Abstract
purpose. The visual processing of text occurs spontaneously in most
readers. Dyslexic persons, however, often report both somatic symptoms
and perceptual distortions when trying to read. It is possible that the
perceptual distortions experienced by those with dyslexia reflect a
disturbance in the basic mechanisms supporting perceptual organization
at the early stages of visual processing. Integration of information
over extended areas of visual space can be measured psychophysically in
a task that requires the detection of a path defined by aligned,
spatially narrow-band elements on a dense field of otherwise similar
elements that are randomly oriented and positioned. In the present
study a contour integration task was used to investigate such
perceptual organization in dyslexia.
methods. The detection of contours or paths composed of Gabor micropatterns was
performed within a field of randomly oriented distracter elements in a
2-alternate forced choice (AFC) task. The stimuli were
manipulated by randomly varying both the density of the background
noise elements and the number of elements that defined a path of
constant length.
results. In all observers, sensitivity to the paths increased with the number of
target elements comprising the path, and subjects in both groups
exhibited similar trends in relative density of the stimuli. However,
in all conditions, dyslexic observers were two to three times less
sensitive to path stimuli than the control group.
conclusions. In the present study the authors have described a visual deficit in a
global integration task in dyslexia. The pattern of deficits reported
suggest that abnormal cooperative associations may be present in
dyslexia that are indicative of poor perceptual
integration.
The specific reading difficulty of dyslexia affects 3% to
10% of the population.
1 2 There are many theories
concerning the origin of dyslexia, and it is likely that the condition
is itself heterogeneous. Although most of the literature supports an
underlying deficit in phonologic processing,
3 4 it is now
widely accepted that low-level visual processing abnormalities are also
present,
5 6 showing a selective loss in sensitivity at
low spatial and high temporal frequencies in anatomic,
7 psychophysical,
5 8 electrophysical,
7 and
brain-imaging studies.
9
Dyslexic persons often report both somatic symptoms (asthenopia,
headaches) and perceptual distortions (small letters and words appear
distorted, move, and are blurred) when trying to read.
6 10 Recent evidence suggests that the global characteristics of text can
produce such symptoms and subsequent difficulties in
reading.
11 12 Reading can be described as a hierarchical
object process, in that letters are grouped into words and words into
lines. The interference of the global percept of a page may cause
disruption to the more salient local analysis at a word–line level in
dyslexia.
It has been well established through physiological
13 and
behavioral
14 studies that the receptive fields of early
visual detection mechanisms are small and highly selective for a
limited range of stimulus attributes, such as spatial frequency and
orientation. This means that information about the fine spatial
structure of letters and words and thereafter the global organization
of text may be based on the combined integrative responses of a number
of independent, local inputs across the visual field. It is possible
that the perceptual distortions experienced by dyslexic persons reflect
a disturbance in the basic mechanisms supporting such perceptual
organization at the early stages of visual processing.
Increasing evidence in cortical neurobiology further suggests that
neurons with disparate receptive fields in primate primary visual
cortex (V1) are linked by long-range connections, depending on the
orientation preferences of cells,
15 16 17 18 19 that may serve to
integrate distributed neuronal activity. The efficiency of such visual
connections that integrate local feature codes into global object
properties across visual space can be measured psychophysically in a
task that requires the detection of a path defined by narrow-band
elements aligned spatially on a dense field of otherwise similar
elements that are randomly oriented and positioned.
20 The
process of this integration has been extensively explored in recent
years through psychophysical studies
15 16 20 21 that have
revealed that the detection of such stimuli is supported by
well-defined interconnections among neighboring detectors, along the
orientation axes of nonoverlapping filters
(Fig. 1) .
In general, sensitivity to contours increases with the length and
straightness of the path,
20 21 22 23 although closure of highly
curved paths can increase sensitivity through the circular structure of
such stimuli.
24 Sensitivity also increases with exposure
duration
25 and with the similarity in the
phase
26 27 28 or spatial frequency of the elements defining
the path.
16 26 Contours can also be integrated within and
across depth with similar factors determining
sensitivity.
29 30 Recent studies have also demonstrated
that such perceptual organization is not fully developed in young
children.
21 This late maturation process has consequently
been shown to be susceptible to the effects of abnormal visual
development in the form of amblyopia.
31 32
In the present investigation, to assess perceptual organization in
dyslexia, we compared the ability to integrate spatial information
across the visual field in the form of a contour or path detection
paradigm.
Ten subjects (mean ± SD age, 22.3 ± 5.5 years) were
recruited for the study who reported a prior diagnosis of dyslexia by
either a psychologist or neurologist. These subjects had a reading age
(variables considered were speed and accuracy) more than one SD behind
that expected from their performance intelligence quotient (IQ). No
subjects reported an attention disorder.
A carefully age- and sex-matched control group (mean age, 24.8 ±
8.5 years) of volunteers were selected who had no reported history of
reading difficulty, visual stress, or any difficulties with near
vision. Both groups had normal visual acuity and binocular vision and
were practiced in contour detection tasks before formal data
collection.
All experimental procedures followed the tenets of the Declaration of
Helsinki, and informed consent was obtained after the nature and
possible consequences of the experiment had been explained.
Stimuli were composed of multiple Gabor elements pseudorandomly
positioned in a 6.6° × 6.6° region. The display was divided into
either an 8 × 8 (64 Gabor elements), 10 × 10 (100 Gabor
elements), or 14 × 14 grids (196 Gabor elements) of equal-sized
cells
(Fig. 2) . Each cell contained a Gabor element that was the product of a
circular gaussian envelope and an oriented sinusoid:
\[G(x,\ y){=}\mathrm{e}^{{-}(x^{2}{+}y^{2}){/}2{\sigma}^{2}}\ {_\ast}\ \mathrm{cos\ }{[}2{\pi}\ {_\ast}\ (\mathrm{cos\ }{\theta}\ {_\ast}\ x{+}\mathrm{sin\ {\theta}}\ {_\ast}\ y){/}{\rho}{+}{\phi}{]}\]
where θ controls orientation and φ the phase of the
sinusoid. The spatial frequency of the elements was 6 cyc/deg and the
SD of the gaussian envelope was 0.1°.
Each trial consisted of a 1-second interval, in which two images with
the same element density
(Fig. 2) were presented simultaneously at
either side of a central fixation cross. One image contained a path,
the other only randomly oriented elements. The observers’ task was to
identify which of the images contained the path. Auditory feedback was
provided after incorrect responses.
The path was a set of either four, five, or six oriented Gabor elements
aligned along a contour that was embedded in a background of similar
but randomly oriented Gabor elements. The elements defining the path
were separated by either an 0.83° (four-element path), a 0.66°
(five-element path), or a 0.54° (six-element path) gap. The starting
phase of the first element was randomly selected (between 0° and
360°). The phase of successive elements along the path were then kept
in phase with the first element.
The complete contour or path was randomly positioned in the display.
The remaining cells (number of elements in the background minus the
number of elements comprising the path) were then occupied by
distracter elements of random orientation and with random starting
phase. The mean separation of the random background elements, including
diagonals was an 0.83° (64-element density), a 0.66° (100-element
density), or a 0.54° (196-element density) gap, plus a randomization
of ±10% to eliminate periodic cues to the presence of the path. The
distracter elements were randomly positioned within these unoccupied
cells, with the constraint that each cell contained the center of only
one Gabor, to eliminate clumping of elements. Overlapping elements
summed. In the random pattern, all cells contained a randomly
positioned element of random orientation and with random starting
phase.
The stimuli were manipulated by randomly varying both the density of
the background noise elements (64, 100, or 196 Gabor elements) and the
number of elements (four, five, or six Gabor elements) that defined a
path of a constant length of 3.3° of visual angle.
A psychophysical procedure
27 was adapted to measure
sensitivity to different paths. Sensitivity to a path is greatest when
the elements are aligned to the contour, and it decreases as the
orientation between adjacent path elements increases.
21 Sensitivity was therefore measured as the amount of local orientation
jitter that produced 75% correct performance in the detection task.
Each path element was aligned to the contour plus a random orientation
jitter selected from a uniform distribution, the range of which was
under the control of a QUEST (quality, utilization, effectiveness,
statistically tabulated) staircase procedure
35 from−θ
j to +θ
j (Fig. 3) . The staircase increased the range when observers correctly identified
the interval containing the path, and decreased the range when
observers were unable to identify the interval containing the path.
Consequently, the ability to perform this task demonstrated that
observers could spatially integrate information about image structure
across extended areas of visual space. The stimuli used make it
unlikely that, the path may be segregated by filtering along any one
dimension because of the following: (1) These were band-pass stimuli
and did not contain any low spatial frequency structure; (2) the path
had a constant visual angle of 3.3°, and successive elements were
spaced up to a distance of 0.85° (These are distances that are much
greater than physiological estimates of the receptive field size of
neurons selective for a 6-cyc/deg grating patch in primary visual
cortex [V1]); and (3) the metric of sensitivity to the paths involved
manipulating the local orientations of the elements defining the path.
This orientation randomization has the same effect as alternating the
spatial phase of path elements.
It is important to note, however, that in conditions in which the
spacing of elements in the path is less than the spacing of the
background elements, it is possible to identify the path simply on the
basis of the relative density of elements around the
path,
20 21 a first-order texture density cue.
One possible central mechanism advanced recently in dyslexia is
the presence of a generalized temporal processing deficit across
sensory modalities
6 with an impaired focus of
attention.
38 39 Is it possible, then, that the differences
observed between subject groups in the present study were due to
attentional mechanisms? The overall consensus with respect to the
visual domain is that there is impaired attention with an increase in
attentional dwell time
40 —that is, it takes longer for
dyslexic persons to disengage their attention from one visual target to
the next. This has been found to be the case for sequences of rapidly
presented stimuli at intervals of less than 1 second. Stimulus duration
in this study was always 1 second, allowing sufficient viewing time in
both subject groups and therefore giving no subject group an advantage.
In addition, much converging evidence indicates an asymmetric
distribution of attention between the two visual fields, hypothesized
as a left-side minineglect in dyslexia.
38 39 41 Could
some form of deficiency in the visual processing of only one side of
the brain have been reflected in our anomalous results?
This is unlikely, because the adaptive staircase procedure used in this
study increased the orientation jitter when observers correctly
identified the interval containing the path and decreased orientation
jitter when observers were unable to identify the interval containing
the path. Therefore, for a threshold to be reliably and accurately
obtained, both subjects groups would have had to be able to perform at
100% (stimuli equally presented to the right and left field) correct
levels when the orientational jitter was 0°.
Furthermore, all observers were practiced in psychophysical testing,
with the dyslexic subjects having completed a previous study in which
spatiotemporal visual processing was investigated.
42 The
procedure in that study also consisted of a 2-alternate forced choice
(AFC) paradigm with both stimuli being presented simultaneously. No
significant difference in visual thresholds was demonstrable between
the dyslexic and control groups. This appears to negate any general
deficiency the dyslexic observers in the present study may have had in
comparing two sides of a screen simultaneously, contradictory to any
underlying weak cross-hemispheric connection.
It is interesting that several lines of recent work have also
demonstrated in amblyopia impairments in contour integration,
especially in persons with strabismus; in path detection
31 and closed-circle paradigms;
32 and in the perceptual
grouping of elements.
43 There is little consensus,
however, at this stage about whether these deficits are indicative
primarily of poor perceptual integrative processes in the amblyope’s
visual system
43 due to anomalous long-range interactions
between orientational detectors,
44 or are indeed a
consequence of the disrupted positional coding that is thought to
underlie the perceptual deficit in amblyopia.
45 46 In the
present study, it seems unlikely in the dyslexic subjects that a
general deficiency would have been so systematically affected by
stimulus variables.
Global precedence is a finding that supports the primacy of global
information in conscious perception. Global information appears to be
processed more efficiently in the right hemisphere,
47 48 and it is particularly interesting that right parietal cortical
dysfunction has been linked to dyslexia.
6 41 Patients with
lesions in the right hemisphere can accurately reproduce local elements
but not the global configuration
49 (Fig. 5) . It is possible that right hemispheric dysfunction in dyslexia
predisposes to the deficits in global processing illustrated in this
study (the integration of local elements = Gabor patches,
producing a global percept = path) and in the difficulties
encountered during the reading process, when single letters and words
may be identified readily when masked but the overall appearance of
text is at times confusing and even aversive.
11 12
In the present study we have described a visual deficit in a global
integration task in which the stimuli used local orientation noise to
ensure that observers were forced to integrate the path with
facilitatory and inhibitory connections among low-level
detectors.
17 The pattern of deficits reported herein
suggest that in dyslexia abnormal cooperative associations may be
present, indicative of poor perceptual integration. If cooperative
associations allow a more coherent visual experience, disruption of
these may manifest in natural viewing as the visuoperceptual
distortions and symptoms that characterize developmental dyslexia.
AJS is supported by a Medical Research Council Fellowship.
Submitted for publication September 27, 2000; revised April 5, 2001;
accepted May 15, 2001.
Commercial relationships policy: N.
The publication costs of this article were defrayed in part by page
charge payment. This article must therefore be marked“
advertisement” in accordance with 18 U.S.C. §1734
solely to indicate this fact.
Corresponding author: Anita J. Simmers, Department of Visual
Rehabilitation, Institute of Ophthalmology, University College London,
11-43 Bath Street, London EC1V 9EL, UK.
[email protected]
The authors thank Uri Polat and an anonymous referee for their
useful and positive comments, which allowed us to improve the
manuscript.
Rutter M. Prevalence and types of dyslexia. Benton AL Pearl D. eds. Dyslexia, an Appraisal of Current Knowledge. 1978;5–28. Oxford University Press New York.
Bradley L, Bryant PE. Difficulties in auditory organisation as a possible cause of reading backwardness. Nature
. 1978;271:746–747.
[CrossRef] [PubMed]Farmer ME, Klein RM. The evidence for a temporal processing deficit linked to dyslexia: a review. Psychol Bull Rev
. 1995;2:460–493.
[CrossRef] Lovegrove WJ, Bowling A, Badcock D, Blackwood M. Specific reading disability: differences in contrast sensitivity as a function of spatial frequency. Science
. 1980;210:439–440.
[CrossRef] [PubMed]Stein J, Walsh V. To see but not to read: the magnocellular theory of dyslexia. Trends Neurosci
. 1997;20:147–152.
[CrossRef] [PubMed]Livingstone MS, Rosen GD, Drislane FW, Galaburda AM. Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proc Natl Acad Sci USA
. 1991;88:7943–7947.
[CrossRef] [PubMed]Cornelissen P, Hansen PC, Gilchrist I, Cormack F, Essex E, Frankish C. Coherent motion detection and letter position encoding. Vision Res
. 1998;38:2181–2191.
[CrossRef] [PubMed]Eden GF, Van Meter JW, Rumsey JM, Maisog JM, Woods RP, Zeiffiro TA. Abnormal processing of visual motion in dyslexia revealed by functional brain imaging. Nature
. 1996;382:66–69.
[CrossRef] [PubMed]Cornelissen P, Bradley L, Fowler S, Stein J. What children see affects how they spell. Dev Med Child Neurol
. 1994;36:716–726.
[PubMed]Wilkins AJ, Nimmo-Smith I. On the reduction of eye-strain when reading. Ophthalmic Physiol Opt
. 1984;4:53–59.
[CrossRef] [PubMed]Conlon E, Lovegrove W, Hine T, Chekaluk E, Piatek K, Hayes-Williams K. The effects of visual discomfort and pattern structure on visual search. Perception
. 1998;27:21–33.
[CrossRef] [PubMed]Hubel DH, Wiesel TN. Receptive fields and functional architecture of monkey striate cortex. J Physiol
. 1968;195:215–243.
[CrossRef] [PubMed]Anderson SJ, Burr DC. Receptive field size of human motion detection units. Vision Res
. 1987;27:621–635.
[CrossRef] [PubMed]Hess RF, Dakin SC. Absence of contour linking in peripheral vision. Nature
. 1997;390:602–604.
[CrossRef] [PubMed]Dakin SC, Hess RF. Spatial-frequency tuning of visual contour integration. J Opt Soc Am A
. 1998;15:1486–1499.
[CrossRef] Gilbert CD, Hirsch JA, Wiesel TN. Lateral interactions in visual cortex. Cold Spring Harbor Symp Quant Biol
. 1990;55:663–677.
[CrossRef] [PubMed]Ts’o DY, Frostig RD, Leike EE, Grinvald A. Functional organization of primate visual-cortex revealed by high resolution optical imaging. Science
. 1990;249:417–419.
[CrossRef] [PubMed]Polat U, Mizobe K, Pettet MW, Kasamatsu T, Norcia AM. Collinear stimuli regulate visual responses depending on cell’s contrast threshold. Nature
. 1998;391:580–584.
[CrossRef] [PubMed]Field DJ, Hayes A, Hess RF. Contour integration by the human visual system: evidence for a local “association field.”. Vision Res
. 1993;33:173–193.
[CrossRef] [PubMed]Kovacs I. Human development of perceptual organization. Vision Res
. 2000;40:1301–1310.
[CrossRef] [PubMed]Pettet MW. Shape and contour detection. Vision Res
. 1999;39:551–557.
[CrossRef] [PubMed]Mullen K, Beaudot WHA, et al. Contour integration in color vision: a common process for the blue-yellow, red-green and luminance mechanisms?. Vision Res
. 2000;40:639–655.
[CrossRef] [PubMed]Kovacs I, Julesz B. A closed curve is much more than an incomplete one: effect of closure in figure-ground segmentation. Proc Natl Acad Sci USA
. 1993;90:7495–7497.
[CrossRef] [PubMed]Roelfsema PR, Scholte HS, Spekreijse H. Temporal constraints on the grouping of contour segments into spatially extended objects. Vision Res
. 1999;39:1509–1529.
[CrossRef] [PubMed]Dakin SC, Hess RF. Contour integration and scale combination processes in visual edge detection. Spat Vis
. 1999;12:309–327.
[CrossRef] [PubMed]Hess RF, Dakin SC. Contour integration in the peripheral field. Vision Res
. 1999;39:947–959.
[CrossRef] [PubMed]Keeble DRT, Hess RF. Discriminating local continuity in curved figures. Vision Res
. 1999;39:3287–3299.
[CrossRef] [PubMed]Hess RF, Field DJ. Contour integration across depth. Vision Res
. 1995;35:1699–1711.
[CrossRef] [PubMed]Hess RF, Hayes A, Kingdom FAA. Integrating contours within and through depth. Vision Res
. 1997;37:691–696.
[CrossRef] [PubMed]Hess RF, McIlhagga W, Field DJ. Contour integration in strabismic amblyopia: the sufficiency of an explanation based on positional uncertainty. Vision Res
. 1997;37:3145–3161.
[CrossRef] [PubMed]Kovacs I, Polat U, Pennefather PM, Chandna A, Norcia AM. A new test of contour integration deficits in patients with a history of disrupted binocular experience during visual development. Vision Res
. 2000;40:1775–1783.
[CrossRef] [PubMed]Pelli DG. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis
. 1997;10:437–442.
[CrossRef] [PubMed]Pelli DG, Zhang L. Accurate control of contrast on microcomputer displays. Vision Res
. 1991;31:1337–1350.
[CrossRef] [PubMed]Watson AB, Pelli DG. A Bayesian adaptive psychometric method. Percept Psychophys
. 1983;33:113–120.
[CrossRef] [PubMed]Yen SC, Finkel LH. Extraction of perceptually salient contours by striate cortical networks. Vision Res
. 1998;38:719–741.
[CrossRef] [PubMed]Nafziger JS, Yen SC, Finkel LH. Psychophysical determination of the spatial connectivity function in a model of contour salience. Neurocomputing. 1999;26–27:823–830.
Facoetti A, Lorusso ML, Paganoni P. The spatial distribution visual attention in developmental dyslexia. Exp Brain Res. 2000;4:531–538.
Facoetti A, Turratto M. Asymmetrical visual fields distribution of attention in dyslexic children: a neuropsychological study. Neurosci Lett
. 2000;290:216–218.
[CrossRef] [PubMed]Hari R, Valta M, Uutela K. Prolonged attentional dwell time in dyslexic adults. Neurosci Lett
. 1999;271:202–204.
[CrossRef] [PubMed]Hari R, Koivikko H. Left side mini-neglect and attentional sluggishness in dyslexic adult. Soc Neuroscience Abstr. 1999;25:1634.
Simmers AJ, Bex PJ, Smith FH, Wilkins AJ. Spatiotemporal visual function in tinted lens wearers. Invest Ophthalmol Vis Sci
. 2001;42:879–884.
[PubMed]Mussap AJ, Levi DM. Amblyopic deficits in detecting a dotted line in noise. Vision Res
. 2000;40:3297–3307.
[CrossRef] [PubMed]Polat U, Sagi D, Norcia AM. Abnormal long-range spatial interactions in amblyopia. Vision Res
. 1997;37:737–744.
[CrossRef] [PubMed]Hess RF, Field DJ, Watt RJ. The puzzle of amblyopia. Blakemore C eds. Vision Coding and Efficiency. 1990;267–280. Cambridge University Press Cambridge, UK.
Watt RJ, Hess RF. Spatial information and uncertainty in anisometropic amblyopia. Vision Res
. 1987;27:661–674.
[CrossRef] [PubMed]Sergent J. The cerebral balance of power: confrontation or cooperation. J Exp Psychol. 1982;8:253–272.
Robertson LC, Lamb MR, Knight RT. Effects of lesions of the temporal parietal junction on perceptual and attentional processing in humans. J Neurosci
. 1988;8:3757–3769.
[PubMed]Delis DC, Robertson LC, Efron R. Hemispheric specialization of memory for visual hierarchical stimuli. Neuropsychologia
. 1986;24:205–214.
[CrossRef] [PubMed]