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Reactivity to Visual Signals in Neurofibromatosis Type 1:
Is Everything OK?
George A. Michael
Université de Lyon Sophie Garcia
Centre Hospitalier Lucien Hussel Vienne, France
Vania Herbillon and Laurence Lion-François
Hôpital Femme Mère Enfant Lyon, France
Objective: Deficits in multiple aspects of attention are a hallmark of the cognitive impairments found
with neurofibromatosis type I (NF1). Given, however, that some attention components are hierarchically
organized, it is possible that sustained attention, flexibility, and resistance to interference deficits
observed in NF1 may be because of weakened lower order attention components. This study investigated
the state of these low-level components in NF1. Method: Twenty participants with NF1 (ages 7–13) and
20 matched controls participated in a visual task. They were required to locate a target as quickly and as
accurately as possible and to ignore a potential distractor that could appear either before, at the same time,
or after the target. Response times (RTs) were collected, and indices of alerting (i.e., reactivity to warning
signals), distraction, and interruption (i.e., reactivity to signals appearing during attentive processing)
were computed. Results: The amplitude of the indices differed between the groups, F(2, 76) ⫽3.1, p⬍
.05. No difference was found with alerting (p⬎.85) or distraction (p⬎.84), but the interruption index
was higher in the NF1 group than the controls (p⬍.043). Conclusions: Elementary components on
which more complex attention processes are based are not all ok in NF1. It is suggested that overreac-
tivity to and longer inspection of visual signals occurring outside the current focus of attention
characterizes NF1 and that this might be partially responsible for focus of attention instability and lower
interference resistance in NF1.
Keywords: neurofibromatosis type I, NF1, visual attention, alerting, distraction, interruption
Neurofibromatosis type I (NF1) is an autosomal dominant con-
dition with a prevalence rate of approximately 1:3000 to 1:4000
(Acosta, Gioia, & Silva, 2006;Friedman, 1999;NINDS, 2007).
Children and adolescents with NF1 demonstrate learning difficul-
ties and poor academic performance, which would appear to stem
from deficits displayed in a wide range of cognitive skills, includ-
ing visual–spatial abilities, language, reading and writing, and
executive functioning (Acosta et al., 2006;Gilboa et al., 2011;
Isenberg, Templer, Gao, Titus, & Gutman, 2013;North, Hyman, &
Barton, 2002). Approximately 33%–50% of children with NF1
demonstrate multiple attention deficits (North et al., 2002;Rosser
& Packer, 2003), a hallmark of cognitive impairments (Templer,
Titus, & Gutmann, 2013). These include deficits in sustained
attention, selective attention, divided attention, task switching, and
response inhibition (Hyman, Arthur, & North, 2006;Hyman,
Shores, & North, 2005;Isenberg et al., 2013;Templer et al., 2013),
especially when tasks require a high degree of cognitive control
(Huijbregts, Swaab, & de Sonneville, 2010;Rowbotham, Pit-ten
Cate, Sonuga-Barke, & Huijbregts, 2009). These deficits are found
across sensory modalities (Isenberg et al., 2013) and are likely the
source of inattentive and impulsive behaviors in natural environ-
ments (Gilboa et al., 2011).
However, attention functions are not completely independent
from one other. Given that some components are hierarchically
organized, it is possible that some attention problems may be
because of deficits at the more elementary level of information
processing. For instance, Sturm, Willmes, Orgass, and Hartje
(1997,Sturm et al., 2004) showed that both attention orienting and
executive functioning in neurologically impaired patients could
benefit from exclusively training a lower level attention compo-
nent, the ability to prepare to process and react to high-priority
signals. Thus, this phasic alerting represents the lowest level of the
hierarchy, which is a prerequisite for higher functions, such as
orienting and executive functioning. This also lends support to the
This article was published Online First November 25, 2013.
George A. Michael, Laboratoire d’Étude des Mécanismes Cognitifs,
Université de Lyon (EA 3082), Université Lyon 2, Lyon, France; Sophie
Garcia, Service de Neurologie, Centre Hospitalier Lucien Hussel, Vienne,
France; Vania Herbillon, Epilepsie, sommeil et explorations fonctionnelles
neuropédiatriques, Hôpital Femme Mère Enfant, Lyon, France; Laurence
Lion-François, Service de Neurologie pédiatrique, Hôpital Femme Mère
Enfant, Lyon, France.
We thank Givors Primary School, France. This work was supported by
the LabEx CORTEX (ANR-11-LABX-0042) of Université de Lyon, within
the program “Investissements d=Avenir” (ANR-11-IDEX-0007) operated
by the French National Research Agency (ANR).
Correspondence concerning this article should be addressed to George
A. Michael, Université de Lyon, Université Lumière – Lyon 2, Laboratoire
d=Etude des Mécanismes Cognitifs, Département de Psychologie Cognitive
& Neuropsychologie, 5, Avenue Pierre Mendès-France, 69676 Bron Ce-
dex, France. E-mail: George.Michael@univ-lyon2.fr
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Neuropsychology © 2013 American Psychological Association
2014, Vol. 28, No. 3, 423–428 0894-4105/14/$12.00 DOI: 10.1037/neu0000046
423
idea that, at least in part, the brain structures subserving attention
are hierarchically arranged (Mesulam, 1999;Petersen & Posner,
2012;Posner & Petersen, 1990). Therefore, one might ask whether
some of the attention deficits described in NF1 stem from disrup-
tions in even more elementary components. The cross-modal na-
ture of attention deficits in NF1 is a sign they are not secondary to
difficulties with perceptual processing of particular types of stim-
uli (Isenberg et al., 2013). It is still possible, however, that prob-
lems with attention and executive functioning may be secondary to
weakened elementary attention components on which selective
attention and executive functioning rely. For instance, selective
attention, cognitive flexibility, and response inhibition could de-
pend on the capacity to interrupt ongoing activities to orient
attention toward potentially relevant environmental signals (Mi-
chael, Boucart, Degreef, & Godefroy, 2001a;Michael, Garcia,
Bussy, François-Lion, & Guibaud, 2009).
Having advance knowledge of a forthcoming target results in
recruiting attention to process that target without being distracted
by irrelevant stimuli (LaBerge, Auclair, & Siéroff, 2000). When
the target appears, attention is oriented toward its location, en-
gaged on it, and maintained on it while it is processed (Posner &
Petersen, 1990). If a task-irrelevant event occurs at the same time
as the appearance of the target, then it produces interference that
should be resolved quickly because of knowledge about the target.
If such an event occurs after the processing of the target has begun,
the presence and location of this event are coded (Posner, Inhoff,
Friedrich, & Cohen, 1987) by specific and early components that
generate excitatory impulses. If these impulses signal that the
event is sufficiently salient (Koch & Ullman, 1985), then reactions
are produced, such as a brief (i.e., phasic) alerting state and
subsequent interruption of the ongoing processing (Posner et al.,
1987) to allow for a brief exploration of the salient event (Michael
et al., 2001a;). Thus, efficient attentional control is not based only
on processes such as selection, inhibition, and higher executive
functioning. At the earliest level, there are components such as the
coding and localizing of sensory signals, which are purely percep-
tual components. They are followed by the establishment of the
salience of these signals and then the reactivity to these signals, the
existence of which is corroborated mostly through the performance
of brain injured patients (Michael et al., 2001a,2009;Michael &
Desmedt, 2004). This study therefore sets out to assess some of
these elementary components in NF1, on the basis of a simple
visual attention task that has been previously described (Michael et
al., 2009). The extreme ease with which this task can be carried out
suggests that it relies less on complex cognitive demands. It
assesses (a) reactivity to stimuli following a warning signal (i.e.,
phasic alerting), (b) reactivity to distractors occurring at the same
time as the target signals (i.e., distractions), and (c) reactivity to
distractors occurring sometime after the target (i.e., interruptions
of ongoing activities).
Method
The method was identical to the one already described in Mi-
chael et al. (2009).
Subjects
The control group consisted of 20 healthy children (10 boys and
10 girls) aged 7–13 (Mage ⫽9.7 ⫾1.8). The patient group
consisted of 20 children with NF1 (14 boys and 6 girls) also aged
7–13 (Mage ⫽9.2 ⫾1.9). The NF1 group had a mean IQ
performance score of 91 ⫾13.4 and a mean verbal IQ score of
97 ⫾13.7 (the IQ was measured with the Wechsler Intelligence
Scale for Children—Third Ed.; Wechsler, 1991). Their mean score
on the short form of the Conners’ Parent Rating Scale (CPRS-
short) was 14 ⫾6 (cutoff score ⫽15). Anatomical MRIs were
available for 18 cases. In 22% of cases the MRI revealed no
T2-weighted hyperintensities (T2H), whereas in the other cases,
such T2H were present in the cerebellum, thalamus, and basal
ganglia. All of the NF1 participants met the diagnostic criteria
defined by the National Institutes of Health Consensus Conference
(1988) and took part in this study before receiving medication. The
participants overall all had normal or corrected-to-normal vision,
and their parents had provided their written informed consent for
them to take part in the study. Ethical approval for the study was
granted by the CCPRB ethics committee of the Léon Bérard
Centre Régional de Lutte Contre le Cancer, Lyons, France.
Stimuli
The stimuli were 10 computerized black-and-white pictures
taken from Living English Structure for Schools (Stannard Allen,
1971), all portraying characters in various humorous situations.
The target was a white chicken, and the distractor a black cat, each
occupying an angular space of 5° ⫻5.7° at a viewing distance of
30 cm. To minimize perceptual confusion, different colors were
used for the target and distractor. All of the stimuli were displayed
within a virtual rectangle subtending an angular space of 27.7° ⫻
13.9°. The rectangle was centered on the fixation point. The
stimuli were displayed against the white background of a Dell
Latitude computer with a Pentium 200MHz processor.
Procedure
At the start of each trial a humorous scene was displayed for
1,500 ms, after which the chicken (i.e., the target) was added to the
left or right of the scene. Four conditions were tested: (a) the
distractor-absent condition, where the distractor (i.e., the cat) was
not present; (b) the ⫺300-ms distractor-present condition, where
the cat appeared 300 ms before the chicken; (c) the 0 ms distractor-
present condition, where the cat and chicken appeared simultane-
ously; and (d) the 300-ms distractor-present condition, where the
cat appeared 300 ms after the chicken. The distractor was always
positioned opposite the target (i.e., when the chicken was on the
left, the cat was on the right, and vice versa). Even though the
distractor may also act as a cue when presented before the target,
the term “distractor” is used throughout for convenience sake. The
display remained on the screen until a response was given, with the
next trial commencing 1,000 ms after the response. The four
conditions were presented in completely random order, and it was
not possible to predict where the target would be in each trial.
Subjects were asked to locate the target (left or right) as quickly
and as accurately as possible by hitting two predefined response
keys with the index finger of their right and left hand, respectively.
Response times (RTs) and errors were recorded by the computer
from when the target appeared. No feedback was given about each
trial. Each subject completed a session of 40 trials (10 trials per
condition). The test was preceded by a 10-trial training session.
The procedure is described in Figure 1.
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424 MICHAEL, GARCIA, HERBILLON, AND LION-FRANÇOIS
Indices and Statistical Analyses
Median RTs were subjected to a mixed analysis of variance
(ANOVA), with the tested condition (absent-distractor, distractor
at ⫺300 ms, 0 ms, and 300 ms) as within-subjects factor and group
(controls vs. NF1) as between-groups factor. Median RTs were
also used to extract three attention indices, each assessing different
components: (a) The alerting component was computed by sub-
tracting RTs recorded in the ⫺300-ms condition from RTs in the
distractor-absent condition (Michael et al., 2009). Phasic alerting
refers to greater readiness to respond to external stimuli soon after
a warning signal (Posner, 1978). In the ⫺300-ms condition, the
sudden prior appearance of the cat serves as a warning signal that
the target is imminent, helps orient attention in time, and speeds up
processing of the target once it is there. The inverse spatial
relationship between the target and distractor also provides infor-
mation about the location of the future target, making processing
even faster. (b) The difference between the 0-ms and ⫺300-ms
conditions denoted distraction (Michael et al., 2009). The overall
screen luminance in these two conditions is the same, but simul-
Figure 1. Trial events forming part of the experiment reported in this article. The stimuli shown are not actual
size. A humorous scene was displayed for 1,500 ms in the center of a computer screen. A target (white chicken)
was then added to the scene, and subjects were asked to locate it (to the right or left of the scene) by hitting two
predefined response keys. In some trials, the target was presented on its own, but in others it was accompanied
by a distractor to ignore (black cat). The target-to-distractor time interval varied systematically: The distractor
was displayed either before or after the target or even at the same time. The conditions tested were intermixed.
All of the stimuli were black and white. Response times were recorded from when the target first appeared. From
Living English Structure for Schools (p. 88), by W. S. Allen, 1971, Essex, UK: Pearson Longman. Copyright,
1971, by Pearson Longman. Adapted with permission.
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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
425
VISUAL ATTENTION IN NF1
taneous presentation of the target and distractor in the 0-ms con-
dition creates interference that slows RTs. Conversely, the prior
appearance of the distractor acts as a cue that speeds up RTs
because the position of the distractor interferes less with that of the
target (c). The brief interruption of ongoing activities, computed
by subtracting RTs recorded in the 300-ms condition from those
recorded in the ⫺300-ms condition (Michael et al., 2009)is
defined as the brief inspection of signals appearing during target
processing (Michael et al., 2001a). In the 300-ms condition, the
distractor appears 300 ms after the target, that is, after target
processing is presumed to have begun. The interference effects
generated by the distractor at these late stages can be attributed to
the inspection of changes during ongoing activities. The indices
were subjected to a mixed ANOVA, with index (alerting, distrac-
tion, interruption) as within-subjects factor and group (controls vs.
NF1) as between-groups factor.
Results
Median RTs
The main effect of group was significant, F(1, 38) ⫽10.7, p⬍
.002,
2
⫽.86. The NF1 group (705 ms) was slower than the
control group (554 ms). The main effect of condition was also
significant, F(3, 114) ⫽18, p⬍.0001,
2
⫽.13, as was the
Group ⫻Condition interaction, F(3, 114) ⫽2.9, p⬍.04,
2
⫽
.01, which was investigated with post hoc (Newman–Keuls) com-
parisons. Regarding the controls’ performance, their RTs were
faster in the ⫺300-ms condition (478 ms) than in any of the other
conditions (absent, 577 ms, p⬍.002; 0 ms, 571 ms, p⬍.001; 300
ms, 590 ms, p⬍.001), but no other difference was found. The
pattern of results for the NF1 group was slightly different. Whereas
their RTs were faster in the ⫺300-ms condition (621 ms) than in
the other conditions (absent, 697 ms, p⬍.007; 0 ms, 708 ms, p⬍
.006; 300 ms, 792 ms, p⬍.0001), they were also slower in the
300-ms condition than in the absent-distractor (p⬍.002) and the
0-ms conditions (p⬍.003). The results are shown in Figure 2A.
The mean error percentage was not analyzed in detail because it
was below 3% (controls, 0.88 ⫾1.7; NF1, 2.5 ⫾6.6) and many
cells contained 0 values.
Attention Indices
The main effect of group did not reach significance, F(1, 38) ⫽
0.1, p⬎.72,
2
⫽.05. However, the main effect of index was
significant, F(2, 76) ⫽4.5, p⬍.015,
2
⫽.63, because of higher
values for interruption (141 ms) than both alerting (87 ms, p⬍
.027) and distraction (89 ms, p⬍.013). No difference was found
between alerting and interruption (p⬎.92). The Group ⫻Index
interaction reached significance, F(2, 76) ⫽3.1, p⬍.05,
2
⫽.32.
Newman–Keuls post hoc comparisons showed that, for the con-
trols, the values of the indices were similar (alerting, 99 ms;
distraction, 92 ms; interruption, 111 ms; all ps⬎.66). For the NF1
group, interruption lasted longer (171 ms) than both alerting (76
ms, p⬍.018) and distraction (86 ms, p⬍.036), with no difference
found between alerting and distraction (p⬎.70). Finally, compar-
isons between the NF1 group and controls in respect of each index
revealed no difference as regards alerting (p⬎.85) and distraction
(p⬎.84), but the interruption index was higher in the NF1 group
(p⬍.043). The results are shown in Figure 2B.
The suggestion based on these results is that the NF1 group
reacts more strongly to visual signals appearing during attentive
processing of a target and, consequently, interrupts such process-
ing for longer. Thus, there is evidence of dissociable components
in NF1. This dissociation supposes decreased internal homogene-
ity through these basic components. And, indeed, Cronbach’s
Figure 2. Performance of controls (black symbols) and NF1 participants (white symbols) in a psychophysical
task which required them to locate (left-right) a target and ignore a distractor. Error bars represent 1 SEM.A:
Mean mdn response times (in ms) for locating the target in the absence of the distractor and when the distractor
appeared before, at the same time as, or after the target. B: Mean attention indices (in ms). C: Regression analysis
showing the difference between the NF1 and control participants in the linear link between distraction and
interruption.
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426 MICHAEL, GARCIA, HERBILLON, AND LION-FRANÇOIS
alpha coefficient was lower in NF1 (.55) than in controls (.83), and
the difference between them was significant (Fisher ztest ⫽1.69,
p⬍.046; Kim & Feldt, 2008). It is interesting that the dissociation
found between distraction and interruption lends support to the
idea that although both these conditions involve distractor process-
ing, they are based on different components (Michael et al., 2001a,
2009;Michael, Kleitz, Sellal, Hirsch, & Marescaux, 2001b). We
investigated the link between these two components further by
subjecting the distraction and interruption indices to a regression
analysis. Interruption predicted distraction in how the controls
performed (⫽.74, p⬍.0045) but not the NF1 group (⫽.09;
p⬎.43). The effect of group on regression slopes was significant,
F(1, 36) ⫽6.62, p⬍.015, suggesting distraction and interruption
are indeed dissociable because how they relate to each other differs
between the two groups. The results are shown in Figure 2C.
Discussion
We assessed some elementary attention components in NF1 by
measuring reactivity to task-irrelevant visual signals occurring at
varying temporal intervals from a target (Michael et al., 2001a,
2009). Apart from our finding of generally slower RTs by partic-
ipants with NF1, which are a hallmark of slowed information
processing overall (Huijbregts & de Sonneville, 2011;Rowbotham
et al., 2009), this study detected disturbed interruption of target
processing because of the appearance of a distractor. The results
suggest that some elementary components of attention can be
selectively disturbed without affecting the others and lead us to
believe that dysfunctions of more complex attentional processes
reported in NF1 may be because of such elementary disturbances.
Evidence for these conclusions stem from the longer raw RTs
recorded when the distractor occurred 300 ms after the target but
also from the increment in the interruption index. Sensory signals
entering the visual field may attract attention even if processing of
task-relevant information is in progress. Interruption reveals the
workings of a mechanism that is actively searching for important
changes occurring outside the current focus of attention. It in-
volves detecting and inspecting scene changes that might require
changes in attitude and is essential for adaptive and coherent
behavior (Michael et al., 2001a,2009). There may be major
consequences for attentive behavior if this component is disrupted.
For instance, reduced reactivity to sensory signals can mean what
happens in the surroundings of a target is ignored, a behavior
found in patients with lesions of the posterior thalamus (Michael et
al., 2001a) and cerebellum (Michael et al., 2009). Conversely,
heightened reactivity, such as those reported after damage to the
frontal lobe (Michael, Garcia, Fernandez, Sellal, & Boucart, 2006;
Michael et al., 2001b) and found in the performance of the NF1
participants in this study, could disrupt one’s ability to focus
attention and, in addition, create a weakened resistance to inter-
ference that could make it difficult to focus continuously on a
primary task. These are problems with which NF1 participants are
frequently characterized (e.g., Gilboa et al., 2011;North et al.,
2002;Templer, 2013).
From a theoretical point of view, there is strong evidence that
distraction and interruption of ongoing processing are independent
functions (Michael et al., 2009). However, there is also evidence
that they may be implemented within the same neural network
involving the reticular formation, thalamus, cerebellum, and right
ventral frontal cortex (Michael et al., 2001b). One interpretation is
that distinct parts of the same network support these distinct
components of attention. This study offers some supporting evi-
dence for this. The strong regression coefficient observed between
these distinct parts and components in the control participants
lends support to the idea that they are linked. In the NF1 group, the
dissociation between the normal distraction and disturbed inter-
ruption, as well as their weakened interrelation, suggest they are
independent of each other.
One limit of our study is that it does not directly rule out the
possibility that the performance of the NF1 participants reflects
just a delay in the development of the elementary attention com-
ponents under investigation. It was previously demonstrated that
these components assessed with our paradigm do not exhibit any
developmental pattern, at least not beyond age 8 years (Michael et
al., 2009). Consequently, the difference in the performance pattern
found in the NF1 group compared to the control group cannot be
attributed to delayed development. Another limit is that this study
does not reveal whether the heightened reactivity found in NF1 is
because of weakened focusing on the target or as a result of
increased salience of signals occurring in the surroundings of the
target, which are two distinct components (Michael & Desmedt,
2004;Theeuwes, 1991) that precede reactivity to sensory signals
(Michael et al., 2001a;Posner et al., 1987). Cognitive and com-
putational models (e.g., Koch & Ullman, 1985) assume that dif-
ferences between elementary visual features serve to determine the
degree at which an item of the visual field is salient compared with
the others and the degree at which visual attention should be
directed toward it. Heightened salience—which is an even more
elementary process than the ones assessed here—can account for
the results of our study. Future research on NF1 should be able to
better characterize such elementary components of attention that
condition interruption of ongoing activities, as well as the way and
the degree at which competing salient yet task-irrelevant events
produce interruptions.
Overall, not all elementary components on which attentive pro-
cessing is built are normal in participants with NF1. We found
overreactivity to, and longer inspection of, visual signals occurring
outside the current focus of attention. This may be partially re-
sponsible for difficulties in focusing attention and weakened re-
sistance to interference in controlled tasks but also for inattentive
and impulsive behavior in natural environments (Payne et al.,
2011).
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Received April 23, 2013
Revision received October 8, 2013
Accepted October 10, 2013 䡲
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