 |
| Volume 4, Number 5, Article 4, Pages 388-402 |
doi:10.1167/4.5.4 |
http://journalofvision.org/4/5/4/ |
ISSN 1534-7362 |
Eye movement control during single-word reading in dyslexics
Manfred MacKeben |
The Smith-Kettlewell Eye Research Institute,
San Francisco, California, USA |
|
Susanne Trauzettel-Klosinski |
Department of Pathophysiology of Vision and Neuro- ophthalmology, University Eye Hospital, Tübingen, Germany |
|
Jens Reinhard |
Department of Pathophysiology of Vision and Neuro- ophthalmology, University Eye Hospital, Tübingen, Germany |
|
Ute Dürrwächter |
Department of Child and Adolescent Psychiatry and Psychotherapy, University of Tübingen, Germany |
|
Martin Adler |
Department of Pathophysiology of Vision and Neuro- ophthalmology, University Eye Hospital, Tübingen, Germany |
|
Gunther Klosinski |
Department of Child and Adolescent Psychiatry and Psychotherapy, University of Tübingen, Germany |
|
Abstract
We investigated whether dyslexics make instantaneous automatic adjustments of reading saccades depending on word length. We used a single-word reading paradigm on 10 dyslexic and 12 normally reading children aged 11-15 years. Eye movements were recorded by scanning laser ophthalmoscope (SLO) while subjects read single words of different length aloud. All subjects passed standardized prescreening tests, which included a reading test, to exclude those with discernible deficits of eyesight, oculomotor skill, or intellectual development. We measured number, direction, frequency, and amplitude of saccades, as well as the durations of inter-saccadic intervals, as functions of word length. The results show that word length influences the number and amplitude of reading saccades in both subject groups, but this relationship showed quantitatively significant group-specific differences: Both groups showed a gradual increase of the saccade amplitudes in either direction dependent on word length, but the gain of this function was significantly lower in the dyslexics. The durations of holding phases between saccades were significantly longer in the dyslexics, and accordingly, we found a lower rate of occurrence of saccades per unit time in the dyslexics. Forward saccade amplitudes showed no correlation with the duration of the preceding or following holding phases in either group. The data show that the mechanisms enabling dyslexics to make instantaneous adjustments of reading saccades depending on word length are present but quantitatively impaired. This supports the view that these adjustments may help dyslexics to increase reading speed, but that they cannot utilize them to the same extent as normal readers.
 |
|
History
Received April 3, 2002; published May 14, 2004
Citation
MacKeben, M., Trauzettel-Klosinski, S., Reinhard, J., Dürrwächter, U., Adler, M., & Klosinski, G. (2004). Eye movement control during single-word reading in dyslexics.
Journal of Vision, 4(5):4, 388-402,
http://journalofvision.org/4/5/4/,
doi:10.1167/4.5.4.
Keywords
dyslexia, perceptual span, saccades, inter-saccadic, language processing
for related articles by these authors
for papers that cite this paper |
Reading has been investigated in numerous studies and
fundamental insights regarding the contributing brain mechanisms have been
gained (Pugh et al., 2000; Salmelin,
Helenius, & Service, 2000; Simos et
al., 2000). Much of the previous work
concentrated on reading eye movements as the most observable manifestation of
this complex process (e.g., Bouma, 1973;
Bouma & de Voogd, 1974; Legge, Pelli,
Rubin, & Schleske, 1985, Legge, Ahn,
Klitz, & Luebker, 1997; McConkie &
Rayner, 1976; O'Regan, 1980; Rayner & McConkie, 1976; Rayner & Pollatsek, 1981).
We have used eye movement recordings as a tool to
investigate fundamental aspects of oculomotor control during reading and their
differences between normal readers and dyslexics. The most common measure of
reading performance is speed, and accomplished readers can reach levels of 200
words per minute (WPM) and more while reading silently, whereas dyslexics hardly
exceed 100 WPM, even after years of training. During the time-consuming process
of learning to read, some children have to fight overwhelming odds before they
get diagnosed as “dyslexic.” Because of the great psychological,
societal, and economic impact of a reading impairment, the problem has been
researched extensively, and the results support different explanations for
dyslexia. These include deficits affecting phonemic awareness (Bradley &
Bryant, 1983; Rudel, Denckla, &
Broman, 1978; Snowling, 1980; Swan & Goswami, 1997; for a review, see Njiokiktjien, 1994), the grapheme to phoneme
conversion (Golden & Zenhausern, 1983), processing of visual signals (Di
Lollo, Hanson & McIntyre, 1983;
Jacobs, 1986; Lennerstrand & Ygge, 1992), selective deficits in the
magnocellular stream of visual input (Best & Demb, 1999; Borsting, Ridder III, Dudeck, Kelly,
Matsui, & Motoyama, 1996; Demb,
Boynton, Best, & Heeger, 1998a; Demb,
Boynton, & Heeger, 1998b; Stein &
Walsh, 1997), asymmetric crowding (Geiger
& Lettvin, 1987), deficits of
attention (Stein & Walsh, 1997;
Steinman, Steinman & Garzia, 1998),
as well as the much debated role of oculomotor deficits (Rubino & Minden, 1973; pro: Biscaldi, Fischer, & Aiple, 1994; Biscaldi, Fischer, & Hartnegg, 2000; Eden, Stein, Wood, & Wood, 1994; Pavlidis, 1991; contra: Brown, Haegerstrom-Portnoy,
Adams, Yingling, Galin, Herron, & Marcus, 1983; Black, Collins, De Roach, & Zubrick,
1984; De Luca, Di Pace, Judica, Spinelli,
& Zoccolotti, 1999; Olson, Conners,
& Rack, 1991; Stanley, Smith, &
Howell, 1983).
Consequently, many subtypes of dyslexia have been
described (Boder, 1973; Njiokiktjien, 1994; Stark, Giveen, & Terdiman, 1991). A recent study of our own also has
provided experimental evidence that a phonemic deficit may underlie the problem
in all dyslexics, which can be made worse in some who show an additional
visual/eidetic deficit that impairs pictogram-naming performance
(Trauzettel-Klosinski, MacKeben, Reinhard, Feucht, Dürrwächter, &
Klosinski, 2002). For the current study,
however, we did not distinguish between subtypes.
Readers scan the text by a pattern of eye movements
that is characterized by horizontal saccades and holding phases between them.
(We elect not to call the latter “fixations,” because they lack the
characteristic fixational eye movements (Cunitz & Steinman, 1969). Neither the saccades nor the holding
phases are always quantitatively the same, so that the question of what controls
their variations has been the focus of much discussion. It is widely accepted
that linguistic and phonemic factors exert a dominating influence, but visual
characteristics are important also (Bouma & de Voogd, 1974; Jacobs, 1986; Rayner, Sereno, & Raney, 1996; Snowling, 1980; Whittaker & Lovie-Kitchin, 1993; Wolf & Bowers, 1999).
A central factor in trying to understand a reading
impairment that is common in countries using alphabetic languages is the fact
that words consist of strings of letters. Groups of letters have to be
identified as syllables, which together form words, whose phonemic equivalent
must be retrieved from memory. Although the use of letters seems to be at the
heart of the problem, the ability to quickly recognize single letters will not
make a person a fluent reader. This is supported by the fact that reading
letter-by-letter slows down reading, which can be seen in normal beginning
readers or in patients with extremely restricted visual fields
(Trauzettel-Klosinski & Reinhard, 1998). Rather, it is the ability to let the
eye jump from one group of letters to the next that can make the process fast.
Reading speed and fluency are thus achieved by sequentially placing strings of
letters (parts of words, complete words, or even groups of words) on a central,
asymmetric horizontal strip of the central visual field, a dynamic behavioral
measure called the “perceptual span” (McConkie, & Rayner, 1975;
McConkie & Rayner, 1976;
Taylor,
1957;
Tinker, 1958).
In addition, readers need the ability to let their gaze
rest in one place just long enough to take in the information needed for
recognition and for gauging the next eye movement. This process requires
simultaneous acquisition of visual information from more than one letter and,
thus, possibly parallel processing (Rayner, 1983, p.102; Schroyens, Vitu, Brysbaert,
& d'Ydewalle, 1999) of which even
some dyslexics seem to be capable (Van Strien, Bouma, & Bakker, 1993), or parallel saccade programming
(Henderson & Ferreira, 1993;
Morrison, 1984). The duration of the
oculomotor holding phases between saccades have been found to be longer in
dyslexics than in controls performing search tasks (Olson et al., 1991), in a subgroup of dyslexics in an
oculomotor task (Biscaldi et al., 1994)
and during reading (Adler-Grinberg & Stark, 1978). In addition, Ciuffreda, Bahill,
Kenyon, and Stark ( 1976) reported that
one "slow reader" (case 2, page 391) had increased "fixation durations." On the
other hand, Rubino and Minden ( 1973) found
no such differences. Clearly, the question whether inter-saccadic holding phases
are longer in dyslexics warrants further research.
Thus, where and when to place gaze on the text during
reading might be a function of the width of the perceptual span and of gauging
each saccade amplitude accordingly (Jacobs, 1986). It has been shown that linguistic and
visual aspects of the reading material contribute to the control of this process
(O’Regan, 1979, 1980; Rayner & Pollatsek, 1981). A particularly interesting fact is
that the brain can adjust saccadic amplitudes according to word length: O'Regan
( 1980) reported that normal readers tend
to use longer saccades within the word when reading a long word and shorter ones
to read a short word. The mechanism controlling this process has not been
identified yet, nor has it been shown whether it is present in dyslexics also.
As an instantaneous and automatic adjustment of saccade amplitude has the
potential to make reading faster and more fluent, one could speculate that a
lack of such a mechanism might be one of the reasons underlying diminished
reading speed in dyslexics. Thus, our investigation was undertaken to find
answers to the following
questions:
1.Is there an instantaneous and automatic adjustment of reading saccade amplitudes to word
length in dyslexics?
2.If yes,is the mechanism quantitatively operating at the same level as in normally
reading children of comparable chronological
age?
3.Is the increased
absolute number of reading saccades reported in dyslexics, at least among
others, caused by an increase of the number of saccades per unit
time?
4. Are the holding phases of the dyslexics' eye movements during reading longer than in
controls?
We base the rationale for our study
design on the facts outlined above. Hence, we hypothesize that we will be able
to manipulate the saccade gauging mechanism directly by varying word length to
create a base for comparison with previous work (O’Regan, 1980). Restricting the reading material to
single words will minimize linguistic control, because it minimizes guessing or
lexical inference based on knowledge of the dictionary (Mansfield, & Legge,
1999) or on knowledge of the context.
The fact that the words will be read aloud will monitor in real time whether the
word was read correctly.
We concentrated on subjects fulfilling the criteria
defined by ICD10 (World Health Organization, 1996) and those for "specific dyslexia" (see
Stark et al., 1991) to limit the
heterogeneity of the experimental group. We did not include those whose poor
reading performance could be accounted for by any other explanation (e.g.,
deficits of the visual or oculomotor system, a primary speech impediment, or an
impeded development of intelligence or general cognitive functions). Second, we
used text reading speed as the distinguishing criterion between subject
groups.
Partial and preliminary results of this study have been
previously communicated (Trauzettel-Klosinski, Klosinski, Sadowski, &
Tornow, 1997; Trauzettel-Klosinski,
Reinhard, Klosinski, & MacKeben, 1999) .
The experimental design included four steps:
Step
1 tested reading speed for continuous text with subsequent assignment to
the dyslexic or the control group.
Step
2 consisted of a psychological and psychiatric evaluation of all subjects
assigned to the dyslexic group.
Step
3 investigated the visual capabilities by a complete ophthalmological and
neuro-ophthalmological examination of the members of the both groups.
Step
4 consisted of the main experiment: reading single words by dyslexic and
control subjects.
Group assignment and pretesting
The diagnosis of dyslexia was based on the criteria
defined by ICD10 (20), so that the results of reading and writing tests were at
least 2 SDs below the level to be
expected based on the age and IQ of the child.
The candidates for the dyslexic group were further
pretested to eliminate additional disorders as explanations for their poor
reading performance. The assessment was based on standardized reading tests,
such as the Zürich reading test (Linder & Grissemann, 1980), intelligence tests (the Wechsler
Intelligence Scale for Children [WISC-R, Tewes, 1983] or the Colored Progressive Matrices
[Raven, Court, & Raven Jr., 1980],
spelling tests (the Diagnostic Orthography Test, 1980) for the appropriate age groups, and
attention tests (e.g., “Test d2”, Brickenkamp, 1981).
As a result of the pretests for the different deficits,
three children were excluded from the list of subjects due to the presence of a
brain tumor that could affect reading, congenital nystagmus, and unstable
fixation. Two groups of subjects were selected for further experiments, 10
dyslexics and 12 normally reading children, aged 11 to 15.5
years.
All data on reading text and single words were obtained
during monocular viewing using a scanning laser ophthalmoscope (SLO) (model 101,
Rodenstock). The stimuli were scanned directly onto the retina by a laser beam
that was modulated by an acousto-optic modulator. Thus, the SLO records the
absolute position of the fovea and that of the stimulus with a spatial
resolution of < 5 arcmin. This is
based on the relative accuracy by comparison with a reference frame, which can
be made with
+/-
1 pixel accuracy, corresponding to
+/-
2 arcmin. The video frequency of 50 fields/s allowed field-by-field analysis
with a temporal resolution of 20 ms. The main advantage of this method is that
it allows reliable recordings that are not dependent on a calibration, because
fovea and stimulus are visible simultaneously and their distance can easily be
converted to units of visual angle off-line. In addition, the method provides an
automatically synchronized sound
recording.
For the preliminary reading tests, the SLO scanned
paragraphs of text into the eye that came from a simple German story of
approximately fourth-grade equivalent. The subjects saw the text as black on a
bright red background of 3.6 ×
104
trolands at 97% Michelson contrast and
read the text aloud. Each paragraph contained 6–7 lines of between 18.1
deg- and 19.7-deg line length. The font was Times New Roman and capital letters
subtended 0.64 deg (38.4 arcmin), which corresponds to 1.4 times the size of
newspaper print at 25-cm distance.
All statistical tests were performed by StatView (v
4.51) software on a personal computer. We used means and
SDs only for the analysis of the
preliminary oculomotor experiments, because they are sensitive to outliers,
which was desirable here, and because their use for this purpose is widely
accepted.
For the statistical analysis of the text reading test
and the main experiment, we made no assumptions regarding a normal distribution
of the data and, thus, used nonparametric methods. This precaution was confirmed
by visual comparison with model Gaussian curves, which showed that some of the
data deviated substantially from normal distributions. Hence, all results of the
main experiment are reported as medians with the inter-quartile range (IQR) as
measure of variability. Group comparisons were performed by the Mann-Whitney
U-test (MWU), and Spearman's rho was used as a measure of correlation.
In cases where printed scattergrams indicated a strong
linear relationship, we used linear regression analysis to calculate the
coefficient of determination
r2.
The recordings were performed on the dominant eye, as
determined by a peephole test. In the preliminary reading tests, the children
read continuous text aloud. All experiments were performed at the Department of
Pathophysiology of Vision and Neuro-Ophthalmology, University Eye Hospital,
Tübingen,
Germany.
Two preliminary experiments were designed (1) to
separate the subject groups by their defining variable under controlled
conditions and (2) to quickly assess whether any of the dyslexic group showed an
obvious deficiency of oculomotor control, which has been reported as a possible
origin of reading problems (see Biscaldi et al., 1994; Pavlidis, 1991). In Experiment 1, each subject read text aloud that
was scanned onto the retina by the SLO, while the movements of the retina were
recorded. In Experiment 2, subjects fixated a
central mark for 10 s to test fixation stability, made 2–4 goal-directed
saccades to each of three marks at
5 ° right and
5 ° left and back to the center to
test saccade accuracy for 10–20 s, and maintained fixation on each mark
for at least 1 s.
Both groups of children read aloud a minimum of three
6–8 line paragraphs of German text. Members of the control group read the
texts at a speed of 114–177 WPM with a median of 143.0
(IQR = 33.0). The speeds were, as
expected, much slower in the dyslexic children, ranging from 24 to 89 WPM with a
median of 45.0 WPM (IQR = 27.25). Due
to our selection criteria, the data from the two groups showed no overlap, and
the difference was statistically highly significant (MWU,
p
= .0001).
While the normal readers showed a moderate correlation
of reading speed with age ( rho =
0.593), which could be expected according to McConkie, Zola, Grimes,
Kerr, Bryant, & Wolff ( 1991), the
dyslexic showed only a very weak one using the same texts
( rho =
0.192). 2. Stability of fixation and accuracy of ± 5-deg saccades
Fixation stability was measured as the
SD of the mean eye
position calculated as
(x2
+
y2)1/2
for 10-s fixation intervals (i.e., in a continuous sequence of 500
video fields). The ranges of SDs
overlapped widely (dyslexics: 0.075
– 0.213 deg; controls: 0.050
– 0.166 deg), group averages were
close (dyslexics: ± 0.135 deg;
controls: ± 0.097 deg), and the
difference was not statistically significant (MWU-test,
p
= .065).
Saccadic accuracy was measured as the mean eye position
after 5-deg saccades to the right and left and middle. Group averages were for
the dyslexics
(Left
= –5.23 deg;
Middle
= –0.10 deg;
Right
= 4.91 deg) and for the controls
(Left
= –5.09 deg;
Middle
= –0.07 deg;
Right
= 4.99 deg). The difference for
none of the positions was statistically significant
(p
> .3).
Gaze stability after 5-deg saccades was measured as
mean SDs of the mean horizontal
components at the same three positions:
5° left, middle, and
5° right: Group averages of the
SDs showed small but not statistically
significant differences (MWU,
p
> .4): dyslexics:
Left
= 0.29;
Middle
= 0.24;
Right
= 0.18; controls:
Left
= 0.20;
Middle
= 0.23;
Right
= 0.21.
These results allow the tentative conclusion that the
small and not statistically significant differences of oculomotor accuracy found
here are not likely to be the cause of these children’s dyslexia and
cannot account for the large differences in reading performance.
In the main experiment, only single German words were
used. Each subject read three words of each of the following lengths: 2, 3, 4,
5, 6, 7, 8, 10, 12, and 14 letters per word. Thus, each subject read 30 words
aloud while they were scanned onto the retina by the SLO. Before each trial, the
subjects fixated a central fixation mark, which allowed us to vary the alignment
of the target words. Thus, one of the three words at each of the 10 word lengths
was right aligned, one was left aligned, and one was centered on the fovea. Figure 1 shows the SLO picture of a subject’s
retina and a target word as seen by the
examiner.
Figure 1. SLO image showing the subject’s
retina and the eight-letter target word “springen” (to jump) seen by
the investigator simultaneously. Note that the word appears upside-down in the
investigator’s view, but not in the subject’s view.
The subjects were instructed to read each word aloud.
No special instructions regarding speed or fluency were given. Each trial
started with the appearance of the word and ended when the subject had
articulated the word correctly.
Continuous
images of the retina and stimuli were recorded on videotape together with a
vertical interval time code (VITC). This allows giving every frame of video its
own unique identifying number.
Analyses of the data were performed off-line in two
stages: The primary analysis used a semiautomatic computer program based on
retinal landmarks (vessel branchings). It calculated the horizontal and vertical
coordinates of the foveola relative to the target image. The video frequency of
50 fields/s allowed field-by-field analysis with a temporal resolution of 20 ms.
Between 2,000 and 6,100 video fields were analyzed for each subject, depending
on the time spent to read all 30 words.
In the second stage, time functions of the horizontal
eye position component were printed and analyzed graphically by ruler in
millimeters (estimated accuracy of judgment, 0.2 mm), which were then translated
into minutes of arc. Thus, the accuracy of measurement was equivalent to 2
arcmin, which is below SLO resolution. In addition, the width of a lower case
" n" (here called
n-space
= 28.8 arcmin) was universally used as an average letter space. A
regressive (backward = leftward)
saccade was analyzed only if it could be considered part of the reading strategy
(i.e., if it was either followed by at least one more forward saccade and if it
was not a "reset" saccade at the end of an episode that returned the eye to the
position where it had been at target appearance). Figure 2 illustrates the data analysis
schematically.
Figure 2. Schematic representation of an eye
movement trace like the ones obtained from the primary analysis of SLO data that
were then used for graphical analysis. The trace denotes the horizontal position
of the fovea; the vertical axis is time. Forward saccades (F1+2), a backward
saccade (B1, here a "reset" at the end), and three holding positions (H1, 2 + 3)
signifying which part of the word fell onto the fovea (shown by vertical arrows
from H2 and H3). The distances to word beginning (DWB) and end (DWE) show the
foveated points when the subject started and ended to read.
Results of the main experiment
We report a detailed analysis of the characteristics of
eye movements made during reading of 30 words of different lengths by 22
subjects (i.e., 660 words all together). Responses of the different variables
will be reported one at a time below.
The differences in reading speed were obvious not only
while reading text but also during reading single words. This was measured as
time to recognition (target appearance to beginning of articulation). The
overall time that subjects needed to read all 30 words varied greatly in the
dyslexics (50 to 122 s, median = 71.5,
IQR = 35.0), but little in the controls
(40 to 50 s, median = 45.0,
IQR = 9.0). The two distributions
touched, but did not overlap, and the group difference was statistically highly
significant (MWU, p
= .0001).
When the short words that are very frequent in German
were excluded from the analysis, the coefficient of determination turned out to
be only 0.068, indicating a negligible influence of word frequency.
The control subjects read each word in 1–2 s,
regardless of length. The values for the dyslexics, on the other hand, varied
substantially. To reduce the noise in the data, we compared recognition times
for short words (2-4 letters/word), for medium length words (6-8 letters/word),
and for long words (10-14 letters/word). The group differences were highly
significant in all three word-length classes, with
p
< .0014 to
p
< .0001. Comparing the medians of the time taken to read the three
shortest versus the three longest words [in s/word], the value for the control
group increased from 1.3 to 1.8 s/word (IQR =
0.14 and 0.28, respectively).
The dyslexics showed a steeper increase from 1.5 to 3.6 s/word (IQR
= 0.26 and 1.91, respectively). The
absolute maximum was 18 s for a 14-letter word, during which the subject's eye
"stepped" through the entire word four times (three of which are shown in Figure 3). This strategy of going back to start
over at or near the word beginning was seen in 7 of the 10 dyslexics, whereas
the other 3 tended to spend more time making many small forward
saccades.
Figure 3. Two
examples of oculomotor behavior while the same four words are read by a dyslexic
(yellow) and a normally reading child (blue) of comparable age (aged 12.8 &
13.4 years). The records show only horizontal movements; time progresses from
top to bottom, and the target word is visible at the top of each recording. The
words could be right aligned, left aligned, or centered. Note that the SLO
allows a direct registration of target and fovea, so that the eye position line
running between the letters b and e in the first word of the control subject
(top left) means that the subject’s fovea looked exactly at that spot
until a small rightward saccade was performed. The time-to-word recognition was
measured from the appearance of the word to the beginning of vocalization.
Comparison between the subjects shows the prolonged struggle that the dyslexic
child had to go through to read words of eight and more letters.
Number of forward saccades per word
We investigated the number of forward (progressive) saccades
(“F-saccades”) necessary to correctly read all 30 words. The
dyslexics made more F-saccades to read them (21 to 232,
median = 90,
IQR = 127) than the control group (26
to 111, median = 54,
IQR = 42). The number of F-saccades was
a function of word length. The dependence of the number of F-saccades per word
is well described by a linear relationship
(r2
= 0.98 for the dyslexics
and
r2=
0.96 for the controls),
with a steeper slope for the dyslexics than for the controls. Group differences
were tested for each word length separately, and they were found to be
statistically highly significant for all words of five or more letters (MWU,
p
< .007).
This could, at least in part, be caused by the
cumulative effect of the many times that some dyslexics made a return sweep of
80% or more of the word length and
started over trying to read the word. Therefore, we separately counted the
F-saccades made only during the first pass through a word for the dyslexics. If
a backward saccade that did not qualify as a return sweep occurred, subsequent
F-saccades were counted only if they led the fovea further rightward than it had
been before. The dependence of the number of F-saccades on word length was still
linear. To simplify comparison, we formed three groups of word lengths: short
(2–4 letters), medium (5–8), and long (10–14). The median
numbers of F-saccades were found to be almost identical in both subject groups
for short words (0.29 [controls] vs. 0.30 [dyslexics]). For medium and long
words, however, the medians in the dyslexics (0.41 and 0.43) were approximately
double of those for the controls (both
0.23). Rate of occurrence of forward saccades
To investigate whether the higher number of F-saccades
could be due to a higher absolute rate of occurrence per unit time, we divided
the total number of F-saccades made by each subject by the sum of seconds spent
reading all 30 words. This quotient showed an increase from the shortest to the
longest words by a factor of 4 in the dyslexics (0.45 to 1.89 saccades/s) and a
factor of 2.3 in the controls (0.84 to 1.94 saccades/s). The relationship was
again approximately linear
(r2
> 0.87 for both groups), but the difference between the groups was not
statistically significant (MWU,
p
= .82).
For further conclusions regarding the rate of
occurrence per unit time, see also Duration of
holding phases.
Forward saccade amplitudes
The amplitudes of all F-saccades were measured for both
groups (dyslexics:
N
= 1076; controls:
N
= 619). The medians at the different word lengths varied between 17 and
68 arcmin in the dyslexics (equivalent to 0.6 and 2.2 n-spaces), and between 20
and 106 arcmin in the controls (0.7 to 3.5 n-spaces). Their dependence on word
length (see Figure 4) was positive in all
subjects of either group and could be described as linear in the controls
( r2
= 0.98), and best for the dyslexics as a second-order polynomial
( r2
= 0.96). The slopes of
these functions varied more widely in the dyslexics (1.69 to 8.3,
median = 3.3,
IQR = 2.89) than in the controls (6.35
to 9.99, median = 7.03,
IQR = 1.45). They showed no appreciable
correlation with either text reading speed or subject age. The group differences
at word lengths of 10 letters per word and above were statistically highly
significant
( p
<
.003).
Figure 4. Median
amplitudes of F-saccades with interquartile ranges of forward saccades during
reading of single words dependent on word length. Note that there was also a
slight decline in word frequency in the longer words, but word length could be
shown to be the stronger influence with
r2
being 1.5-1.6 times higher for length versus frequency. Up to five-letter word
length, amplitudes in the dyslexic children (bottom,
N = 1125) adapted equally to those in
the controls (top, N= 630), but then
grow at a weaker rate. The group differences at word lengths of 10 letters per
word and above were statistically highly significant
( p < .003). It cannot be ruled out
that word length inversely correlates with word frequency and familiarity (see
Discussion), although their influence on a word
reading task is likely to be weak here due to the unequivocal rules of
pronunciation in German, in contrast to English.
Eye movement stops near the word end
None of the subjects moved the fovea to the last letter
of left-aligned and centered words, but rather stopped some distance before. We
measured this distance-to-word-end (DWE) for these words from four-letter length
on upward. These data contain only 16 such episodes per subject (eight word
lengths, two kinds of alignment). A schematic example of this behavior is shown
in Figure 2, whereas Figure 3, top left, shows data from a control
subject (see first three words).
The median DWE across subjects for each word length
ranged from 34 to 51 arcmin (1.2 to 1.8 n-spaces) in the dyslexics, and from 41
to 125 arcmin (1.4 to 4.4
n-spaces) in the
control group. The group difference was statistically significant
(p
< .0025). For the longest words of
≥ 10 letters length, DWE in the
controls was always at least double as large as in the dyslexics. DWE correlated
with word length only weakly in the dyslexics
(rho = 0.373), much less than F-saccade
amplitudes, which was not so in the control group (rho
= 0.82), where the relationship
could be reasonably fit by a linear function
(r2
= 0.76).
Eye movement stops near the word beginning
Equivalent data were measured as the distance to word
beginning (DWB) for the right-aligned words (i.e., the point where subjects
started to read after a large leftward saccade). Figure 3 shows an example (top left) where the
control subject reads the right-aligned word “empfehlenswert.” This
could be done only in
eight trials per subject (eight word lengths, one alignment). The medians showed
a range of 42–56 arcmin for the dyslexics (equivalent 1.5 to 2 n-spaces)
and of 61–124 arcmin for the controls (2.1 to 4.3 n-spaces). The group
difference was again statistically highly significant
( p
< .0008). Here too, the controls showed a strong correlation of DWB
with word length (rho = 0.90) and a
linear relationship
( r2
= 0.91), whereas the dyslexics
did not ( rho =
0.38). Number of backward saccades
As can be expected, the dyslexics made many more backward (regressive)
saccades ("B-saccades") during the reading episodes of all 30 words (369 vs.
170), with a median of 35 (IQR = 37)
per subject (range, 9 to 72). The corresponding values for the control group
were 15 (IQR = 7) per subject (range, 1
to 27). While the number of B-saccades increased with word length in the
dyslexics, it did not in the control group. Group comparison showed
statistically significant differences for all word lengths from seven letters
upward
(p
< .05).
Backward saccade amplitudes
As in the F-saccades, the median amplitudes of the
B-saccades were larger in the control group and ranged from 10 to 92 arcmin,
whereas those for the dyslexics ranged from 20 to 61 arcmin. In both groups the
amplitude increased with word length, a tendency that ended at a word length of
10 letters in the dyslexics (see Figure 5).
Figure 5. Median
amplitudes with interquartile ranges of backward saccades during reading of
single words dependent on word length. As in Figure
4 (see legend), decreasing frequency of longer words had only a minor
influence on eye movement amplitudes. Here the dyslexics (bottom,
N = 457) performed equal to the
controls (top, N = 338), at least up to
a word length of 10 letters. Regarding word length in relation to frequency and
familiarity, see Discussion and the legend of Figure 4.
Duration of holding phases
The dyslexic subjects showed longer median durations of
the holding phases between forward saccades (124 to 877 ms,
median = 297,
IQR = 158,
N
= 629) than in the controls (74 to 581 ms, median
= 250, IQR
= 110,
N
= 372), although the distributions overlapped (see Figure 6). The difference was statistically highly
significant (MWU,
p
< .0001). This shows that the rate of occurrence of F-saccades was, in
fact, lower in our dyslexics than in the control
group.
Figure 6. Group comparison of median holding durations (inter-saccadic intervals) while reading single words (yellow bars = dyslexics, blue bars = controls). Note the overlap between the groups. The difference between the group medians is statistically highly significant (MWU, p < .0001).
Regarding word length in relation to frequency and familiarity, see
“Discussion” and the legend of Figure
4.
Investigating the relationship of holding durations to
word length like O'Regan ( 1980), we found
a moderate dependence only in 10/12 members of our control group, with rho
ranging between 0.02 and –0.66
(median = –0.36,
IQR = 0.485). In the dyslexics, on the
other hand, we found that the dependence of duration of holding phases on word
length was entirely inconsistent: Five subjects had a mild to moderate negative,
four had a similar positive correlation, and one had none
( rho < 0.06). This correlation
varied between 0.595 to –0.717
(median = 0.111,
IQR = 0.70), which was larger than in
the control group. The medians for the subgroups of dyslexics with
positive/negative rho were 0.349 and
-0.367, respectively. Furthermore, word
length dependence correlated moderately with text reading speed
( rho = –0.538), but not with
subject age.
We hypothesized that a long F-saccade might be fostered
by a long preceding holding duration, which allowed processing of more letters
that lay ahead. In this case, any F-saccade amplitude should show a correlation
with the duration of the preceding holding phase. We tested this relationship in
1,146 pairs of values and found that the results varied strongly between
individuals, regardless of subject group. Only weak correlation coefficients
were found in both, the dyslexics (rho =
–0.357 to 0.262) and the controls
(rho = –0.481 to 0.355).
This hypothetical relationship was then reversed, and
the same calculation was performed for each forward saccade and the duration of
its following holding phase. The
rationale was that a longer F-saccade brings more letters into the perceptual
span for processing during the next holding phase than a short one, and that
this might necessitate a longer holding phase to allow adequate time for
processing.
Hence, we tested the correlation of all F-saccade
amplitudes with the durations of the following holding phases. We printed the
individual data sets out as scattergrams and visually checked for obvious
nonlinear relations, but none was found. Neither group showed an appreciable
correlation, with rho between
–0.264 and 0.280 for the
dyslexics and between –0.334 and 0.219 for the controls.
The influence of phonemic/linguistic factors
We varied the influence of these factors here only by
manipulating word length, while tables assessing the vocabulary of young German
teenagers were not available to us at the time. The frequency of occurrence of
each word in the language is likely to be of lesser importance, because Inhoff
and Rayner ( 1986) used a comparable
paradigm in their “one-word-window condition” and found no influence
of word frequency on saccade size or first fixation duration (see their p. 435).
However, as their paradigm was not strictly identical to ours, we cannot
completely rule out the possibility that differences in word frequency may have
influenced the measured eye-movement parameters. This will be investigated in a
subsequent study.
Familiarity with a word is not likely to have played as
important a role here as it would for children reading English, due to the
straight-forward rules of pronunciation in German. This was shown by experiments
on children reading German (Wimmer, 1996;
Wimmer & Goswami, 1994) and similarly
unambiguous languages such as Italian (De Luca et al., 1999) and Spanish (Goswami, Gambert, & de
Barrera, 1998). However, a slight
influence on the eye movement parameters investigated here cannot be ruled
out.
It is not surprising that the sum of the durations of
single-word reading episodes in our dyslexic group was significantly longer than
that in the control group. It reflects the “struggle” to read (see
Figure 3), which often involved starting over at
the beginning of the word. Although the median durations that were needed to
read words were significantly longer in the dyslexics
( p
< .002), they were close for words up to four letters (1.48 s
[dyslexics] vs. 1.28 s [controls]), and then parted increasingly dependent on
word length. As this was achieved by an increasing number of saccades, this may
mean that having to combine information from two or more holding phases
constituted an additional level of difficulty for the dyslexics.
Saccade strategy and frequency
The almost identical F-saccade/word ratios for short
words in both groups correlated well with the fact that the recognition times
for these words were quite similar for both groups. On the other hand, a
dependence on word length could be expected (Tinker, 1958), and the much higher ratios in the
dyslexics for medium and long words agree with the fact that the recognition
times for longer words were significantly longer in the dyslexics.
The high coefficient of determination
( r2) of the number of
F-saccades versus word-length functions for 8 out of 10 dyslexic subjects
confirms that the oculomotor strategy chosen for long words has a strong
influence on reading text. Any opinion about why the two children with the
smallest F-saccade/word ratios had so strongly divergent reading performance
can, at this time, only be speculative. It is of interest, though, to note that
the subject with the lowest ratio showed, clearer than any other subject, the
tendency to perform reverse reading eye movements, as described by Zangwil and
Blakemore ( 1972).
The fact that there was a significant difference
between the groups in regard to the rate of occurrence of saccades was a
consequence of the significantly longer holding durations. The fact that the
absolute number of saccades performed by the dyslexics to solve the same task
was much higher was caused by the longer time they spent to read each word with
many shorter saccades. However, the relative proportion of their median number
of forward saccades to the median number of backward saccades was only
insignificantly higher than that for the control group
(68.9 % vs.
64.4 %, respectively). In addition, the
constituent individual values showed a wide range of inter-individual variation,
both of which agree with Olson, Conners, and Rack ( 1991), who found no substantial difference in
this regard between groups, albeit matched by reading-level.
Forward saccade amplitudes
The adaptation of F-saccade amplitude to word length in
dyslexics is a new finding that constitutes the most important result of this
study: The function turned out to be approximately linear for the control group,
which confirms and adds much detail to the original finding by O’Regan ( 1980) in normal adults. The same function in
the dyslexics saturates at an amplitude of approximately 1 deg (2 n-spaces, see
Figure 4), which, nonetheless, shows that a
mechanism for adapting the gain of reactive, stimulus-triggered saccades
(Deubel, 1995) is active during reading in
dyslexics also, but that it is quantitatively less developed. It might have an
important practical consequence, because it opens the possibility to develop
perceptual or attentional training methods to increase the gain of this function
goal directedly, from which dyslexic children could benefit (Beard, Levi, &
Reich, 1995;
Chung, Legge, & Cheung, 2004;
Fahle, & Henke-Fahle, 1996; Fahle
& Luberichs, 1995; Geiger, Lettvin,
& Fahle, 1994).
Tentatively, the adjustment of F-saccade amplitude to
word length may reflect a reading strategy based on the density of information
in short words, which can be much higher than in a long word: Note the
differences between words like "then,” "them," "thin," and "than,"
analogous to "über," "üben," "oben," and "eben" in German. This makes
reading short words in small saccadic steps more advisable for those who stress
accuracy over speed, such as the children in our test situation, especially the
dyslexics. In contrast, longer words permit higher reliance on recognition of
entire suffixes or prefixes such as "-ous," "-ward," "con-," and "sub-,"
analogous to "-keit," "-lich," "ent-," and "ver-" in German. As our use of
single words ruled out grammatical and contextual inferences, our results
highlight the importance of word length for gauging reading eye movements
particularly.
According to McConkie and Rayner ( 1976), the perceptual span is a behavioral
measure based on the number of letters in a gaze-contingent display and the
resulting reading speed. In normal, skilled readers, it can extend up to 15
letters to the right of the fovea. Two factors are likely to play a role in
limiting F-saccade amplitudes in our subjects: (1) reading skills due to lower
age, and (2) the fact that our subjects did not read continuous text. It is
noteworthy, though, that the largest F-saccade amplitudes in the dyslexics were
approximately half as large as the ones in the control group (see Figure 4). We tentatively interpret the shorter
F-saccades as an indication of a more timid gaze strategy, which in the paradigm
used by McConkie and Rayner would have shown as a narrower perceptual span.
Consequently, it is likely that the number of letters processed in any one
holding phase in the dyslexics is smaller. As our dyslexics had times to
recognition for short words (2–4 letters) quite comparable to those in the
controls, it is not likely that this might be caused by an increased
“foveal processing difficulty” (Henderson & Ferreira, 1990). Furthermore, the relative
statistical distribution of saccade amplitudes was found to be approximately the
same as that reported for skilled readers (Morris & Rayner, 1991).
The lack of a relationship of the F-saccade
amplitude/word length functions with text reading speed must be considered on
the basis of the fact that they were derived from different paradigms: text
reading versus single-word reading. Continuous reading of text presumably
requires more skills dealing with the relationships between words, an element
that is missing in single-word reading. We hypothesize that the mechanisms of
between-the-words control might be more important in determining text reading
speed than those of within-one-word control.
The fact that these functions also did not show any
dependence on age correlated well with the fact that none was seen in this group
for text reading speed either. It is conceivable that this could have been
caused by the limited cohort investigated
here.
The fact that
we found the final landing points of saccades not at the end of words but rather
some distance before can again be interpreted as a manifestation of the
rightward extent of the perceptual span that made further progression simply not
necessary due to parafoveal processing (McConkie & Rayner, 1976; Rayner, Well, Pollatsek, &
Bertera, 1982)
The same can be said about the distances to the word
beginning in the right-aligned words, where the leftward extent of the
perceptual span could be used. Together with the findings regarding the
F-saccade amplitudes (see above), these data further support the hypothesis that
the dyslexics investigated here had a significantly narrower perceptual span
than the children in the control group. Note that a similar result was also
reported by Rayner ( 1986) in children who
are learning to read, from which he concluded that this “...indicated that
the size of the perceptual span is variable and can be influenced by the
difficulty of the
text.” Durations of holding phases
It has been shown that there are considerable
variations in the durations of inter-saccadic intervals during reading as well
as other visual tasks in normally reading adults (Hooge & Erkelens, 1996; Jacobs, 1986; Osaka, 1992; Rayner & McConkie, 1976) as well as in normally reading children
(McConkie et al., 1991). The results
from our control group are in good agreement with these findings. O'Regan ( 1980) reported a negative dependence of
duration of holding phases on word length in normal readers. That we could
confirm O'Regan's finding only in a majority of our control group (10/12) does
not diminish the fact that the group median still showed a moderate negative
dependence.
The significantly longer median durations of the
holding phases in dyslexics confirms earlier findings by Adler-Grinberg and
Stark ( 1978) and conflicts with
Rubino and Minden ( 1973). It is noteworthy
that individual medians within the groups showed almost the same ranges (53 ms
[dyslexics] vs. 55 ms [controls]), but an overlap of values in only five
subjects (see Figure 6). Although the longer
group median in the dyslexics contributes to their reading impairment (Olson et
al., 1991; Rayner et al., 1996), it does not allow the conclusion that
it causes the impairment. This is supported by our finding that the individual
holding duration medians showed no significant correlation with the subject's
reading speed in the dyslexics. The longer holding phases more likely reflect
prolonged attentional dwell times demonstrated in dyslexics by Hari et al. ( 1999).
The higher variability of individual holding durations
found in the dyslexics is based on the fact that the shortest values showed only
small differences between the groups, whereas the longest durations were 200-ms
longer in the dyslexics. In addition, only 3 values from the control group
exceeded 500 ms, but 46 did in the dyslexics (i.e.,
0.08% vs.
7%). Forward saccade amplitude correlations with durations of holding phases
Models of reading impairments stress differences between a phonemic/linguistic and a visual/oculomotor component of the reading process (see Stark et al., 1991). With respect to the sensory input, it
could be argued based on work by Salthouse and Ellis ( 1980) that the holding duration may depend
on the amplitude of the preceding saccade. In the case of reading, a longer
F-saccade amplitude might cause a longer duration of the following holding
phase, because more letters take a longer time to process. The fact that we
found only loose and inconsistent correlations between amplitudes and subsequent
holding durations allows rejecting this hypothesis for reading. This also
confirms the findings of Rayner and McConkie in normal readers ( 1976), although they found a smaller range of
variation. We conclude that in the dyslexics, the phonemic/linguistic factors
must have the stronger influence on either variable.
Our findings agree with those reported by Rayner et al.
( 1996), who used the durations of the
holding phases in normal readers as an indicator for which component tells the
eyes to move on. Their findings support the view that this decision is primarily
influenced by "on-line language processing" rather than by visual or oculomotor
factors.
Further support of this finding in dyslexics comes from
a previous study investigating the relationship of text reading with
pictogram-naming performance in dyslexics. We found that both, a
phonemic/linguistic and a visual/eidetic deficit, can contribute to the
phenomenology of an individual's dyslexia. While the deficit in the
phonemic/linguistic component may be common to all dyslexics, which may be the
main reason for their poor text reading, the visual/eidetic component was
compromised only in some dyslexic subjects (Trauzettel-Klosinski et al., 2002). Thus, the latter turned out to be poor
pictogram namers, whereas the others performed as well in this task as the
normally reading children.
Regarding the correlation of holding duration with word
length, O'Regan ( 1980) found large
differences between adult normal readers, which was in conflict with findings by
Rayner and McConkie ( 1976). We found such
differences also between our young normal readers, but particularly between the
dyslexics. This makes it likely that a negative correlation – the longer
the word, the shorter the holding duration – may be an acquired skill that
promotes reading speed and fluency (see also the discussion of forward saccade
amplitudes, above). We found it in most of our control group (10/12) and in 6/10
of the dyslexics. The others may still need more practice to recognize
frequently occurring syllables in long words and, thus, show a positive
correlation. The fact that the dependence of this correlation on age was weak
could be due to the small group size. Nonetheless, the dyslexic child with the
highest positive correlation
coefficient ( rho = 0.595), whose eye
rested the longest on long words, was the second oldest of the group, the
slowest text reader and had the longest times to word recognition. On the other
hand, the two dyslexics with the strongest negative correlation
( rho = –0.72 and
rho = –0.48) had the shortest
holding durations, and were numbers 1 and 3 in text reading speed.
Our results also fit the larger conceptual framework of
saccades performed in other visual tasks, where past experience as well as
prediction can play a role. For instance, Hooge and Erkelens ( 1996) found in a search task that "control of
fixation duration appears to be indirect" (i.e., not exclusively dependent on
the currently fixated target). In a later study, they reported that fixation
durations are not commensurate with the current task at hand, but are controlled
by a mechanism that uses estimations of the foveal analysis time of
previous fixated stimulus elements
(Hooge & Erkelens, 1998; we added the
italics). Corroborating evidence for endogenous eye-movement control was also
presented by Andrews and Coppola ( 1999),
who found "idiosyncratic characteristics" in saccadic eye movements that could
not be explained otherwise. Moreover, the current results can be linked to
reports of low-level deficits in the magnocellular stream of visual neurons in
dyslexics (Borsting et al., 1996; Demb
et al., 1998a, 1998b; Stein & Walsh, 1997; Steinman et al., 1998), which can affect the control of
attention (Fischer, 1987; Heinze &
Mangun, 1995; Kowler et al., 1995; MacKeben & Nakayama, 1993) via a frontoparietal network
(Corbetta, 1998). This might then affect
preprogramming of reading saccades (Morrison, 1984) as well as control of the sequential
flow of attention during reading, which has been shown to be an important
component in modeling reading eye movements (Henderson & Ferreira, 1993; Vidyasagar, 1999; Radach, Inhoff, & Heller, 2002).
Our results show that the mechanism allowing normal
readers to adjust forward saccade amplitudes to word length is present in
dyslexics, but that it is amplitude-limited during reading of words of
five-letter length and longer. Thus, the dyslexic cannot fully take advantage of
this adjustment that promotes reading speed. A tentative interpretation of this
finding could be that the rightward extent of the perceptual span used for
reading longer words is limited in dyslexics. These data allow no conclusion
whether this reflects a saccade control problem possibly caused by a
magnocellular deficit, or whether longer words simply pose a higher degree of
decoding difficulty. We also found that the increased number of saccades in
either direction made by the dyslexics during reading reflect only the longer
time they have to spend deciphering words, but not a higher absolute rate of
occurrence of saccades per unit time. Furthermore, in some dyslexics,
single-word reading speed is reduced by longer durations of the holding phases
between saccades, which could reflect the need for longer processing time of
individual syllables or a speed deficit in finding their phonological
equivalents. Three parameters measured here reflected the difficulties the
dyslexics encountered while reading single words: The longer durations of
holding phases, the slower progression through shorter forward saccades, and the
tendency in some to start the reading process over again after failing to read a
word correctly. We hypothesize that these deficits during single-word reading
likely also contribute to the reduced text reading speed in dyslexics.
The authors wish to thank Björn Krämer for
his help with the analysis of the SLO videotapes and two anonymous reviewers for
many helpful comments. Commercial
relationships: none.
Corresponding author: Manfred MacKeben.
Email: mm@ski.org.
Address: The Smith-Kettlewell Eye Research Institute, San Francisco, California, USA.
Adler-Grinberg, D.,
& Stark, L. (1978). Eye movements, scanpaths and dyslexia.
American Journal of Optics and Physiological
Optics, 55, 557-570. [ PubMed]
Andrews, T. J., &
Coppola, D. M. (1999). Idiosyncratic characteristics of saccadic eye movements
when viewing different visual environments.
Vision Research 39, 2947-2953. [ PubMed]
Beard, B., Levi, D. M., &
Reich, L. N. (1995). Perceptual learning in parafoveal vision.
Vision Research 35, 1679-1690. [ PubMed]
Best, M., & Demb, J. B.
(1999). Normal planum temporale asymmetry in dyslexics with a magnocellular
pathway deficit. Neuroreport 10,
607-612. [ PubMed]
Biscaldi, M., Fischer, B.,
& Aiple F. (1994). Saccadic eye movements of dyslexic and normal reading
children. Perception & Psychophysics 23,
45-64. [ PubMed]
Biscaldi, M., Fischer, B.,
& Hartnegg, K. (2000). Voluntary saccadic control in dyslexia.
Perception & Psychophysics, 29,
509-521. [ PubMed]
Black, J. L., Collins, D. W.,
De Roach, J. N., & Zubrick, S. R. (1984). Dyslexia: Saccadic eye movements.
Perception & Motor Skills, 58,
903-910. [ PubMed]
Boder, E. (1973). Development
dyslexia: A diagnostic approach based on three atypical reading-spelling
patterns. Developmental Medicine & Child
Neurology 15, 663-687. [ PubMed]
Borsting, E., Ridder III,
W. H., Dudeck, K., Kelly, C., Matsui, L. & Motoyama, J. (1996). The presence
of a magnocellular defect depends on the type of dyslexia.
Vision Research 36, 1047-1053. [ PubMed]
Bouma, H. (1973). Visual
interference in the parafoveal recognition of initial and final letters of
words. Vision Research, 13,
767-782. [ PubMed]
Bouma, H., & de Voogd, A.
H. (1974). On the control of eye saccades in reading.
Vision Research, 14, 273-284.
Bradley, L., & Bryant,
P. E. (1983). Categorizing sounds and learning to read: A causal connection.
Nature, 301, 419-421.
Brown, B.,
Haegerstrom-Portnoy, G., Adams, A. J., Yingling, C. D., Galin, D., Herron, J.,
& Marcus, M. (1983). Predictive eye movements do not discriminate between
dyslexic and control children.
Neuropsychologia, 21, 121-128. [ PubMed]
Brickenkamp, R.(1981).
Aufmerksamkeit-Belastungs-Test d2 (The d2 test - A timed test of selective
attention). Göttingen: Hogrefe.
Ciuffreda, K. J., Bahill,
A. T., Kenyon, R. V., & Stark, L. (1976). Eye movements during reading: case
reports. American Journal Optometry &
Physiological Optics, 53, 389-395. [ PubMed]
Chung,
S. T., Legge, G. E., & Cheung, S. (2004). Letter-recognition and reading
speed in peripheral vision benefit from perceptual learning.
Vision Research, 44, 695-709. [ PubMed]
Corbetta, M. (1998).
Frontoparietal cortical networks for directing attention and the eye to visual
locations: Identical, independent, or overlapping neural systems?
Proceedings of the National Academy of
Sciences, U.S.A., 95, 831-838. [ PubMed] [ Article]
Cunitz, R. J., &
Steinman, R. M. (1969). Comparison of saccadic eye movements during fixation and
reading. Vision Research 9, 683-693.
[ PubMed]
De Luca, M., Di Pace, E.,
Judica, A., Spinelli, D., & Zoccolotti, P. (1999). Eye movement patterns in
linguistic and non-linguistic tasks in developmental surface dyslexia.
Neuropsychologia. 37, 1407-1420. [ PubMed]
De Luca, M., Borrelli, M.,
Judica, A., Spinelli, D., & Zoccolotti, P. (2002). Reading words and
pseudowords: An eye movement study of developmental dyslexia.
Brain & Language, 80, 617-626. [ PubMed]
Demb, J. B., Boynton, G. M.,
Best, M., & Heeger, D. J. (1998a). Psychophysical evidence for a
magnocellular pathway deficit in dyslexia.
Vision Research 38, 1555-1559. [ PubMed]
Demb, J. B., Boynton, G. M.,
& Heeger, D. J. (1998b). Functional magnetic resonance imaging of early
visual pathways in dyslexia. Journal of
Neuroscience, 18, 6939-6951. [ PubMed] [ Article]
Deubel, H. (1995). Separate
adaptive mechanisms for the control of reactive and volitional saccadic eye
movements. Vision Research, 35,
3529-3540. [ PubMed]
Diagnostischer
Rechtschreibtest (Diagnostic Orthography Test) #1, 6, 7, 8 (1980). Weinheim:
Beltz.
Di Lollo, V., Hanson, D.,
& McIntyre, J. S. (1983). Initial stages of visual information processing in
dyslexia. Journal Experimental Psychology,
Human Perception & Performance, 9, 923-935. [ PubMed]
Eden, G. F., Stein, J. F.,
Wood, H. M., & Wood, F. B. (1994). Differences in eye movements and reading
problems in dyslexic and normal children.
Vision Research 34, 1345-1358. [ PubMed]
Fahle, M., & Luberichs, J.
(1995). Extension of a recent therapy for dyslexia.
German Journal of Ophthalmology 4,
350-354. [ PubMed]
Fahle, M., & Henke-Fahle,
S. (1996). Interobserver variance in perceptual performance and learning.
Investigative Ophthalmology & Visual
Science, 37, 869-877. [ PubMed]
Fischer, B. (1987). The
preparation of visually guided saccades.
Review of Physiology & Biochemical
Pharmacology, 105, 1–35. [ PubMed]
Geiger, G., & Lettvin, J.
Y. (1987). Peripheral vision in persons with dyslexia.
New England Journal of Medicine, 316,
1238-1243. [ PubMed]
Geiger, G., Lettvin, J. Y.,
& Fahle, M. (1994). Dyslexic children learn a new visual strategy for
reading: A controlled experiment. Vision
Research, 34, 1223-1233. [ PubMed]
Golden, M., & Zenhausern,
R. (1983). Grapheme to phoneme conversion: The basis of reading disability?
International Journal of Neuroscience,
20, 229-239. [ PubMed]
Goswami, U., Gambert, J. E.,
& de Barrera, L. F. (1998). Children’s orthographic representations
and linguistic transparency: Nonsense word reading in English, French and
Spanish. Applied Psycholinguistics, 19,
19-52.
Hari, R., Valta, M., &
Uutela, K. (1999). Prolonged attentional dwell time in dyslexic adults.
Neuroscience Letters, 271, 202-204. [ PubMed]
Heinze, H. J., & Mangun, G. R. (1995). Electrophysiologi-cal signs of sustained and transient attention to spatial locations. Neuropsychologia, 33, 889-908. [ PubMed]
Henderson, J. M., &
Ferreira, F. (1990). Effects of foveal processing difficulty on the perceptual
span in reading: Implications for attention and eye movement control.
Journal of Experimental Psychology, Learning,
Memory & Cognition, 16, 417-429. [ PubMed]
Henderson, J. M., &
Ferreira, F. (1993). Eye movement control during reading: Fixation measures
reflect foveal but not parafoveal processing difficulty.
Canadian Journal of Experimental Psychology
47, 201-221. [ PubMed]
Hooge, I. T., & Erkelens,
C. J. (1996). Control of fixation duration in a simple search task.
Perception & Psychophysics 58,
969-976. [ PubMed]
Hooge, I. T., & Erkelens,
C. J. (1998). Adjustment of fixation duration in visual search.
Vision Research, 38, 1295-1302. [ PubMed]
Inhoff, A. W., & Rayner,
K. (1986). Parafoveal word processing during eye fixations in reading: Effects
of word frequency. Perception &
Psychophysics, 40, 431-439. [ PubMed]
Jacobs, A. M. (1986).
Eye-movement control in visual search: How direct is visual span control?
Perception & Psychophysics, 39,
47-58. [ PubMed]
Kowler, E., Anderson, E.,
Dosher, B., & Blaser, E. (1995). The role of attention in the programming of
saccades. Vision Research 35,
1897-1916. [ PubMed]
Legge, G. E., Pelli, D. G.,
Rubin, G. S., & Schleske, M. M. (1985). Psychophysics of reading.I. Normal
vision. Vision Research, 25, 239-252.
[ PubMed]
Legge, G. E., Ahn, S. J.,
Klitz, T. S., & Luebker, A. (1997). Psychophysics of reading. XVI. The
visual span in normal and low vision. Vision
Research, 37, 1999-2010. [ PubMed]
Lennerstrand, G., &
Ygge, J. (1992). Dyslexia; Ophthalmological aspects 1991.
Acta Ophthalmologica
(Copenhagen) , 70, 3-13. [ PubMed]
Linder, M., & Grissemann,
H. (1980). Zürcher Lesetest (The Zürich Reading Test). Bern: Huber.
MacKeben, M., &
Nakayama, K. (1993). Express attentional shifts.
Vision Research, 33, 85-90. [ PubMed]
Mansfield, S. J., &
Legge, G. E. (1999). From letters to words: The role of lexical inference [Abstract].
Investigative Ophthalmology & Visual
Science (Suppl.), 40, 186.
McConkie, G. W., &
Rayner, K. (1975). The span of the effective stimulus during a fixation in
reading. Perception & Psychophysics,
17, 578-586.
McConkie, G. W., &
Rayner, K. (1976). Asymmetry of the perceptual span in reading.
Bulletin of the Psychonomic Society, 8,
365-368.
McConkie, G. W., Zola, D.,
Grimes, J., Kerr, P. W., Bryant, N. R., & Wolff, P. M. (1991). Children's
eye movements during reading. In J. F. Stein (Ed.),
Vision and visual dyslexia (pp.
251-262). Boston: CRC Press.
Morris, R. K., & Rayner,
K. (1991). Eye movements in skilled reading: Implications for developmental
dyslexia. In J. F. Stein (Ed.), Vision and
visual dyslexia (pp. 233-242). Boston: CRC Press.
Morrison, R. E. (1984).
Manipulation of stimulus onset delay in reading: Evidence for parallel
programming of saccades. Journal of
Experimental Psychology, Human Perception & Performance, 10, 667-682.
[ PubMed]
Njiokiktjien, C.
(1994). Dyslexia: A neuroscientific puzzle.
Acta Paedopsychiatrica, 56, 157-167.
[ PubMed]
Olson, R. K., Conners, F. A.,
& Rack, J. P. (1991). Eye movements in dyslexic and normal readers. In J. F.
Stein (Ed.), Vision and visual dyslexia
(pp. 243-250). Boston: CRC Press.
O'Regan, K. (1979). Saccade
size control in reading: Evidence for the linguistic control hypothesis.
Perception & Psychophysics, 25,
501-509. [ PubMed]
O'Regan, K. (1980). The
control of saccade size and fixation duration in reading: The limits of
linguistic control. Perception &
Psychophysics, 28, 112-117.
Osaka, N. (1992). Size of
saccade and fixation duration of eye movements during reading: Psychophysics of
Japanese text processing. Journal of the
Optical Society of America A, 9, 5-13. [ PubMed]
Pavlidis, G. T. (1991).
Diagnostic significance and relationship between dyslexia and erratic eye
movements. In J. F. Stein (Ed.), Vision and
visual dyslexia (pp. 263-270). Boston: CRC Press.
Pugh, K. R., Mencl, W. E.,
Jenner, A. R., Katz, L., Frost, S. J., Lee, J. R., et al. (2000). Functional
neuroimaging studies of reading and reading disability (developmental dyslexia).
Mental Retardation and Developmental
Disability Research Review, 6, 207-213. [ PubMed]
Radach, R., Inhoff, A., &
Heller, D. (2002). The role of attention in fluent reading. In E. Witruk, A.
Federici, & T. Lachman (Eds.), Basic
mechanisms of language, reading and reading disability. Dordrecht:
Kluver.
Raven, J. C., Court, J., &
Raven, J. (1980). Colored progressive
matrices. Weinheim: Beltz.
Rayner, K. (1983). The
perceptual span and eye movement control during reading. In K. Rayner (Ed.),
Eye movements in reading (pp. 97-120).
New York: Academic Press.
Rayner, K. (1986). Eye
movements and the perceptual span in beginning and skilled readers.
Journal of Experimental Child Psychology, 41,
211-236. [ PubMed]
Rayner, K., & McConkie,
G. W. (1976). What guides a reader's eye movements?
Vision Research, 16, 829-837. [ PubMed]
Rayner, K., & Pollatsek,
A. (1981). Eye movement control during reading: Evidence for direct control.
Quarterly Journal of Experimental Psychology,
33A, 351-373. [ PubMed]
Rayner, K., Well, A. D.,
Pollatsek, A., & Bertera, J. H. (1982). The availability of useful
information to the right of fixation in reading.
Perception & Psychophysics, 31,
537-550. [ PubMed]
Rayner, K., Sereno, S. C.,
& Raney, G. E. (1996). Eye movement control in reading: A comparison of two
types of models. Journal of Experimental
Psychology, Human Perception and Performance, 22, 1188-1200. [ PubMed]
Rubino, C. A., & Minden,
H. A. (1973). An analysis of eye-movements in children with a reading
disability. Cortex, 9, 217-220. [ PubMed]
Rudel, R. G., Denckla, M. B.,
& Broman, M. (1978). Rapid silent response to repeated target symbols by
dyslexic and nondyslexic children. Brain &
Language, 6, 52-62. [ PubMed]
Salmelin, R., Helenius, P.,
& Service, E. (2000). Neurophysiology of fluent and impaired reading: A
magnetoencephalographic approach. Journal of
Clinical Neurophysiology, 17, 163-174. [ PubMed]
Salthouse, T. A., &
Ellis, C. L. (1980). Determinants of eye-fixation duration.
American Journal of Psychology, 93,
207-234. [ PubMed]
Schroyens, W., Vitu, F.,
Brysbaert, M., & d'Ydewalle, G. (1999). Eye movement control during
reading: Foveal load and parafoveal processing.
Quarterly Journal Experimental Psychology A,
52, 1021-1046. [ PubMed]
Simos, P. G., Breier, J. I.,
Fletcher, J. M., Foorman, B. R., Bergman, E., Fishbeck, K., & Papanicolaou,
A. C. (2000). Brain activation profiles in dyslexic children during non-word
reading: A magnetic source imaging study.
Neuroscience Letters, 290, 61-65. [ PubMed]
Snowling, M. J. (1980). The
development of grapheme-phoneme correspondence in normal and dyslexic readers.
Journal of Experimental Child Psychology 29,
294-305. [ PubMed]
Stanley, G., Smith, G. A.,
& Howell, E. A. (1983). Eye movements and sequential tracking in dyslexic
and control children. British Journal of
Psychology, 74, 181-187. [ PubMed]
Stark, L. W., Giveen, S. C.,
& Terdiman, J. F. (1991). Specific dyslexia and eye movements. In J. F.
Stein (Ed.), Vision and visual dyslexia
(pp. 203-232). Boston: CRC Press.
Stein, J., & Walsh, V.
(1997). To see but not to read: The magnocellular theory of dyslexia.
Trends in Neuroscience, 20, 147-152.
[ PubMed]
Steinman, B. A., Steinman,
S. B., & Garzia, R. P. (1998). Vision and attention. II. Is visual attention
a mechanism through which a deficient magnocellular pathway might cause reading
disability? Optometry & Vision Science,
75, 674-681. [ PubMed]
Swan, D., & Goswami, U.
(1997). Phonological awareness deficits in developmental dyslexia and the
phonological representations hypothesis.
Journal of Experimental Child Psychology, 66,
18-41. [ PubMed]
Taylor, E. A. (1957). The
spans: Perception, apprehension and recognition.
American Journal of Ophthalmology, 44,
501-507. [ PubMed]
Tewes, U. Wechsler
Intelligence Scale for Children - Revised German version (1983)(Hamburg-Wechsler
Intelligenztest für Kinder). Bern: Huber.
Tinker, M. A. (1958). Recent
studies of eye movements in reading.
Psychological Bulletin, 55, 215-231.
[ PubMed]
Trauzettel-Klosinski, S.,
Klosinski, G., Sadowski, B., & Tornow, R. P. (1997). Reading strategies in
dyslexia - assessed by SLO: First research results [Abstract].
Investigative Ophthalmology & Visual
Science (Suppl.) , 38, 551.
Trauzettel-Klosinski, S.,
& Reinhard, J. (1998). The vertical field border in hemianopia and its
significance for fixation and reading.
Investigative Ophthalmology & Visual
Science, 39, 2177-2186. [ PubMed]
Trauzettel-Klosinski, S.,
Reinhard, J., Klosinski, G., & MacKeben, M. (1999). Reading of texts and
pictograms in dyslexic and normal children - assessed by SLO [Abstract].
Investigative Ophthalmology & Visual
Science (Suppl.), 40, 319.
Trauzettel-Klosinski, S.,
MacKeben, M., Reinhard, J., Feucht, A., Dürrwächter, U., &
Klosinski, G. (2002). Pictogram naming in dyslexic and normal children assessed
by SLO. Vision Research, 42, 789-799.
[ PubMed]
Van Strien, J. W., Bouma,
A., & Bakker, J. (1993). Lexical decision performances in P-type dyslexic,
L-type dyslexic, and normal reading boys. Journal of
Clinical & Experimental Neuropsychology,
15, 516-524. [ PubMed]
Vidyasagar, T. R. (1999).
A neuronal model of attentional spotlight: Parietal guiding the temporal.
Brain Research & Brain Research Reviews,
30, 66-76. [ PubMed]
Whittaker, S. G., &
Lovie-Kitchin, J. (1993). Visual requirements for reading.
Optometry & Vision Science, 70,
54-65. [ PubMed]
Wimmer, H. (1996). The
nonword reading deficit in developmental dyslexia: Evidence from children
learning to read German. Journal Experimental
Child Psychology, 61, 80-90. [ PubMed]
Wimmer, H., & Goswami, U.
(1994). The influence of orthographic consistency on reading development: Word
recognition in English and German children.
Cognition, 51, 91-103. [ PubMed]
Wolf, M., & Bowers, P. G.
(1999). The double-deficit hypothesis for the developmental dyslexias.
Journal of Educational Psychology, 91,
415-438.
World Health Organization
(1996). The ICD10 Classification of Mental and
Behavioural Disorders: Clinical descriptions and diagnostic guidelines.
Bern: Huber.
Zangwil, O. L., &
Blakemore, C. (1972). Dyslexia: Reversal of eye movements during reading.
Neuropsychologia, 10, 371-373.
|
|