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Neuropsychologia 40 (2002) 2144–2155

Executive functioning in adults and children with developmental dyslexia


Mark Brosnan∗ , James Demetre, Stephen Hamill, Kate Robson, Haidee Shepherd, Gerard Cody
Department of Psychology, School of Social Sciences and Law, University of Greenwich, London SE9 2UG, UK
Received 28 March 2001; received in revised form 18 March 2002; accepted 20 March 2002

Abstract
The performance of developmentally dyslexic children and adults was studied upon a range of tasks that involved executive functioning.
Both adult and child samples of dyslexics were found to under-perform on the group-embedded figures test. This test required the
identification of constituent parts from within complex visual arrays, with good performance necessitating the inhibition of the processing
of the surrounding context. A general deficit on visual–spatial tasks was eliminated as an explanation as dyslexics performed normally
upon a range of other non-verbal assessments. The dyslexics consistently demonstrated a deficit in digit span tasks, a decrement that was
increased with distractors, again suggesting difficulties in inhibiting the processing of the surrounding context. A deficit was also identified
upon a verbal fluency task without a deficit in vocabulary level. Additionally, a specific deficit in the recollection of the temporal order
of the presentation of items was in evidence, without a deficit in the recognition of the items themselves. The findings taken as a whole
suggest that dyslexic individuals show deficiencies in executive functions relating to inhibition of distractors and to sequencing of events,
a set of tasks associated with left prefrontal cortex functioning in the acquired neuropsychology literature.
© 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Group-embedded figures test; Inhibition of distractors; Left prefrontal cortex

Developmental dyslexia (DD) is defined by the World see [61] for a meta-analysis). In the most comprehensive
Federation of Neurology [85] as a disorder manifested by MRI study of brain anatomy in DD, Eliez et al. [17] report
difficulty in learning to read despite conventional instruc- a significant decrease in grey matter on the left side and a
tion, adequate intelligence and sociocultural opportunity. (possibly consequent) non-significant greater-than-normal
This definition is consistent with the DSM-IV classifica- rightward symmetry of grey matter.
tion of specific reading difficulty, for which prevalence is A rightward symmetry is significant as the right hemi-
estimated to be around 5–10% in the school-aged popu- sphere primarily subserves the processing of the relatively
lation [1], although some estimates are as high as 20% global level, whilst the left hemisphere primarily subserves
of schoolchildren [72]. The earliest theorising of DD has the processing of the relatively local level [37]. With respect
implicated possible abnormalities in cerebral lateraliation, to reading, initial reading processes focus on the (relatively
specifically a failure to acquire left hemisphere speciali- global level) word, or ‘logographic’ [25] level (primarily un-
sation for language [57]. Evidence that hemispheric spe- dertaken by the right hemisphere) with a developmental shift
cialisation may play a role is suggested by the relatively to a focus on the processing of (relatively local level) letters
high incidence of left-handed or ambidextrous individuals (and the subsequent formation of grapheme–phoneme corre-
within the dyslexic population [51]. Geschwind and Behan spondences subserved mainly by the left hemisphere) occur-
[31] hypothesised that left-handedness and DD are related ring at around 7 years of age. This refocusing of processing
to a common factor affecting the development of the left onto local level elements requires the inhibition of global
hemisphere in utero, which results in right hemisphere level processing [9]. A major theory of DD [3–6] suggests
dominance. Neuroimaging studies consistently reveal that that the abnormal cerebral symmetry underpins a failure to
the dyslexic brain is distinguished from the non-dyslexic shift from the word level to the letter level of processing, ar-
brain in the degree to which language areas in the brain are resting reading development at the (relatively more global)
asymmetric (see [35]; Table 20.1, p. 624–5 for a summary, logographic level [25]. Unlike normal readers, dyslexic in-
dividuals do not show increased left hemisphere activation
∗ Corresponding author. Tel.: +44-20-8331-9622; when processing language nor a right ear advantage on di-
fax: +44-20-8331-8905. chotic listening tasks [6,51,78] highlighting that the DDs’
E-mail address: m.j.brosnan@greenwich.ac.uk (M. Brosnan). reading strategies are less phonemically based [50,56].

0028-3932/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 8 - 3 9 3 2 ( 0 2 ) 0 0 0 4 6 - 5
M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155 2145

Thus, DD can be described as a deficit in the inhibitory trend is the group-embedded figures test (GEFT; [84]).
processes required to shift from the logographic level of The GEFT requires participants to identify a simple shape
reading and as such we would expect the abnormal symme- (such as a cube) within a complex visual array, designed
try described above to be evident in the prefrontal regions, to provide distracting context. Effective inhibition of the
which are associated with the control of inhibition. Whilst distracting context allows for successful completion of the
most neuropsychological studies focus on more posterior ar- task. The poor GEFT performance of young children and
eas of the brain associated with language, Hynd et al. [36] elderly individuals is similar to the performance of frontal
found that atypical symmetry of the prefrontal regions cor- lobe patients. Frontal lesions affect the ability to control
related with deficits in reading skills. Abnormal symmetry interference from external and internal sources, without af-
has been found to be evident in the prefrontal cortex in fecting established IQ [75] and ERP studies have confirmed
language impaired children, in the absence of such abnor- the role of the frontal lobes in GEFT performance, specif-
malities in more posterior areas associated with language ically the left prefrontal cortex [19,20]. This is particularly
[28,39]. This would suggest that the hemispheric symmetry pertinent to reading as most text passages contain abundant
underpinning the deficit in DD would be manifest in other sources of interference (e.g. ambiguities, see [14,15] for a
cognitive assessments not directly related to reading, such full account). Some text processing difficulties exhibited
as tasks benefiting from inhibitory control. The main aim of by DDs maybe due to inefficient inhibition as they are
the four studies reported here is to evaluate this hypothesis with frontal patients, as ‘s/he will have difficulty remaining
by assessing dyslexic individuals on a series of tasks that “. . . within the selective system of connections given by
are not specifically associated with assessments of reading. the text” ([49, p. 286]; [14, p. 62]). Thus, in addition to its
Given the prefrontal symmetry that has been identified in impact on reading strategies, inhibition plays a significant
DD, we would predict biases in assessments of executive role in learning—particularly in the presence of interference
functioning, which include the capacity for inhibition. from distractors [14].
Executive functions refer to a collection of cognitive Whilst the prefrontal cortex is not a homogeneous struc-
abilities such as planning, sequencing, organisation and ture, having several distinct cytoarchitectonic regions, the
inhibition, associated with the functioning of the prefrontal capacity for inhibition is an intrinsic property of the pre-
cortex [27,49]. DDs have been shown to demonstrate poor frontal cortices as a whole [65]. The abnormal cerebral sym-
strategy formation and a lack of planning and organis- metry in dyslexia discussed above is particularly relevant
ing [11,12,41,52,62]. DDs, for example, under-perform on to this aspect of executive functioning as the left prefrontal
Tower of Hanoi (ToH) assessments of planning and strategy region inhibits the processing of the right prefrontal region
formation. Despite the potentially significant role of inhibi- [24] raising the possibility that a deficit in the control of in-
tion in the development of reading, this executive function hibition in the left prefrontal cortex may underpin DD. ERP
has been largely neglected in the assessment of DD. The studies have identified the left frontal lobe as particularly
potential significance of inhibitory processes is highlighted important for the selective processing of the local level [86],
by the consistent deficit that has been identified in verbal a process that requires the inhibition of the global level
digit span tasks, which assess aspects of working memory. processing (as described above). These inhibitory processes
Increasingly taxing working memory resources results in mediate selective attention and the inability to inhibit dis-
increased difficulty in controlling inhibition [60]. Working tractors may underlie the distractibility frequently found in
memory demand and the demand for inhibition have been frontal patients [24] and is also reported in dyslexics [83].
identified as the two dimensions critical for understanding In normal processing, increased blood flow in the left
the breadth of executive functioning tasks. Tasks with a prefrontal cortex is associated with efficient planning and
high demand for either or both of these dimensions are organisation [54]. The verbal fluency task, for example, is
sensitive to prefrontal function and may be mediated by a associated with left prefrontal cortex functioning which re-
single cognitive mechanism (see [64] for a review). quires the generation of words that begin with a specified
This is consistent with a large body of research that argues letter (F, S). Patients with bilateral or left frontal lesions but
the capacity for inhibition (or ‘resistance to interference’) not right frontal lesions have been found to generate signif-
within the perceptual domain is a major factor in cognitive icantly fewer words than matched controls [38,53]. These
development that is intimately associated with the operation findings from the acquired literature are comparable to the
of the prefrontal cortex; young children ‘find it difficult study of developmental dyslexics who also display a deficit
to resist misleading, irrelevant visual and auditory stimuli’ on this task [44,47]. Whilst it is probable that the represen-
([14], p. 224). This sensitivity to interference declines tations of words are stored in the temporal lobes, the left
throughout the school years through increased effectiveness prefrontal cortex is involved in generating appropriate re-
in inhibiting or suppressing stimuli or associations that are sponses and inhibiting inappropriate responses [26].
not relevant to the task at hand [27,49]. This sensitivity As Bakker’s [3–6] proposal of abnormal symmetry in DD
also increases again during the ageing process, beginning extends to the prefrontal cortex, we would predict deficits
in the 50s [46]. A task that assesses the effectiveness of in executive functions associated with the left prefrontal
these inhibitory processes and mirrors this developmental cortex, one of which is a failure to inhibit the processing
2146 M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155

of distractors by the right hemisphere. This is consistent Table 1


with Eliez et al. [17, p. 642] who conclude ‘Although the Means (S.D.) for study 1
reading disorder that defines dyslexia may primarily reflect Dyslexic Non-dyslexic P-value
left-sided anatomical and functional abnormalities, the more (N = 9) (N = 9)
subtle involvement of homologous right-sided regions may Age 34 (11.80) 30 (7.25) NS
contribute to additional deficits that are not yet well recog- DS 13.44 (4.28) 18.22 (2.95) <0.01
FDS 7.67 (2.00) 10.11 (1.97) <0.01
nised or understood’. The present study aims to incorporate
BDS 5.78 (2.68) 8.11 (1.27) <0.05
the lateralisation to right or left frontal regions associated GEFT 10.11 (4.76) 14.33 (3.00) <0.05
with executive functions to better understand the cognitive Phoneme fluency 5.78 (3.87) 7.89 (2.37) NS (<0.1)
deficits associated with dyslexia. We predict that a failure WAIS sequencing 15.33 (4.47) 17.78 (2.11) NS
to inhibit the processing of irrelevant context will be re- ToH errors 78.44 (28.26) 78.67 (26.82) NS
ToH initial thinking 20952 (11917) 27239 (18954) NS
flected in a poor GEFT performance in DDs. Additionally
ToH subsequent thinking 3480 (4145) 3204 (2971) NS
we would predict a poor performance on the verbal fluency Free recall 1 15.33 (3.46) 17.56 (3.94) NS (<0.1)
task that has also been associated with left prefrontal func- Free recall 2 20.56 (4.50) 23.11 (3.22) NS (<0.1)
tioning. Planning will be assessed using the ToH task, as this ARC 1 (clustering) 0.60 (0.37) 0.46 (0.24) NS
has been used previously to assess this aspect of executive ARC 2 (clustering) 0.89 (0.13) 0.83 (0.13) NS
functioning. DS, digit span (F—forward, B—backward); ToH, Tower of Hanoi; ARC
The ability to resist the effects of interference also ex- 1, first instance when items were randomly arranged; ARC 2, second
plains the development of recall skills more effectively than instance when items were placed in semantic categories. Items are in
Appendix A.
the development of strategies, such as clustering [15,69].
The organisation of recall will be also be examined as the
reading ability of dyslexic children has been shown to bene- 1.2. Design
fit from explicit training on these skills (such as clustering),
suggesting that a failure to develop processes that generate The executive functions of inhibition, planning, sequenc-
and apply effective reading strategies impacts on the read- ing and organisation were examined in an undergraduate
ing ability of dyslexic children [77,79]. Intervention based sample of ‘compensated’ DDs, who may be able to com-
around organisational strategies for DDs can, therefore, im- pensate for strategies that can be explicitly demonstrated
pact upon their reading abilities. A particular group of DDs, through interventions but not for capacity to inhibit interfer-
who have entered higher education, despite their reading dif- ence, such as cues that are not relevant to the task at hand.
ficulties, will be studied initially. The childhood problems As mentioned above, a deficit in digit span is characteristic
with DD extend into adulthood generally including those of DD and this measure was put in place to ensure that our
who enter university education [10,22,33,74]. These ‘com- adult dyslexics still demonstrated a deficit in digit span.
pensated dyslexics’ still demonstrate underlying difficulties This ensured that the ‘compensated’ dyslexics have a profile
and a profile similar to younger DDs despite compensating consistent with the DD literature. The development of digit
for their reading difficulties and progressing through the edu- span is dependant upon effective inhibitory processing as is
cation system [59]. For example, the deficit in digit span task an effective GEFT performance. These inhibitory processes
is consistently identified in dyslexia across the age span. It is are associated with the left prefrontal cortex, as is an effec-
conceivable, therefore, that the ‘compensation’ occurs in the tive verbal fluency performance. Verbal fluency has been
explicit strategies employed to facilitate reading but not in found to be very sensitive to left prefrontal cortex damage
the capacity for inhibition. The first study will examine the [7] probably as the unusual nature of the task requires par-
executive functioning of planning, sequencing, organising ticipants to devise their own strategy. Parker and Crawford
and inhibition in a population of dyslexic undergraduates. [58] suggest that this is the most widely used formal test of
frontal dysfunction.
Planning and sequencing are also associated with pre-
1. Study 1 frontal cortex functioning. The planning task used previ-
ously is the ToH task. The present version allows for motor
1.1. Participants ability to be factored out (see below). For the sequencing
task, the participant must be sensitive to subtle changes in
Nine dyslexic and nine non-dyslexic male undergraduates. the pictures to enable him/her to order a sequence of events.
The dyslexic sample had all received a formal diagnosis of This kind of comprehension of event structure is associated
dyslexia from an appropriately qualified professional during with prefrontal cortex functioning [27,49]. Finally, the or-
their formal schooling, prior to their arrival at University. ganisation of memory was assessed to allow for an index of
The sample was matched upon academic year and major, free recall and the extent to which the free recall has been
current academic grades and SES and undertook additional clustered, both when superordinate categories are and are
assessments, which are reported elsewhere. The ages are not made salient. This allows us to investigate absolute recall
reported in Table 1. in addition to an index of the clustering strategy employed.
M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155 2147

1.3. Tasks/measures Participants had to touch the ball they wish to move and then
touch the stocking in which they wanted to drop the ball.
1.3.1. Digit span This procedure was practised to ensure that participants were
The digit span procedure from the WAIS-R [82] was used familiar with the touch screen technology and the task. After
for both forward and backwards digit span. Participants were participants attempted the problems they were then asked to
read a series of numbers that they had to repeat back in the simply follow the display as it moves. In fact these moves
correct order. Two instances of each digit span length were were the moves that the participant made whilst attempting
given. A point was recorded for all correct responses and the problems. The subtraction of this motor element allows
testing ceased when an error occurred in both instances of a for the calculation of thinking times. Initial thinking time
digit span length. Forward digit span required the digits to was the time prior to the first move and subsequent thinking
be repeated in the order they were presented and backward time was the time between the first move and completion.
digit span required the order to be reversed. Each task had a minimum number of moves for completion,
additional moves were counted as errors.
1.3.2. Inhibition
The group-embedded figures test [84] was used to assess 1.3.5. Sequencing
the ability to inhibit the processing of irrelevant context. Af- The WAIS-R [82] contains a picture arrangement subtest
ter a practice session to ensure the principles are understood, that required participants to arrange a series of pictures in a
participants undertook two 5 min testing sessions, each of sequence. Participants were presented with a series of cards
which contained nine items (and a possible maximum score that had to be rearranged into a specific sequence for the
of 18). Participants located a simple figure within a complex pictures to form a coherent story. The tasks were timed and
visual array. The purpose of the visual array was to provide had a maximum score of 20.
a context that made disembedding the searched for part diffi-
cult. As an example, one of the simple figures resembles the 1.3.6. Organisation
outline of an upside-down kite. In the complex visual array, Organisation of memory was used to assess recall under
the lines that make up this outline are extended and over- two conditions, namely when superordinate categories were
laid with many parallel and perpendicular lines (of identical not made salient and then again when this potential organis-
colour and width). The complex visual array, therefore, pro- ing structure was made salient. Participants underwent two
vides a series of potential outlines that are similar (though recall tasks of the same 30 items to investigate categorical
longer or shorter or disproportionately wider or narrower) clustering in long-term memory. The to-be-recalled (TBR)
to the simple figure. Where the lines merge to form a geo- list comprised 30 items from three superordinate categories.
metric figure, for example a triangle, this element is lightly Previous research has shown that each of these items had
shaded to ‘reinforce given sub-wholes’ providing additional produced at least 90% agreement on name [73]. Each item
distraction that has to be ignored to complete the task suc- was represented as a black line drawing on laminated white
cessfully. There are a range of simple figures and complex card. Appendix A provides a list of the TBR items. A mixed
visual arrays to prevent practice effects. This measure has measures design was employed, with independent groups on
been found to be both valid and reliable [13,84]. group (dyslexic and non-dyslexic) and repeated measures on
trial (randomised and categorised TBR list). One TBR list
1.3.3. Verbal fluency was used for both trial conditions in order to eliminate po-
The verbal fluency task lasted 1 min during which time tential inter-list differences contaminating any obtained ef-
participants has to generate as many words as possible (ex- fects involving trial. Counterbalancing of two different lists
cluding plurals and proper nouns) beginning with a given was viewed as a risky design strategy, given the small sam-
letter (either F or S). Only one trial was undertaken per par- ple sizes anticipated in this study. A fixed order was used for
ticipant. the presentation of the two trials, with the randomised list
preceding the categorised list. A point was recorded for each
1.3.4. Planning item correctly recalled (maximum of 30). In Table 1, recall
Planning was assessed through a ToH task (called ‘stock- 1 is the number of items recalled from the randomised list
ings of Cambridge’ and referred to as ‘ToH’ in Table 1) and ARC 1 the adjusted ratio of clustering (ARC) for this
that required balls to be moved from one position to an- initial list. Similarly recall 2 and ARC 2 relate to the same
other to move from a start state to a goal state. There were measures for the second (categorised) instance of the list.
two instances of two, three, four and five move problems.
The problems were presented through the Cambridge neu- 1.4. Procedure
ropsychological test automated battery (CANTAB version
2.3; CeNeS Ltd. 1998) system that in addition to noting er- For the first trial, the TBR cards were shuffled prior to the
rors made, recorded the timing of initial thinking time (prior participant’s arrival. Once the participant had been seated,
to the first move) and subsequent thinking time (between E explained that a number of pictures of common objects
subsequent moves). The system uses a touch screen display. would be presented on the table before him/her, and that
2148 M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155

he/she will be asked to name each item, and would then be task (by 27% compared with controls) and the two recall
given 1 min to study these, and subsequently, remember as tasks (by around 2.5 TBR items compared with controls).
many as possible in any order. The cards were arrayed in
three rows of ten, and the participant was asked to name 1.6. Discussion
each item. The participant was then given 1 min to study the
items, but was not allowed to manipulate or move the cards. The difference in digit span confirmed that the student
Once the minute had elapsed, E collected the cards, and then dyslexic sample retained the typical dyslexic pattern of re-
asked the participant to undertake a brief repetition task of duced verbal working memory, despite undoubtedly having
repeating back each line of a poem that was read out by the to compensate for their deficit [55]. The deficit was found
experimenter. This filler task took approximately 1 min, and in both forward and backward digit spans. There were no
was intended to reduce the size of the recency effect, and group differences for any of the executive functioning mea-
hence, result in recall that was dependent upon the control sures of planning, sequencing or organisation of memory.
processes that govern the long-term memory component [2]. As hypothesised, however, there was a significantly poorer
Participants were given 2 min to recall items, their recall performance upon the GEFT, suggesting an inability to in-
being recorded on audiocassette tape. hibit irrelevant context in the dyslexic sample.
The second trial commenced approximately 40 min after The results of the planning, sequencing and organising
the first trial, with the other tasks above being interposed tasks are not consistent with previous research, some of
between the two trials. The same procedure was followed as which used the same measures of executive functioning as
for the first trial, with the exception that each of the three the present study. The use of adult ‘compensated’ dyslexics
rows comprised items from one superordinate category. The in the present study suggests that the compensation that
recordings were transcribed, and two measures obtained: occurs may be related to certain executive functions. Sim-
total correct recall, and an index of categorised recall, the ilarly, despite a trend to a lower recall score, DDs did not
ARC [66]. ARC indexes the extent to which the frequency demonstrate a deficit in the use of categorical clustering as a
of category adjacencies in a given recall protocol departs strategy (ARC scores). This is consistent with other research
from what would be expected by chance, given the number that found that certain executive function deficits diminish
of items recalled and the number of instances recalled from as DDs progress through the education system [12]. The
each category. Thus, ARC is independent of the absolute executive measures that did show a difference between the
level of accurate recall. ARC has a possible maximum of +1 groups were those requiring inhibition and associated with
(indicating perfect categorical clustering of recalled items), the left prefrontal cortex. The deficit in GEFT performance
with a score of 0 indicating a chance-level of clustering. is consistent with a description of a failure to inhibit the
ARC can also assume a negative value (below-chance levels processing of contextual information to facilitate the extrap-
of clustering). olation of constituent parts. The trend to a deficit in verbal
In between these tasks the GEFT, verbal fluency, the fluency is also consistent with a description of a deficit in
stockings of Cambridge, the WAIS-R digit span and se- left prefrontal cortex activity. Benton’s [7] original study
quencing tasks were undertaken in a random order. Partic- identified damage to the left prefrontal cortex resulting in
ipants were tested individually in a quiet room away from a 30% decrease in word generation. This is comparable to
any distractions. study 1, where the dyslexic sample demonstrated a 27%
decrement on the verbal fluency task.
1.5. Results It is conceivable that the stockings of Cambridge and the
WAIS-R sequencing tasks did not target one frontal lobe
Table 1 shows the group means and standard deviations specifically. Deficits in the WAIS-R sequencing task do not
for the dyslexic and non-dyslexic groups. As expected the appear to be specific to either the right or left frontal lobe
dyslexic group had a significantly reduced digit span com- and indeed greater impairment occurs with more posterior
pared with the non-dyslexic group (t = 2.76, d.f. = 16, damage [80]. Additionally, whilst Shallice [70] originally re-
P < 0.01). This was the case for both forward (t = 2.62, ported impairment upon the ToH task following left frontal
d.f. = 16, P < 0.01) and backward (t = 2.36, d.f. = 16, damage, a subsequent study failed to replicate the finding
P < 0.05) digit spans when they were separated out. The [71, p. 347]. This suggests that the compensation that occurs
GEFT, too, is consistent with the hypothesis that the dyslexic in DD may be restricted to executive functions that are not
group would underachieve upon this task (t = 2.25, d.f. = associated with the left prefrontal cortex. The frontal sym-
16, P < 0.05). For all the assessments of planning, sequenc- metry described in the introduction may underpin the lack of
ing and organisation of memory, there were no significant ability to compensate for the executive functions associated
differences between the groups. The improvement in recall with the left prefrontal cortex.
and ARC scores on the memory task when the superordinate The poor GEFT and digit span performances suggest
categories were made salient was also comparable across that DDs under-perform when the demands are high for
groups. The only trends (P < 0.1, one-tailed) were for the the critical dimensions of executive functioning [60]. The
dyslexic group to under-perform upon the verbal fluency deficit in digit span is a common finding in studies of DD
M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155 2149

Table 2 across memory tasks presented in different modalities [40].


Means (S.D.) for study 2 Other research, however, reports no differences in the
Dyslexic (N = 30) Non-dyslexic (N = 30) P-value visual–spatial abilities of dyslexics compared with matched
Age 14.0 (0.8) 13.8 (0.6) NS
controls [32,34]. The sensitivity to interference described
GEFT 8.2 (5.7) 13.3 (2.4) <0.05 above has also been argued to facilitate success within cer-
tain domains [83]. The visual–spatial abilities of dyslexic
students were, therefore, further examined in the third study.
but identification of a poor GEFT performance is a novel
finding. Having identified a deficit in the GEFT in a small 3.1. Participants
number of adult dyslexics in study 1, study 2 sought to
replicate the finding with a larger and younger sample.
Fifteen dyslexic university students and 15 matched con-
trols, diagnosed and matched as in study 1, aged 18–29 years
with eight females and seven males in each sample. None
2. Study 2
of these participants took part in study 1.
2.1. Participants
3.2. Design
Thirty dyslexic males from a school for dyslexic children
and 30 non-dyslexic males matched for age, demographic The digit span assessment from the WAIS-R was admin-
variables, SES and academic performance from a nearby istered as before. Additionally, the CANTAB touch screen
school. The sample was selected to be as young as possible system described above was used to administer four tests of
for the reliability of the measure. The youngest participant visual spatial cognition. These were as follows.
was 13 years of age. For ages much below this, the children’s • Spatial span: A pattern of white squares was shown on
embedded figures test (CEFT) is recommended [84]. The the screen. Some of the squares change in colour, one by
ages are presented in Table 2. one, in a variable sequence. At the end of the sequence,
a tone indicates that the subject should touch each of the
2.2. Design, results and discussion boxes coloured by the computer in the same order as they
were originally presented. Two instances are presented at
All participants were given the GEFT as before. As pre- each sequence level that increases in length by one item
dicted, study 2 replicates the findings from study 1. Table 2 until the participant fails both instances of the same level
shows that dyslexics have greater difficulty inhibiting the (mirroring exactly the verbal digit span procedure).
processing of the visual context to identify the parts of stim- • Spatial recognition: The participant was presented with
uli than matched controls (t = 4.40, P < 0.001). This a white square that moves in sequence to five different
finding from study 1 is, therefore, extended to a larger and places on the screen. The participant then sees a series of
younger dyslexic sample. five pairs of squares, one of which they have already seen
in the presentation phase and one of which was not seen
in the presentation phase. The participant has to touch the
3. Study 3 previously seen square. Locations are tested in the reverse
order of presentation order. This procedure is repeated
The results from studies 1 and 2 are consistent with de- three times, each time with five new locations.
scriptions of DD as a deficit in inhibiting irrelevant visual • Delayed matching to sample: The participant was shown
cues, associated with a deficit in left prefrontal cortical a complex visual pattern and then after a brief delay, four
processing. This has been demonstrated using the GEFT, choice patterns. The participant has to point to the pre-
an assessment that is visual–spatial in nature. An alterna- viously seen pattern. These patterns are designed so they
tive hypothesis might contend that just as DDs have poor cannot easily be given verbal labels. Each pattern is made
reading ability, they also have poor visual–spatial ability up of four sub-elements each of a different colour. To dis-
(generally). Normally, whilst phonological aspects of work- courage encoding strategies based upon encoding single
ing memory are primarily subserved by the left hemisphere, quadrants, all four choices have one quadrant in common.
visual–spatial aspects of working memory are normally The choices are presented either simultaneously or with
primarily sub served by the right hemisphere [29]. In DD, 0, 4 or 12 s delays. Ten examples of each delay were used,
however, it is conceivable that the over-involvement of giving a total of 40 presentations.
the right hemisphere in reading compromises non-verbal • Pattern recognition: The participant was presented with a
abilities [42,51]. Indeed Fein et al. [21] report that dyslex- series of 12 visual patterns (as above) in the centre of the
ics show working memory deficits for both verbal and screen. In the recognition phase, participants are presented
non-verbal material. This is consistent with research that ar- with a previously seen pattern and a novel pattern. The
gues the maintenance of serial order shares common features participant has to touch the previously seen square. The
2150 M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155

Table 3 working memory is part of the working memory model but


Means (S.D.) for study 3 would appear not to suffer the effects of high demand as
Dyslexic Non-dyslexic P-value verbal working memory does.
(N = 15) (N = 15) The results of study 3 are consistent with the proposal that
Age 23 (3.6) 24 (4.1) NS the deficit evidenced in the GEFT is not due to a general
Digit span 14.13 (4.2) 17.73 (4.3) <0.001 deficit in visual–spatial abilities. The pattern of results of the
Spatial span 7.13 (1.3) 7.53 (0.9) NS first three studies is consistent with the proposal that DD can
Spatial recognition 83.3 (46) 80.7 (38) NS
Pattern recognition 93.1 (42) 88.1 (43) NS (<0.1)
be characterised as a specific deficit in control of inhibition,
Delayed matching 90.2 (40) 88.0 (37) NS assessed using the GEFT. The relative weakness of executive
functioning associated with the left prefrontal cortex was
also implicated in study 1 and was further examined in the
final study.
recognition phase is presented in the reverse order of the
presentation order.
4. Study 4
The scores for the latter three assessments are presented
as percentages and did not deviate significantly from a
normal distribution. The tests were presented in a random Study 4 aimed to examine executive functioning in a larger
order. and younger sample with tasks specifically associated with
the left prefrontal cortex. In addition to study 1 containing a
relatively small sample size, controlling for some sort of lit-
3.3. Results eracy standard is recommended for clinical assessment [48]
and was incorporated into the final study. It is clear that a
The difference in digit span was again in evidence, reaf- neuropsychologically informed understanding of executive
firming that dyslexic students again demonstrate a deficit functioning is required to characterise the deficits associated
in this task. Table 3 highlights, however, that there were no with DD. From the study 1, we can infer that there will be
significant differences upon the visual–spatial measures. specific deficits that are associated with left frontal func-
tioning. This was confirmed in study 2 for the GEFT in a
3.4. Discussion younger sample and the final study examined verbal fluency
in a younger sample. Additionally, a specific aspect of se-
Once again the deficit in digit span provides support for quencing tasks that is associated with lateralised executive
the contention that dyslexics at university still retain verbal functioning was assessed.
working memory deficits. There were no visual spatial dif- Temporal order judgements can be seen as a specific
ferences, however, suggesting neither enhanced nor inhibited example of sequencing and have been found to be deficient
visual spatial abilities (associated with the right hemisphere) in dyslexic children and adults [21,44]. Patients with pre-
in DD. Examining the means highlights that dyslexics frontal lesions (bilateral, left) have also been found to suffer
averaged higher scores (albeit non-significantly) than the selective impairment in the recall for order of presentation
non-dyslexics on the visual–spatial measures. The pattern with the absence of recognition deficits for the same images
recognition difference shows a trend at P < 0.08, two [43,68]. Aspects of retrieval other than the temporal order,
tailed, for example. Overall, however, dyslexic individuals such as recognition, have not been associated with the pre-
perform comparably to non-dyslexic individuals on visual frontal cortex [68,76]. Executive functions associated with
spatial tasks associated with right hemisphere speciali- the left prefrontal cortex would selectively impair the judge-
sation. ment of the order of items to be recognised without necessar-
It would appear that the abnormal symmetry does not ily impacting upon the recognition itself. The introduction
enhance cognitive abilities associated with the right hemi- to the present series of studies also provided evidence to
sphere. The aim of these assessments was to confirm that support the contention that the inability to inhibit interfer-
DDs do not have a general visual–spatial deficit. Only a ence extends beyond the visual plane to other modalities.
small range of visual–spatial tasks were used and it may be A specific hypothesis is drawn from the acquired literature
that other assessments could yield an advantage. The failure that a deficit associated with the left prefrontal cortex will
to identify any advantage on these tasks may be due to the become manifest in an inability to inhibit the processing
normal right hemisphere specialisation for non-verbal tasks of distracting verbal material [55]. The susceptibility of
being compromised by the verbal activity that the hemi- DDs to verbal distraction has been observed in the class-
sphere undertakes. room [62].
Previous findings of impaired spatial span in DD were not Therefore, specific aspects of planning (verbal fluency),
replicated. As with study 1, this may be due to the ability sequencing (temporal order) and inhibition (of distraction)
of ‘compensated dyslexics’ to compensate for deficits not associated with left prefrontal functioning were examined
directly associated with left hemisphere processing. Spatial in study 4. Younger children were selected to minimise any
M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155 2151

effects of strategy tuition that may occur through the educa- Table 4
tion process. Means (S.D.) for study 4
Dyslexic Non-dyslexic P-value
4.1. Participants (N = 16) (N = 16)
Age 9.9 (0.9) 9.9 (0.9) NS
Sixteen dyslexics aged 8–10 years (6 girls and 10 Verbal fluency 7.0 (3.7) 10.5 (3.2) <0.01
Vocabulary 98.7 (11.8) 93.9 (12.1) NS
boys) had all received a diagnosis from an educational
Digit span silent 5.0 (1.5) 5.8 (1.3) <0.05
psychologist with no history or evidence of sensory im- Digit span noisy 4.4 (1.0) 5.8 (1.2) <0.001
pairments, hyperactivity or emotional problems. The DS difference 0.6 (1.1) 0.0 (1.0) NS
dyslexics attended a mainstream school and 16 age- and Temporal order 3.6 (1.0) 4.2 (0.8) <0.05
gender-matched controls were selected as before from class Recognition 9.2 (1.9) 9.9 (0.5) NS
peers.
As the measures produce parametric data and we are
4.2. Design and procedure
predicting that the dyslexic group will under-perform upon
As before, the verbal fluency task lasted 1 min during specific tasks, parametric one-tail tests were performed.
which time participants has to generate as many words as
possible (excluding plurals and proper nouns) beginning 4.3. Results
with a given letter (either F or S). Only one trial was un-
dertaken per participant. To ensure that all participants had As predicted the dyslexic group produced significantly
a similar level of vocabulary, the british picture vocabulary fewer items on the verbal fluency task than the non-dyslexic
scale (BPVS [16]) was also administered. This requires par- group (t = 2.90, d.f. = 30, P < 0.01) with no significant
ticipants to point to one of four pictures that correspond to difference on the BPVS scores (t = 1.14, d.f. = 30, NS).
the word spoken by the experimenter. Indeed the dyslexic group scored insignificantly higher upon
Forward digit span was assessed using the standard this latter task. The dyslexic group also obtained a lower
WISC-III procedure [81]. An increasing series of digits digit span in the silent condition (t = 1.65, d.f. = 30,
is read to the participant who recalls the digits immedi- P = 0.05). This difference was enhanced in the background
ately. Each sequence length occurs twice and when both noise condition (t = 3.51, d.f. = 30, P < 0.001) and the
sequences of that length are recalled erroneously, testing decrement for the dyslexic group showed a trend towards a
ceases. Digit span is the highest sequence length cor- greater decrement than the non-dyslexic group (t = 1.48,
rectly recalled. This occurred under the traditional con- d.f. = 30, P = 0.075). This can be described as a trend for
dition of silence and under an additional condition with dyslexics to be distracted, especially as the distraction had
background voices. A different set of sequences was read no impact upon the performance of non-dyslexics. Finally
out as above. To the right of the participant 0.5 m away and again in line with prediction the dyslexic group scored
a tape recorder played a tape of continuous speech (no significantly lower on the recall of temporal order (t = 1.77,
numbers). The tape recorder was set at 30 db. At the d.f. = 30, P < 0.05) with no significant difference for the
end of each session the children were asked if they had recognition scores (t = 1.42, d.f. = 30, NS). All the means
heard the digits clearly. All the children reported that they are reported in Table 4.
had.
To assess long-term memory processes children were 4.4. Discussion
shown ten cards with simple line drawings from Snodgrass
and Vanderwart (as study 1). Each card was presented for Once again the deficit in digit span was evident in the
3 s and then removed untill all ten cards had been presented. younger sample. This difference increased with verbal dis-
A brief filler task was undertaken whilst the ten cards were tractors, which is consistent with the left prefrontal cortex
shuffled (as study 1) and paired with a previously unseen failing to inhibit analysis of irrelevant background verbal
card. The participant was then presented with a pair of material [55] and observations of dyslexic children’s dis-
cards and asked to point to the card that has been previously tractibility in the classroom [62]. The detrimental impact of
seen. The order was random as was whether the previously additional interference suggests that a sensitivity to distrac-
seen card was on the right or left. After this assessment tion may be related to the diminished digit span capacity in
of recognition the previously seen cards were presented in DD.
pairs (1st and 10th, 2nd and 9th, 3rd and 8th, 4th and 7th, The results are also consistent with the proposal that the
5th and 6th) and participants were asked to point to the verbal fluency and temporal order tasks associated with the
picture that had been shown first in the original presentation left prefrontal cortex are impaired independent of the vocab-
(identified as temporal order in Table 4). The ordering of ulary and recognition tasks, which are not associated with
the pairs was random and a point recorded for each correct prefrontal functioning. The decrement in verbal fluency was
response (maximum of 5). 33%, again similar to the 30% decrement identified in left
2152 M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155

frontal patients [7]. These three findings are all consistent tasks. Similarly the deficits in temporal order judgements
with the proposal that DD can be characterised as a deficit in and recall are consistent between dyslexics and frontal lobe
the executive functioning associated with the left prefrontal patients, in isolation from any deficits in recognition tasks or
cortex. general sequencing tasks [68]. The left and right prefrontal
cortices are not independent from each other and one aspect
of the functioning of the left prefrontal cortex is to inhibit
5. General discussion aspects of the processing of the right prefrontal cortex.
Thus, a single neuropsychological deficit may underpin the
Eliez et al. [17] suggested that an understanding of right cognitive performances of a bias towards failing to inhibit
and left hemisphere processing is required to fully appreciate the processing of context (and poor GEFT performance,
the deficits associated with DD. A rightward symmetry in the distractibility) and the decrement in verbal fluency and tem-
frontal lobes has been identified in DD, even in the absence poral order judgements. This concurs with assumptions that
of more posterior symmetry, and consequently the aim of the resistance to interference is a fundamental feature of the
this paper was to examine executive functioning in child and cognitive system (i.e. a psychological primitive), that cannot
adult dyslexics. Studies 1 and 2 demonstrated a deficit upon be explained in terms of other cognitive processes [15].
the GEFT in dyslexic children and adults. This is a novel The impact of irrelevant background verbal material of
finding, not previously identified. The GEFT requires the digit span in study 4 confirms this bias extends to the au-
identification of a specific element within a more complex ditory modality. DDs were less able to inhibit the process-
display. The task requires the inhibition of the processing of ing of the auditory context to maximise performance upon
irrelevant context to facilitate the identification of the salient the digit span task. DDs, however, did not demonstrate a
part. deficit on the spatial span task. Whilst the control of these
This perspective is consistent with a large body of liter- two working memory span systems resides within executive
ature that has identified the right hemisphere as processing functioning [2], the processing during span tasks activates
a relatively global level of stimuli and the left hemisphere more posteriors areas in the left and right hemispheres, re-
as processing a relatively local level. The rightward sym- spectively [29]. There are many links from the prefrontal
metry, therefore, favours a processing of the word (logo- cortices to posterior areas that are reciprocal. It is possible
graphic) level for reading in preference to the more efficient that the neuropathology resides outside of the prefrontal cor-
letter level. The present study suggests that this account of tex, in a closely connected brain system. From the range of
dyslexia is underpinned by a failure to inhibit the process- tasks described above, however, it seems more plausible that
ing of the logographic level that is required to establish the the left prefrontal cortex itself is responsible for a deficit in
normal reading process via grapheme–phoneme correspon- inhibiting interference.
dences [25]. The development of these reading processes is Working memory processes are involved in the inhibi-
facilitated by inhibiting the processing of distractors at the tion of inappropriate activity [64] and the extent to which
more global level. Recent neuroimaging research has iden- dyslexia could be described as a working memory deficit
tified that the normal processing of distractors, which indi- is unclear. As mentioned, DDs demonstrate a pattern sim-
cated the presence of potentially relevant information at the ilar to frontal lobe patients with deficits on recall (study 1)
unattended level, resulted in delayed lateralization of pro- and temporal order (study 4) tasks without deficits upon
cessing [18]. Distractors delayed the asymmetric processing recognition tasks [68]. Pennington et al. [60] argue that
of the local level to the left hemisphere and the global level temporal order and recall tasks utilise a memory system
to the right hemisphere. This is consistent with the neuropsy- that allows an individual to access, organise and manipulate
chological evidence that DDs fail to specialise language to memories, therefore, placing strong demands on working
the left hemisphere. Thus, the shaky grapheme–phoneme memory. The authors argue that this can be distinguished
representations associated with dyslexia (see [74] for an ac- from recognition memory, which relies on effective stor-
count) can be viewed as a specific manifestation of a more age and consolidation and place relatively few demands
general bias towards delayed asymmetry of processing— on working memory. The concept of working memory is
a process delayed by a failure to inhibit the processing of not distinct from inhibitory processing, however, as in-
interference. creasing demands on working memory results in increasing
The contention that these deficits in DD identified in the difficulty in controlling inhibition and a high demand for
present study can be characterised as an inability to inhibit either or both of these dimensions are sensitive to prefrontal
the processing of to-be-ignored information is supported function. A smaller digit span will, by definition, approach
by the poor performance of dyslexics upon the Stroop task capacity earlier (than a normal digit span) and demand in-
[45]. This performance upon the Stroop task also mirrors hibitory resources earlier. Additionally deficits in inhibitory
the performance of left frontal lobe patients [8]. A deficit in control will result in a poorer digit span performance,
left prefrontal cortex processing in DD is also suggested by highlighting how these two critical dimensions of execu-
the comparable deficit in the dyslexic samples (27 and 33%) tive functioning are inter-dependant and pertinent to under-
to the left frontal lobe patients (30%) on verbal fluency standing DD.
M. Brosnan et al. / Neuropsychologia 40 (2002) 2144–2155 2153

A potential contradiction resides in the failure to find a Appendix A. TBR items


difference in clustering in study one. Both groups recall
improved by around five items (from a list of 30) on the
Animals Objects Fruits/vegetables
second recall condition with no differences between groups
Frog Broom Lemon
or conditions for the clustering (ARC) scores. The acquired
Horse Anchor Pumpkin
literature would suggest that a left prefrontal deficit would
Cat Pencil Strawberry
manifest itself in a deficit in spontaneously applying a
Elephant Toothbrush Pear
clustering strategy and a consequently disproportionate in-
Owl Hammer Grapes
creased in free recall when the strategy was made explicit
Kangaroo Axe Onion
[67]. In the present study, the words were presented or-
Rabbit Candle Pineapple
thographically (rather than verbally), participants were not
Dog Belt Banana
explicitly told to cluster and related word lists were used
Fish Comb Carrot
on both recall trials—variations that reduce the demand
Camel Candle Apple
upon the left prefrontal cortex [23]. Future research could
explicitly manipulate these variables for the dyslexic pop-
ulation. It is interesting that the trend in DDs for a deficit
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