslexic children (N = 10)
were consistently more shallow. The dyslexic children
differed from the control children by showing no leftward bias in line bisection and even more shallow slopes
of the psychometric curve. This corresponds to a highly
significant rightward bias (t (18) = 2.901, one-sided
p < 0.005), thus confirming our hypothesis of a left
‘‘minineglect’’ in children with developmental dyslexia.
Probability of answering “left“
1.00
0.75
0.50
4. Discussion
0.25
100 ms, 14.8˚
100 ms, 22.2˚
1.000 ms, 14.8˚
1.000 ms, 22.2˚
0.00
- 1.5
- 1.0
- 0.5
0.0
0.5
1.0
1.5
Transector location (degrees)
Fig. 3. Visual pseudoneglect in age-matched dyslexic children (n =10
subjects). Symbols as in Fig. 1.
deviation 0.24°. The overall effect was statistically highly
significant (t (9) = 3.412, p < 0.008).
Dyslexic children showed even more shallow slopes
than the age-matched control subjects (t (18) = 2.384,
p < 0.028; see Fig. 3), but they did not show a bias in line
bisection. The average standard deviation was 0.46°,
overall average bias was 0.13°, which means that, to
be perceived as centered, the transector had to be located 0.13° to the right of the veridical center of the line;
this shift was not statistically significant. Neither the
individual, nor the averaged biases differed statistically
significantly from the objective straight-ahead direction.
Fig. 4 shows a summary of the results of this experiment. For all experimental groups, performance was
averaged over the four conditions. Adult controls and
control children showed the same leftward bias (0.24°),
but the slopes of the psychometric curves of the children
The results of the present study replicate the consistent leftward deviation in subjective line bisection
(‘‘pseudoneglect’’) in normal adult observers (cf.
McCourt, 2001). They also show a similar leftward
deviation in non-dyslexic schoolchildren, thus extending previous reports, in which a pseudoneglect was described in preschool children (Chockron & De
Agostini, 1995). In addition, they demonstrate that
dyslexic schoolchildren do not show a leftward deviation, thus exhibiting a significant left visual ‘‘minineglect’’. We thus extend the previous suggestion of a
left minineglect in adult dyslexic subjects (Hari et al.,
2001). These results add to the evidence in favour of
an attentional deficit in developmental dyslexia, implicating a lesion in the neural structures subserving spatial attention.
The most likely candidates for this deficit are neural
structures involved in visual hemineglect in neurological
patients. These structures are believed to be located
mainly in the posterior temporo-parietal cortex, typically on the right side of the brain (the inferior parietal lobule: Vallar & Perani, 1986; or the superior temporal
region: Karnath et al., 2001; Pisella & Mattingley,
2004). Thus, our findings suggest that developmental
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dyslexia might be associated with a selective attentional
deficit, possibly due to a discrete neural disorder of the
right posterior temporo-parietal cortex.
This suggestion is consistent with the recent reports
of selective impairments, in dyslexic adults, in both auditory (Ben-Yehudah, Sackett, Malchi-Ginzberg, & Ahissar, 2001) and visual (Ben-Yehudah & Ahissar, 2004)
sequential tasks. Ben-Yehudah and Ahissar (2004) suggested that dyslexia might involve a selective impairment
in ‘‘retain-and-compare’’ type of tasks and interpreted
their findings in terms of an attentional impairment
involving the parietal cortex. Thus, it seems that the
hypothesis of a parietal deficit in dyslexic adults (BenYehudah & Ahissar, 2004) can be extended to children
with developmental dyslexia.
The conclusion of a deficit on the right side of the
brain is corroborated by the existence of an impairment,
in dyslexic adult subjects, in a visual contour integration
task (a function known to involve neural structures
located in the right cerebral hemisphere; Simmers &
Bex, 2001). Recent corroborating evidence for a possible
deficiency in the right posterior parietal cortex comes
from the reports of a left inattention and a right overdistractability in visual flanker and reaction time tasks
in developmental dyslexics (Facoetti & Molteni, 2001;
Facoetti & Turatto, 2000).
The brain structures involved in the orienting of spatial attention form part of the dorsal, so-called ‘‘where’’
visual pathway, as opposed to the ventral, ‘‘what’’ pathway (Ungerleider & Mishkin, 1982). More recently,
structures belonging to the dorsal, ‘‘where’’ pathway
were reported to form part of a ‘‘vision-for-action’’
pathway (as opposed to the ventral, ‘‘vision-for-perception’’ pathway; Goodale, 1997). The dorsal pathway was
reported to involve structures in the posterior parietal
cortex and to continue in the dorsolateral prefrontal
lobe (Courtney, Ungerleider, Keil, & Haxby, 1996;
McCarthy et al., 1996; Wilson, Scalaidhe, & GoldmanRakic, 1993), thus providing a continuity for the dorsal
vs. ventral dichotomy of visual processing.
The question arises, whether developmental dyslexics
might show deficits in other brain regions known to be
involved in the deployment of goal-directed spatial
attention (Corbetta & Shulman, 2002; Kastner &
Ungerleider, 2000), in addition to their deficits in the
right posterior parietal cortex, and to their known deficits in the left parietal and left prefrontal cortical regions, involved in rapid auditory and phonological
processing. Several findings suggest that the right prefrontal cortex might be involved as well.
Visual functions requiring the allocation of attentional resources, like serial visual search for conjunctions of
features, were reported to be selectively affected in adult
dyslexic subjects (Casco & Prunetti, 1996; Vidyasagar &
Pammer, 1999). When searching for conjunctions of orientation and shape, children with developmental dyslex-
5
ia exhibited a dramatically elevated number of errors,
but significantly shorter reaction times (Sireteanu
et al., 2005), suggesting an involvement of executive
functions and visual working memory; these functions
are known to be associated with activity of the dorsolateral prefrontal cortex (Baddeley, 1996, 1998). Visual
functions which do not require visual attention (visual
search for single features, like orientation or shape, segmentation of oriented textures and pop-out for elementary visual features), were not affected in the same
dyslexic children, suggesting that extrastriate occipital
regions and areas on the ventral visual pathway are
unlikely to be affected. The dyslexic children did not
show functional deficits in basic visual functions like
visual acuity, contrast sensitivity, binocular status, and
ocular motility, suggesting that the primary cortical
visual areas are not affected (Sireteanu et al., 2005).
Taken together, these findings show that, in addition
to the known deficits in parietal and prefrontal areas on
the left side of the brain, responsible for phonological
and rapid auditory processing, developmental dyslexics
show subtle impairments in a network of cortical areas
responsible for directing and sustaining visual attention,
including areas in the right temporo-parietal and the
dorsolateral prefrontal areas on the right side of the
brain. Thus, dyslexia might reflect a more generalized,
albeit subtle, brain deficit, involving circuits located in
the parietal and frontal areas on both sides of the brain.
Deficits in higher-order, global visual tasks like motion coherence sensitivity (Cornelissen, Richardson, Mason, Fowler, & Stein, 1995; Slaghuis & Ryan, 1999;
Talcott, Hansen, Assoku, & Stein, 2000), visual contour
integration (Simmers & Bex, 2001), and visual change
detection (Rutkowski, Crewther, & Crewther, 2003) suggest an involvement, in developmental dyslexia, of higher-order cortical areas and/or abnormal cooperative
associations between distant cortical loci. The hypothetical disruption of pathways connecting different brain
structures in developmental dyslexics (Paulesu et al.,
1996), as well as their deficits in motor coordination
and automatization (Nicolson & Fawcett, 1993; Nicolson, Fawcett, & Dean, 2001), including deficits in posture, proprioception and oculomotor coordination (cf.
Biscaldi, Fischer, & Aiple, 1994; Biscaldi, Fischer, &
Hartnegg, 2000), appear to coexist with the dysfunctions
in the posterior temporo-parietal and the prefrontal cortex and thus support the suggestion of developmental
dyslexia as a deficit of an extended cortical network.
A prominent hypothesis put forward for the explanation of the visual deficits in dyslexia is the magnocellular
deficit theory, which proposes that dyslexicsÕ impaired
visual performance stems from an abnormal magnocellular pathway, related to a deficit in the processing of
transient stimuli (cf. Cornelissen, Hansen, Hutton,
Evangelinou, & Stein, 1998; Demb, Boynton, Best, &
Hegger, 1998; Eden et al., 1996; Livingstone, Rosen,
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Drislane, & Galaburda, 1991). This hypothesis is still
controversial (Amitay, Ben-Yehudah, Banai, & Ahissar,
2002; Borsting et al., 1996; Skottun, 2000; Spinelli et al.,
1997; Stein, Talcott, & Walsh, 2000; Stuart et al., 2001;
Victor, Conte, Burton, & Nass, 1993; Walther-Muller,
1995).
The magnocellular, the oculomotor and the attentional deficit theories are not entirely independent of each
other: indeed, the magnocellular visual pathway provides
the major input to the dorsal cortical stream, including
areas in the posterior parietal cortex (Mishkin &
Ungerleider, 1982), which are part of the posterior cortical attentional network (Corbetta, Shulman, Miezin, &
Petersen, 1995) and at the same time are involved in
eye movement control (Corbetta et al., 1998). Together
with the dorsolateral prefrontal areas on the right side
of the brain, these areas form part of the cortical network
sustaining the goal-directed, selective spatial attention
(Corbetta & Shulman, 2002; Kastner & Ungerleider,
2000). Thus, developmental dyslexia might involve a
weakness in a string of cortical areas on the dorsal part
of the brain, overlapping partially, but not entirely, with
the magnocellular geniculo-cortical pathway.
In spite of the multitude of its expression modes (cf.
Paulesu et al., 2001; Ramus, Rosen, Dakin, Day, & Castellote, 2003; Williams, Stuart, Castles, & McAnally,
2003), the combination of phonological, oculomotor,
postural, and attentional deficits involved in developmental dyslexia are likely to result from a common
genetic deficit. The puzzling question arises, why some
brain circuits appear to be so deeply affected, while others are spared. The answer to this question must await
further experimentation.
Acknowledgments
Part of the experiments reported in this study were
supported by grants from the Deutsche Forschungsgemeinschaft (Si 344/16-1). We are grateful to Wolf
Singer for support and to our subjects for their patience.
Thanks are due to Johann Schelchshorn and MyungHyun Yoo for support with pilot data acquisition and
to two anonymous referees for helpful comments on
the manuscript.
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