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Journal of

Clinical Medicine

Article
Specific Learning Disabilities and Emotional-Behavioral
Difficulties: Phenotypes and Role of the Cognitive Profile
Paola Cristofani 1 , Maria Chiara Di Lieto 1, * , Claudia Casalini 1 , Chiara Pecini 2 , Matteo Baroncini 1 ,
Ottavia Pessina 3 , Filippo Gasperini 1 , Maria Bianca Dasso Lang 1 , Mariaelisa Bartoli 1 , Anna Maria Chilosi 1
and Annarita Milone 1

1 Department of Developmental Neuroscience, IRCCS Fondazione Stella Maris, 56128 Pisa, Italy
2 Department of Education, Languages, Intercultures, Literatures and Psychology, University of Florence,
50121 Firenze, Italy
3 Department of Clinical and Experimental Medicine, University of Pisa, 56126 Pisa, Italy
* Correspondence: [email protected]; Tel.: +39-050886111

Abstract: Specific Learning Disabilities (SLD) are often associated with emotional-behavioral prob-
lems. Many studies highlighted a greater psychopathological risk in SLD, describing both inter-
nalizing and externalizing problems. The aims of this study were to investigate the emotional-
behavioral phenotype through the Child Behavior Checklist (CBCL), and evaluate the mediating
role of background and cognitive characteristics on the relationship between CBCL profile and learn-
ing impairment in children and adolescents with SLD. One hundred and twenty-one SLD subjects
(7–18 years) were recruited. Cognitive and academic skills were assessed, and parents completed the
questionnaire CBCL 6–18. The results showed that about half of the subjects manifested emotional-
behavioral problems with a prevalence of internalizing symptoms, such as anxiety and depression,
over externalizing ones. Older children showed greater internalizing problems than younger ones.
Males have greater externalizing problems compared to females. A mediation model analysis re-
Citation: Cristofani, P.; Di Lieto, vealed that learning impairment is directly predicted by age and familiarity for neurodevelopmental
M.C.; Casalini, C.; Pecini, C.; disorders and indirectly via the mediation of the WISC-IV/WAIS-IV Working Memory Index (WMI)
Baroncini, M.; Pessina, O.; Gasperini, by the CBCL Rule-Breaking Behavior scale. This study stresses the need to combine the learning and
F.; Dasso Lang, M.B.; Bartoli, M.; neuropsychological assessment with a psychopathological evaluation of children and adolescents
Chilosi, A.M.; et al. Specific Learning with SLD and provides new interpretative insights on the complex interaction between cognitive,
Disabilities and Emotional- learning, and emotional-behavioral phenotypes.
Behavioral Difficulties: Phenotypes
and Role of the Cognitive Profile. J. Keywords: specific learning disabilities; emotional-behavioral manifestation; child behavior checklist-
Clin. Med. 2023, 12, 1882. https://
CBCL; learning impairment; working memory; cognitive profile
doi.org/10.3390/jcm12051882

Academic Editor: Manuel A.


Franco-Martin
1. Introduction
Received: 24 January 2023
Revised: 20 February 2023 Specific Learning Disabilities (SLD) are neurodevelopmental disorders characterized
Accepted: 22 February 2023 by difficulties in reading, writing, and/or mathematics skills in parallel with average intelli-
Published: 27 February 2023 gence and adequate educational and sociocultural opportunities, which occur in the absence
of sensory, neurologic, or other psychiatric disorders [1]. On average, 5–15% of students are
diagnosed with SLD, such as Dyslexia, Dyscalculia, Dysgraphia, and Dysorthography [1].
SLD persist despite normal schooling and can interfere with school education and daily
Copyright: © 2023 by the authors. life by having an impact on academic achievement, relational experiences, and quality of
Licensee MDPI, Basel, Switzerland. life. Furthermore, SLD can be characterized by the coexistence of emotional and behavioral
This article is an open access article problems [2–7]. In fact, a relevant feature of SLD is comorbidity [8,9]: It frequently happens
distributed under the terms and
to encounter the coexistence not only of several types of SLD (“homotypic comorbid-
conditions of the Creative Commons
ity”), but also of other neurodevelopmental disorders or clinical conditions (“heterotypical
Attribution (CC BY) license (https://
comorbidity”) in the same subject [10].
creativecommons.org/licenses/by/
4.0/).

J. Clin. Med. 2023, 12, 1882. https://doi.org/10.3390/jcm12051882 https://www.mdpi.com/journal/jcm


J. Clin. Med. 2023, 12, 1882 2 of 15

The comorbidity between SLD and emotional-behavioral disorders is high: About 30%
of children with SLD have emotional and behavioral problems [11], whose phenomenol-
ogy can be very heterogeneous and is often described in terms of both internalizing and
externalizing disorders [12]. From an empirical point of view of child behavior classifica-
tion, anxiety, depression, social withdrawal, and somatic complaints are conceptualized
as internalizing problems, while disinhibited or externally-focused behavioral symptoms,
including aggression, conduct problems, rule breaking behavior, oppositionality, hyperac-
tivity, are conceptualized as externalizing problems [13]. For what concerns internalizing
symptoms, children with SLD show a higher rate of separation anxiety and generalized
and social anxiety compared to children who do not have SLD problems [6]. Moreover,
dyslexic children report higher levels of somatic symptoms [3] and depressive symptoma-
tology [14]. Regarding externalizing symptoms, both oppositional defiant [15] and conduct
disorders [16] have been reported in SLD. However, the highest comorbidity is with Atten-
tion Deficit Hyperactivity Disorder (ADHD) [17,18], occurring between 25% and 45% of
SLD cases [19,20].
The interaction between emotional-behavioral functioning and learning difficulties is
very complex and its explanation calls into question several hypotheses.
The association between SLD and emotional-behavioral disorders can be traced back
to a causal role of the former on the latter (e.g., school failure causes emotional distress in
the student) but also of the latter on the former (e.g., a subject with emotional-behavioral
problems does not work hard in learning tasks, caused by different factors, such as reduced
motivation, low tolerance to frustration or resistance to stress, impulsiveness). Therefore,
SLD can be hypothesized as a risk factor for high levels of internalizing and externalizing
symptoms, which might be considered a consequence of SLD themselves, deriving from
the impact of the disorder on the mental health of SLD subjects [21]. Moreover, emotional-
behavioral disorders can be hypothesized as a risk factor for SLD too.
However, the concept of comorbidity contemplates the idea that different clinical
conditions arise together without any causal link between them and may be the expression
of a more general malfunction that shares a common neuropsychological substrate. In
this regard, the hypothesis of the “Multiple Deficit Model” [21] suggests that disorders
are linked together by multiple factors, some specific to a given disorder while others
are in common, and they can derive from the interaction between several risk factors [8].
Indeed, the interaction between SLD and emotional-behavioral problems seems mediated
by a series of biological, cognitive, and environmental factors that document the role of
many distinct and shared aspects. Willcutt and Pennington [3] found a close relationship
between reading disorders and externalizing disorders in males, while females show
more internalizing symptoms and, specifically, they report more depressive and somatic
symptoms than males. The association between SLD and emotional difficulties seems to
be mediated also by age: For example, Giovagnoli and colleagues [22] found higher levels
of internalizing symptoms in schoolers with developmental dyslexia, specifically, school
anxiety in those children who attended secondary school compared to the primary ones.
The age of diagnosis also influences the emotional-affective aspect. An early diagnosis
allows the activation of more effective coping strategies for the disorder with positive effects
on self-esteem and sense of self [23]. The absence of an adequate diagnosis represents a
negative aspect as the person reports a sense of inability [24]. Evidence in the literature
shows that children identified later as dyslexics report greater feelings of low self-esteem
and fear of judgment [25]. At the same time, self-esteem seems to be higher in the presence
of an early diagnosis of dyslexia [26].
Furthermore, there are still relatively few studies investigating the relationship be-
tween the cognitive and neuropsychological profile and the presence of internalizing and
externalizing symptoms in SLD. Mugnaini and collaborators [27] report that a border-
line cognitive level in subjects with dyslexia represents a risk factor for the presence of
internalizing problems. Some further studies examined the association between cogni-
tive profile and emotional difficulties in poor reader children without a clear diagnosis
J. Clin. Med. 2023, 12, 1882 3 of 15

of SLD. Nachshon and Horowitz-Kraus [28] demonstrated the relationship between low
reading scores, emotional abilities, and executive functions (such as speed of processing,
inhibition, visual attention, and switching abilities). Another cognitive factor mediating the
interaction between SLD and emotional-behavioral problems is the presence of language
impairment (assessed in 20% of preschool-aged children with reading disorders) [29]. It
is well-known that language disorders, besides being a risk factor for the development of
literacy difficulties [30,31], seem to be a precursor for the development of emotional and
behavioral problems [32–35].
Moreover, some studies report that even the extent of learning difficulties could be
associated with different manifestations of emotional-behavioral difficulties. Prior and
collaborators [12] found that impairment of a single learning domain is usually associated
with internalizing disorders, while the presence of impairment of multiple learning domains
is more frequently associated with externalizing disorders.
In summary, the interaction between emotional-behavioral functioning and learning
difficulties in SLD could be complex and affected by multiple risk factors. Thus, further
investigations are needed in order to shed light on the characteristics of the emotional-
behavioral disorders in subjects with SLD and on the mediator role of several other factors,
such as cognitive and background factors. Specifically, it would be appropriate to better
understand how these factors influence the relationship between emotional and behavioral
clinical manifestations and learning disorders. Such knowledge will allow better under-
standing of the symptom manifestation and severity of the clinical picture of children with
SLD to better support the clinical management of these disorders [10,36].
Our study is part of this line of research with a dual purpose: (a) To describe the
psychopathological profile of a clinical sample of subjects with SLD, (b) to investigate the
mediator role of sex, age, and cognitive indices on the relationship between emotional and
behavioral manifestations and learning impairment in children and adolescents with SLD.
According to the literature, we hypothesize individuals with SLD show more internalizing
than externalizing problems. Furthermore, regarding individual background factors, based
on previous studies, we expect that males have more externalizing symptoms than females
and that older age is associated with more internalizing symptoms.

2. Materials and Methods


2.1. Participants
The study included 121 subjects (73 males and 48 females, age range: 7–18 years, mean
age: 11.9 ± 3.03 years) with SLD diagnosis, in accordance with the international diagnostic
classification criteria [1,37] and the Italian Clinical Recommendations on SLD [38], recruited
from the Specific Learning Disorder Reference Centre of the Stella Maris Foundation
Hospital (Pisa, Italy). The recruitment of participants was conducted within the standard
clinical care of the service, and no additional compensation was required.
Criteria for participants’ inclusion [1,38] were: (i) Age between 7 and 18 years old,
(ii) second grade of primary school onward, (iii) absence of severe hearing and/or visual
deficits, epilepsy, cerebral palsy, encephalitis or other major neurological abnormalities or
neurodevelopmental disorders such as autism spectrum disorder, intellectual disabilities,
and genetic syndromes.
All the selected subjects had the following results at the assessment carried out with
standardized instruments:
• Both Perceptual Reasoning Index (PRI) and Verbal Comprehension Index (VCI) at the
WISC-IV or WAIS-IV intelligence scales [39–42] within 1.5 standard deviation (SD)
from the mean;
• A deficient score (z score ≤−2 or percentage rank ≤5◦ ) in at least two reading aloud
tests and/or dictation test and/or mathematics test.
Based on DSM-5 criteria, SLD can affect one or more of the following academic do-
mains: Reading decoding, as in the case of Developmental Dyslexia, written expression
or mathematics, as in the case of Developmental Dysorthography or Dyscalculia, respec-
J. Clin. Med. 2023, 12, 1882 4 of 15

tively [1]. When mathematics difficulties were associated with both reading and spelling
disorders, usually the most frequently encountered in clinical practice, a diagnosis of
“Mixed Disorder of Scholastic Skills” was given [43].
Age of first diagnosis ranged from about 7 to 18 years and correlated with chronologi-
cal age (r(120) = 0.72, p < 0.001), indicating that the older subjects examined in the study
were being diagnosed for the first time, receiving a later diagnosis. Forty-nine percent of the
participants were attending primary school (third, fourth, and fifth grade), 27% the middle
school, and 24% high school. Twenty-two percent of children (26/121) had a previous
psychopathological diagnosis: 10 children (8%) presented ADHD, 14 children had anxiety
or depressive problems, and for 2 children the emotional-behavioral problems were not
specified. All subjects were native Italian speakers of Caucasian ethnicity. This research
project was approved by the Paediatric Ethics Committee of Tuscany. All parents gave
written consent for their son or daughter’s participation and for publication of the results.

2.2. Assessment Procedure


Parents completed the Child Behavior Checklist (CBCL) [44,45], an anamnestic inter-
view and a questionnaire on early development [46].
Each child was individually assessed by intelligence and learning tests in a quiet room
with adequate lighting and a comfortable seat.

2.2.1. Child Behavior Checklist (CBCL)


The presence and type of emotional and behavioral problems were explored through
the Italian version of the CBCL [47–49]. It is a standardized scale of 118 items to be
completed by the parents of children and adolescents aged between 6 and 18 years.
Each item was scored on a 3-step response scale (completely agree, I do not know, com-
pletely disagree) and the items were aggregated in 8 main syndrome subscales (Anx-
ious/Depressed, Withdrawn/Depressed, Somatic Complaints, Social Problems, Thought
Problems, Attention Problems, Rule-Breaking Behaviors, Aggressive Behaviors) and six
DSM-oriented sub-scales (Affective Disorder, Anxiety Disorder, Somatic Problems, Atten-
tion Deficit/Hyperactivity Problems, Oppositional Defiant Problems, Conduct Problems).
All raw scores for each CBCL scale and subscale were expressed as T scores (mean:
50; SD: 10) with respect to the age and sex norms using Achenbach’s normative data [44].
T-scores below 64 were considered normal, those between 65 and 69 in the borderline range,
and those higher than 70 were in the clinical range. Three composite syndrome scales were
also computable: Internalizing scale (sum of Anxious/Depressed, Withdrawn/Depressed,
and Somatic Complaints), Externalizing scale (sum of Aggressive Behavior and Rule-
Breaking Behavior), and Total Problem scale (sum of all syndrome subscales). For all
composite scales, T-score ranges for all composite scales were as follows: Below 59 was
considered normal, between 60 and 63 was borderline, and higher than 64 was clinical.
Moreover, the Child Behavior Checklist Dysregulation Profile (CBCL-DP) was assessed
using the sum of T-scores of the following CBCL subscales: Anxious/Depressed, Attention
Problems, and Aggressive Behavior syndrome [45,50]. The combination of behavioral,
affective, and cognitive dysregulation measured by the CBCL-DP was associated with an
increased likelihood of psychopathology and psychosocial impairment in childhood [51].
The clinical CBCL-DP score range was ≥210.

2.2.2. Intelligence
The Wechsler Intelligence Scale for Children–Fourth Edition (WISC-IV) [39] and the
Wechsler Intelligence Scale for Adults–Fourth Edition (WAIS-IV) [40] were administered to
evaluate the subjects’ cognitive profiles. The scales provided a full-scale IQ (FIQ) and four
composite scores relating to specific cognitive abilities: (a) The Verbal Comprehension Index
(VCI) measured the use and understanding of language and evaluated abstraction skills,
generalization, practical reasoning, and long-term memory recovery, (b) the Perceptual
Reasoning Index (PRI) assessed nonverbal reasoning and problem-solving and the ability
J. Clin. Med. 2023, 12, 1882 5 of 15

to collect, organize, and interpret visual data to solve complex cognitive problems, (c) the
Working Memory Index (WMI) measured subject’s ability to recall and manipulate auditory
information in short-term memory, (d) the Processing Speed Index (PSI) included timed
activities that required the analysis of visual material, visual perception, and visual scanning
and hand-eye coordination. Normative data and psychometric properties for the Italian
population are available [41,42].

2.2.3. Academic Abilities


The academic abilities were assessed by reading decoding and comprehension, writing,
and arithmetic tests described below.
Reading decoding was individually evaluated through tests of reading aloud a passage
with a 4-min time limit [52–54], and words and non-words [54,55]. In each test, both
decoding speed (i.e., in syllables for second), later expressed as z scores with reference to
normative values, and accuracy (i.e., number of errors), converted to percentile rank, were
computed and converted on a 3-point scale (Deficient, Borderline and Normal).
Reading comprehension was assessed through a text comprehension test, in which
the subject had to answer 10 multiple-choice questions, each with four alternatives, after
reading a story silently with no time limit [52–54]. The number of correct responses was
transformed into ordinal scores on a 4-point scale (Deficient, Borderline, Within Average,
and Optimal) based on normative values.
As for writing skills, they were investigated through the writing under dictation of a
brief passage [54,56] and of twelve sentences containing words with unpredictable spelling
only on the basis of Italian phoneme-to-grapheme correspondence rules [55]. For each
test, the total number of spelling errors was computed and converted to a percentile rank
according to normative value. Each percentile rank was transformed into an ordinal score
on a 3-point scale (Deficient, Borderline, and Normal).
Finally, also arithmetic abilities were evaluated through standardized tests [54,57]. For
each test, we converted the scores to a percentile rank according to normative value and
transformed them into ordinal scores on a 3-point scale (Deficient, Borderline, and Normal).

2.3. Statistical Analysis


Statistical Package for Social Sciences, version 22.0 (IBM SPSS Statistics, IBM Corpo-
ration, Armonk, NY, USA) was used for statistical analyses. For missing data, case-wise
deletion was applied.
Given the use of ordinal scales for the academic tests, the learning profile, and the
effect of familiarity for neurodevelopmental disorder, SLD type, and sex were investigated
through the non-parametric Mann–Whitney and Wilcoxon tests. Accordingly, the relation
between performances at the academic tests and chronological age was investigated by
non-parametric Spearman correlation.
Because of only moderate deviations from normality for the WISC-IV indices and the
CBCL scales (value for both skewness and kurtosis were between −1 and +1 for each of
these variables, with only 1 exception out of 19) [58] and the “robustness” of the ANOVA to
non-normality of data distribution [59], parametric analyses were performed. Sphericity of
data was evaluated through Muchly’s test, and in those cases where it was not confirmed,
Epsilon correction on degrees of freedom of both numerator and denominator was adjusted
in order to maintain the F statistic valid.
The presence of discrepancies within the cognitive and psychopathological profile,
respectively, was investigated by descriptive statistics and repeated Measures ANOVAs,
with Bonferroni post-hoc corrections for multiple comparisons on the Wechsler indices and
the CBCL scales and subscales.
The effect of sex, familiarity for neurodevelopmental disorder, and SLD type on the
scores at the Wechsler and CBCL scales and subscales was assessed through a series of
between-groups ANOVAS. In order to account for potential inflation of the Type I error,
Bonferroni adjusted alpha levels were used for each set of comparisons. For each of
J. Clin. Med. 2023, 12, 1882 6 of 15

the performed ANOVAs, the effect size for the independent variable was measured by
calculating Partial Eta Squared statistics.
Parametric correlation (Pearson) and regression analyses were used to investigate
whether demographic and cognitive scores correlated and predicted inter-subject variability
at the CBCL and learning profiles.
Based on the results from the regression analysis, we tested a mediation model (SPSS;
Process v. 4.0, Model 4) on the relationship between the main background, cognitive,
learning, and emotional-behavioral variables.

3. Results
3.1. Academic and Cognitive Profile
Descriptive statistics of the score range obtained at the academic test are reported in
Table 1. The SLD type included Developmental Dyslexia and/or Dysorthography (51%,
62/121), Developmental Dyscalculia (6%, 8/121), and Mixed SLD (42%, 51/121). The group
with Mixed SLD showed a higher (z = −5.65, p < 0.001) median impairment than the groups
with isolated SLD (Dyslexia, Dysorthography, or Dyscalculia).
Table 1. Descriptive statistics of the score range (1, Normal, 2, Borderline, 3 Deficient) obtained at the
academic tests.

Text Compre- Sentences


Text Decoding Text Decoding Text Dictation Math
hension Dictation
Accuracy Speed Accuracy Quotient
Accuracy Accuracy
Median 2 3 2 3 2 2
Interquartile
2 1 1 1 1 1
Differences

Cognitive characteristics of the SLD sample are reported in Table 2. Missing data
concern the cognitive assessment conducted in another clinical center. In particular, all
cognitive scores for three subjects, the WMI and PSI scales for three children, and the CVI
scale for one child were not available.
Table 2. Cognitive profile at the Wechsler scales.

N Minimum Maximum M SD
VCI 117 70 124 98.90 11,724
PRI 118 65 141 101.58 13,145
WMI 115 55 115 84.83 13,543
PSI 115 53 138 90.99 13,646
Legend: WISC-IV descriptive statistics of the sample of subjects. VCI: Verbal Comprehension Index; PRI: Percep-
tual Reasoning Index; WMI: Working Memory Index; PSI: Processing Speed Index.

A significant difference across WISC-IV indices was found (F(3, 339) = 49.52, p < 0.001),
with a large effect-size (Partial Eta Squared = 0.30). Post-hoc analyses revealed the ab-
sence of significant differences between VCI and PRI, while significant better performances
were found for both VCI and PRI with respect to both WMI and PSI (p < 0.05). A sig-
nificant difference between WMI and PSI was also found in favor of the latter (p < 0.05)
(VCI = PRI > PSI > WMI). In the appendix (Table S1), t statistics for Bonferroni post-hoc
corrections are reported.
Accordingly, borderline (<85) or deficient (<70) indexes were recorded in 53% of the
sample at the WMI, 43% at the PSI, 12% at the VCI, and 6% at the PRI.

3.2. Behavioral and Emotional Characteristics


As shown in Figure 1, scores in the Internalizing syndrome scale were significantly
higher than in the Externalizing syndrome scales (t(120) = 7.69, p < 0.001). Five percent
corrections are reported.
Accordingly, borderline (<85) or deficient (<70) indexes were recorded in 53% of the
sample at the WMI, 43% at the PSI, 12% at the VCI, and 6% at the PRI.

3.2. Behavioral and Emotional Characteristics


J. Clin. Med. 2023, 12, 1882 7 of 15
As shown in Figure 1, scores in the Internalizing syndrome scale were significantly
higher than in the Externalizing syndrome scales (t(120) = 7.69, p < 0.001). Five percent
(6/121) of the children presented CBCL DP scores within the clinical range. Partial Eta
(6/121)was
Squared of the
0.33,children presented
indicating CBCLsize
a large effect DP for
scores within the
the general clinical
type range. Partial Eta
of symptoms.
Squared was 0.33, indicating a large effect size for the general type of symptoms.

Figure 1. (a) Mean and Standard Deviation of T scores in each CBCL syndrome composite scale, * rep-
resent1.the
Figure (a) statistical
Mean andsignificant
Standard differences (pT< scores
Deviation of 0.05) between
in each CBCL syndrome
syndrome scales; (b) scatterplot
composite scale, *
represent the statistical
distribution significant
of Internalizing differences
(black) (p<.05) between
and Externalizing CBCL syndrome
(gray) Problems scales. scales; (b) scatter-
plot distribution of Internalizing (black) and Externalizing (gray) Problems scales.
Forty-eight percent of the children (58/121) showed borderline or clinical range scores
in one or both CBCL
Forty-eight syndrome
percent composite
of the children scales.
(58/121) Specifically,
showed on the
borderline orInternalizing
clinical rangesyndrome
scores
in scale,
one or33%
bothofCBCL
the children
syndrome(40/121) had scores
composite scales.inSpecifically,
the borderline (7/40)
on the or clinicalsyn-
Internalizing range
(33/40).
drome On33%
scale, the Externalizing
of the children syndrome scale,scores
(40/121) had 16% ofinthe
thechildren (20/121)
borderline (7/40)had scores in
or clinical
the borderline
range (33/40). On (12/20) or clinical (8/20)
the Externalizing range. scale, 16% of the children (20/121) had
syndrome
On the Total Problem syndrome scale,
scores in the borderline (12/20) or clinical (8/20) 22%range.
(27/121), showed clinical and 12% (15/121)
borderline range scores.
A significant difference across the eight syndrome subscales was found (F(6, 672) = 28.32,
p < 0.001) in the CBCL syndrome subscales. Partial Eta Squared was 0.14, indicating a large
effect size. Post-hoc comparisons revealed that Anxious/Depressed, Withdrawn/Depressed,
and Social Problems subscales had significantly higher scores than the Thought Problems,
Rule Breaking Behavior, and Aggressive Behavior subscales (p < 0.05).
The Attention Problem subscale had significantly higher scores than Rule-Breaking
Behavior and Aggressive Behavior subscales (p < 0.05) (Anxious/Depressed = With-
drawn/Depressed = Social Problems > Thought Problems = Rule Breaking Behavior =
Aggressive Behavior, Attention Problem > Rule Breaking Behavior = Aggressive Behavior).
In the appendix (Table S2), t statistics for Bonferroni post-hoc corrections are reported.
Accordingly, as shown in Figure 2, scores in the borderline or clinical range were found
in 19% (23/121) of the patients in the Anxious/Depressed subscale, 15% (18/121) in the
Withdrawn/Depressed, 15% (18/121) in the Attention Problems subscale, 12% (14/121) in
The Attention Problem subscale had significantly higher scores than Rule-Breaking
Behavior and Aggressive Behavior subscales (p < 0.05) (Anxious/Depressed = With-
drawn/Depressed = Social Problems > Thought Problems = Rule Breaking Behavior = Ag-
gressive Behavior, Attention Problem > Rule Breaking Behavior = Aggressive Behavior).
In the appendix (Table S2), t statistics for Bonferroni post-hoc corrections are reported.
J. Clin. Med. 2023, 12, 1882 Accordingly, as shown in Figure 2, scores in the borderline or clinical range8were of 15
found in 19% (23/121) of the patients in the Anxious/Depressed subscale, 15% (18/121) in
the Withdrawn/Depressed, 15% (18/121) in the Attention Problems subscale, 12% (14/121)
in Somatic
the the Somatic Complaints,
Complaints, 11% (13/121)
11% (13/121) in the Problems,
in the Social Social Problems, 10% in
10% (12/121) (12/121) in the
the Thought
Thought Problems subscales, 4% (5/121) in the Rule Breaking Behaviors, and
Problems subscales, 4% (5/121) in the Rule Breaking Behaviors, and 3% (4/121) in the 3% (4/121)
in the Aggressive
Aggressive Behaviors
Behaviors subscales.
subscales.

20
18
16
14
% of subjects 12
10
8
6
4
2
0

Figure2.2.%%of
Figure ofscores
scoresin
inthe
theborderline
borderline(64–69)
(64–69)ororclinical
clinical(>70)
(>70)range
rangeatatthe
thesyndrome
syndromesubscales.
subscales.

AAsignificant
significantdifference
difference across
across the the DSM-oriented
DSM-oriented sub-scales
sub-scales emerged
emerged (F(4,= 468)
(F(4, 468) 27.20,=
27.20, p < 0.001), with a large effect-size (Partial Eta Squared = 0.18). Post-hoc
p < 0.001), with a large effect-size (Partial Eta Squared = 0.18). Post-hoc comparisons comparisons
revealedthat
revealed thatAnxiety
AnxietyProblem
Problemsubscale
subscaleshowed
showed significantly
significantly higher
higher scores
scores than
than all
allthe
the
othersubscales
other subscales(p(p<<0.05),
0.05),Affective
AffectiveProblem
Problemsubscale
subscalemean
meanscore
scorewaswassignificantly
significantlyhigher
higher
than the
than the mean scores
scores in in Somatic
SomaticProblems
Problems(p(p< < 0.05), Oppositional
0.05), Oppositional Defiant Problems
Defiant Problems(p <
(p0.05), and and
< 0.05), Conduct Problems
Conduct (p < 0.05)
Problems (p <subscales. Attention
0.05) subscales. Deficit/Hyperactivity
Attention Problem
Deficit/Hyperactivity
Problem
subscale subscale had significantly
had significantly higher scoreshigher
thanscores than Oppositional
Oppositional Defiant ProblemsDefiant(p <Problems
0.05) and
(pConduct
< 0.05) Problems
and Conduct Problems
(p < 0.05) (p < (Anxiety
subscales 0.05) subscales
Problem (Anxiety Problem
> all subscales, > all subscales,
Affective Problem
Affective
> Somatic Problem
Problem > Somatic ProblemDefiant
= Oppositional = Oppositional
Problems Defiant Problems
= Conduct = Conduct
Problems, Problems,
Attention defi-
Attention deficit/Hyperactivity
cit/Hyperactivity problem >Defiant
problem > Oppositional Oppositional
Problems Defiant Problems
= Conduct = Conduct
Problems). In the
Problems). In theS3),
appendix (Table appendix (Table
t statistics S3), t statistics
for Bonferroni for corrections
post-hoc Bonferroni are post-hoc corrections
reported.
are reported.
At DSM-oriented sub-scales, scores in the borderline or clinical range were found in
25%At DSM-oriented
(30/121) of patientssub-scales,
in Anxietyscores
Problemsin the borderline
subscale, 15% or clinical
(18/121) in range were found
the Affective Prob-
in 25% (30/121) of patients in Anxiety Problems subscale, 15%
lem, 11% (13/121) Attention Deficit/Hyperactivity problem subscales, 7% (8/121) (18/121) in the Affective
Somatic
Problem, 11% (13/121)
Problem subscale, Attention
3% (4/121) Deficit/Hyperactivity
in Conduct problem
Problem Oppositional, subscales,
and 3% (4/121) 7%in(8/121)
Defiant
Somatic
Problems Problem subscale,
sub-scales (Figure 3%3).(4/121) in Conduct Problem Oppositional, and 3% (4/121)
in Defiant Problems sub-scales (Figure 3).

3.3. Relationships and Interactions among the Background, Learning, Cognitive, and
Emotional Characteristics
3.3.1. Relationship with the Background Characteristics
Sex did not affect learning scores, either in terms of the median score of impairment or
the number of impairments across measures (z < 1, n.s.). Age significantly correlated with
the median impairment score (rho(121) = −0.19, p = 0.02) as higher age corresponded to
lower impairment. The group with a positive familiarity for neurodevelopmental disorders
(26/121, 22%) showed a higher median impairment than that one with a negative familiarity
(z = −2.4, p < 0.05).
No effects of sex, age, or familiarity for neurodevelopmental disorders were found on
the cognitive indexes.
J. Clin. Med. 2023, 12, 1882 9 of 15
J. Clin. Med. 2023, 11, x FOR PEER REVIEW 9 of 16

Figure 3. % of scores in the borderline (64–69) or clinical (>70) range at the DSM-5 oriented sub-
Figure 3. % of scores in the borderline (64–69) or clinical (>70) range at the DSM-5 oriented sub-scales.
scales.
Regarding the CBCL scores, worse scores were found in males than females in the At-
3.3. Relationships
tentional Problemsand Interactions
(F(1, 121) = 7.1,among the Background,
p < 0.001) Learning,
and Rule-Breaking Cognitive,
Behaviors and121)
(F(1, Emotional
= 6.08,
Characteristics
p < 0.01) CBCL subscales. No significant effect of familiarity for neurodevelopmental
3.3.1. Relationship
disorders was found with the Background
on any CBCL scalesCharacteristics
and subscales. Higher scores at the Withdraw,
SomaticSex did not affect learning scores, either were
Complaints, and Internalizing scales associated
in terms with higher
of the median score chronological
of impairment
age (r ranging from 0.18 to 0.26, p < 0.05).
or the number of impairments across measures (z < 1, n.s.). Age significantly correlated
with the median impairment score (rho(121) = −0.19, p = 0.02) as higher age corresponded
3.3.2. Relationship with the Cognitive Profile
to lower impairment. The group with a positive familiarity for neurodevelopmental dis-
Subjects
orders with
(26/121, 22%)Mixed
showedSLDa higher
showedmedian
lower impairment
scores in the intelligence
than indexes,
that one with with
a negative
the exception
familiarity (z =of−2.4,
PRI,p than those with an isolated SLD (IQ: F(1, 113) = 17.3, p < 0.001;
< 0.05).
VCI: F(1, 113) = 10.4, p
No effects of sex, age, or PRI:
< 0.005; F(1, 113)
familiarity for =neurodevelopmental
3.11, ns; WMI: F(1, 113) p < 0.001;
= 12.9,were
disorders found
PSI: F(1, 113) = 8.02,
on the cognitive indexes.p < 0.01). Regression analysis, with Intelligence Indexes (VCI, PRI,
WMI, PSI) as predictors and median learning impairment as outcome variable, showed
Regarding the CBCL scores, worse scores were found in males than females in the
that the intelligence profile of the child significantly predicted the learning impairment
Attentional Problems (F(1, 121) = 7.1, p < 0.001) and Rule-Breaking Behaviors (F(1, 121) =
(R2 = 0.34, F(4, 113) = 3.7, p < 0.001), although only the WMI resulted in being a significant
6.08, p < 0.01) CBCL subscales. No significant effect of familiarity for neurodevelopmental
predictor (beta = −0.24, t = −2.41, p < 0.005).
disorders was found on any CBCL scales and subscales. Higher scores at the Withdraw,
Correlational analysis between Intelligence Indexes (i.e., VCI, PRI, WMI, PSI) and
Somatic Complaints, and Internalizing scales were associated with higher chronological
CBCL scores showed a significant relationship between WMI and scores in the Rule-
age (r ranging from 0.18 to 0.26, p < 0.05).
Breaking subscale (r = −0.30, p < 0.001).
Based on the obtained results, a mediation model analysis was run on the median
3.3.2. Relationship with the Cognitive Profile
learning impairment as a dependent variable. As shown in Figure 4, learning impairment
Subjects
is predicted bywith Mixed
age and SLD showed
familiarity lower scores in the intelligence
for neurodevelopmental disorders and,indexes, withvia
indirectly, the
exception
the mediationof PRI, than
of the those with
Working Memoryan isolated
Index by SLD
the(IQ: F(1, 113) = 17.3,
Rule-Breaking p < 0.001;
Behavior scale.VCI: F(1,
113) = 10.4, p < 0.005; PRI: F(1, 113) = 3.11, ns; WMI: F(1, 113) = 12.9, p < 0.001; PSI: F(1, 113)
= 8.02, p < 0.01). Regression analysis, with Intelligence Indexes (VCI, PRI, WMI, PSI) as
predictors and median learning impairment as outcome variable, showed that the intelli-
gence profile of the child significantly predicted the learning impairment (R2 = 0.34, F(4,
113) = 3.7, p < 0.001), although only the WMI resulted in being a significant predictor (beta
= −0.24, t = −2.41, p < 0.005).
Correlational analysis between Intelligence Indexes (i.e., VCI, PRI, WMI, PSI) and
CBCL scores showed a significant relationship between WMI and scores in the Rule-
Breaking subscale (r = −0.30, p < 0.001).
Based on the obtained results, a mediation model analysis was run on the median
learning impairment as a dependent variable. As shown in Figure 4, learning impairment
is predicted by age and familiarity for neurodevelopmental disorders and, indirectly, via
the mediation of the Working Memory Index by the Rule-Breaking Behavior scale.
J. Clin. Med. 2023, 11, x FOR PEER REVIEW 10 of 16
J. Clin. Med. 2023, 12, 1882 10 of 15

Figure 4. A mediation model analysis on the relationship between background, cognitive, and CBCL
Figure 4. Aon
variables median model
mediation learning impairment
analysis on the(Indirect effect:
relationship BootLLCI
between = 0.0057; cognitive,
background, BootULCIand= 0.03306).
CBCL
variables on median learning impairment (Indirect effect: BootLLCI = 0.0057; BootULCI = 0.03306).
4. Discussion
Specific Learning Disabilities (SLD) are clinical conditions in which difficulties in
4. Discussion
specific academic areas (reading, writing, and/or mathematics) present high comorbidity
Specific Learning Disabilities (SLD) are clinical conditions in which difficulties in spe-
with emotional-behavioral disorders. In the literature, the presence of psychopathological
cific academic areas (reading, writing, and/or mathematics) present high comorbidity
difficulties in subjects with SLD varies from about 30% [11] to 70% [60]. The presence
with emotional-behavioral disorders. In the literature, the presence of psychopathological
of emotional-behavioral problems in SLD could be associated with a series of biological,
difficulties in subjects with SLD varies from about 30% [11] to 70% [60]. The presence of
cognitive, and environmental factors, such as the severity of symptomatology, the late
emotional-behavioral
diagnosis, the cognitive problems in SLDthe
level border, could
age,beand
associated
the male with
sexa[3,22,24,27].
series of biological,
However, cog-the
nitive,
number andofenvironmental
studies examining factors,
these such as the
aspects is severity
scarce, thusof symptomatology,
the type of relationshipthe late diag-
between
nosis,
thesethe cognitive
factors and the level border,ofthe
presence age, and the
internalizing andmale sex [3,22,24,27].
externalizing symptomsHowever, the num-
in subjects with
ber of studies examining
SLD have to be further investigated. these aspects is scarce, thus the type of relationship between
these factors
This studyand wasthe presence
aimed at of internalizing
investigating theand externalizing
presence and thesymptoms
typology ofinemotional
subjects
with SLD have to be further investigated.
and behavioral problems in a sample of subjects with SLD and the factors mediating
the This study was
relationship aimedlearning
between at investigating
impairment the presence and the typologysymptoms.
and psychopathological of emotional For
and behavioral problems in a sample of subjects with SLD and
this purpose, we described the psychopathological profiles at the CBCL [44,45] and their the factors mediating the
relationship
relation withbetween
cognitive, learning
learning, impairment
and background and psychopathological
variables in a sample symptoms. For this
of 121 children and
purpose, we described
adolescents with SLD. the psychopathological profiles at the CBCL [44,45] and their rela-
tion with Thecognitive,
profiles foundlearning,withinandthe background variables in
learning, cognitive, a sample
and of 121 children areas
emotional-behavioral and
adolescents
confirmed with SLD.
and extended the results of previous studies. Regarding the learning profile,
Theconfirmed
it was profiles found within the
that subjects withlearning,
Mixed SLD cognitive, and emotional-behavioral
or familiarity for neurodevelopmental areas
confirmed
disorders and had extended
higher median the results of previous
impairment studies.
than those with Regarding
isolated SLDthe learning
disorder profile,
or absence it
was confirmed[17,61].
of familiarity that subjects with Mixed
In addition SLD or
to previous familiarity
results, it wasfor neurodevelopmental
found that age was related dis-to
orders
learning hadimpairment,
higher median impairment
as the than those
younger subjects with isolated
showed SLD disorder iforcompared
worse performances absence
oftofamiliarity
the older ones.[17,61].Given
In addition
that into previous
the presentresults, it was
study, the found that age
chronological ageswas related toto
correspond
learning
the age impairment,
of first diagnosis,as thethis
younger
result subjects
suggestsshowed worsewith
that subjects performances if compared
milder symptoms to
require
the olderconsultation
clinical ones. Given later. that in the present study, the chronological ages correspond to the
age of Concerning
first diagnosis, the WISC-IV/WAIS-IV
this result suggests cognitive
that subjectsprofile,
withWorking Memory and
milder symptoms Processing
require clin-
Speed
ical Indices were
consultation later.worse than both Verbal Comprehension and Perceptual Reasoning
Indices, as shownthe
Concerning in the literature [62]. Indeed,
WISC-IV/WAIS-IV cognitiveimpairment
profile, of workingMemory
Working memory and and speed
Pro-
of processing
cessing characterized
Speed Indices were worse nearlythanhalfboth
of the sample,
Verbal 53% and 43%,and
Comprehension respectively.
PerceptualSeveral
Rea-
studiesIndices,
soning also documented
as shown inthe theinfluence
literatureof[62].
working memory
Indeed, and speed
impairment of processing
of working memory on
learning
and speeddisorders
of processingand the predictive role
characterized of working
nearly half of thememory
sample, on53%the and
degree of learning
43%, respec-
deficitSeveral
tively. [63]. In studies
our results,alsocognitive
documented profiles
the explain
influence almost 34% of the
of working learning
memory andimpairment,
speed of
and the Working Memory Index was a significant predictor.
processing on learning disorders and the predictive role of working memory on the de-
gree ofThe analysis
learning of the
deficit results
[63]. In our of results,
the CBCL showed
cognitive that about
profiles explainhalfalmost
(48%)34%of the SLD
of the
subjects manifested emotional-behavioral symptoms
learning impairment, and the Working Memory Index was a significant predictor. with a prevalence of internalizing
(33%), such as anxiety and depression, over externalizing (16%) disorders. The incidences
found are similar to those reported in the literature in SLD [3,60] and higher than in typical
J. Clin. Med. 2023, 12, 1882 11 of 15

development [64,65]. Despite this result, CBCL was not directly related to cognitive profile
and learning measures.
The present study enriches the previous literature by investigating the role of cog-
nitive and background characteristics on the emotional-behavioral phenotypes and their
relationship with the learning profile in SLD.
Chronological age represents a crucial factor for the display of internalizing prob-
lems in SLD subjects: In fact, the manifestation of internalizing symptoms, particularly
withdrawal and somatic problems, tends to increase with age. As older subjects showed
a milder learning impairment, that result supports further that there is not a direct rela-
tionship between learning and internalizing problems in SLD. In adolescence, a learning
problem can have a greater impact on mood even in cases of milder disorders and probably
the late diagnosis could have exposed the subject to a longer history of school failure, with
consequent repercussions on the self-esteem. Sex and cognitive characteristics represent a
crucial factor for the expressiveness of externalizing problems: Attentional problems and
rule-breaking behaviors are higher in males than females, and emotional problems are
related to higher working memory impairment [3,24,28].
One other main contribution of the present study came from the mediation model
analysis. Learning impairment was predicted by age and familiarity for neurodevelop-
mental disorders and, indirectly, via the mediation of the Working Memory Index, by the
Rule-Breaking Behavior scale. This result enriches the previous literature as it suggests
that behind the acknowledged relation between low working memory skills and learning
impairments in SLD, there could be the role of behavioral regulation. Those subjects with
greater difficulties in following rules and controlling behavior may pay less attention to
maintaining and updating verbal information in working memory with cascade effects on
learning competence [66].
Considering the results as a whole, on the one hand, our study confirms the previous
literature concerning the greater presence of internalizing problems in subjects with SLD,
especially when they are older, and the higher manifestation of externalizing problems in
males and in children with low working memory profiles. On the other hand, the present
study increases the knowledge about the relationship between externalizing problems
and learning impairment, reporting that this relation is not direct but mediated by cross-
cognitive processes, such as working memory. Thus, a potential role of working memory
as a mediator of the relationship between behavioral regulation and learning impairment
may be supposed.
The present study has some limits, such as the inclusion of a widespread age range and
the need to collect longitudinal data that could help in describing the developmental trajec-
tories of the emotional-behavioral problems in SLD and their relationship with learning
disorders. Another limitation is that the chronological age of our sample overlapped with
the age of first diagnosis, thus limiting the interpretation of the age effects. Despite the good
psychometrical properties of the CBCL, it is a parental reports diagnostic screening tool,
thus future and longitudinal studies are needed to implement other clinical or educational
data on the emotional-behavioral characteristic of children and adolescents with SLD.
These results may have implications for clinical practice: Beyond the importance of
combining learning assessment with emotional and neuropsychological profile, it is of
the utmost importance to provide psychological and emotional support to subjects with
SLD, because of the high presence of internalizing problems and the cascade effects of
externalizing problems on cognitive and learning profile. Moreover, our results support the
growing literature on the implementation of training on working memory [67,68] and on
emotional-behavioral problems [69–71] in SLD, especially in this clinical condition when
behavioral and regulation problems are revealed.
J. Clin. Med. 2023, 12, 1882 12 of 15

5. Conclusions
An emotional-learning-cognitive model is proposed in order to relate the different
factors that may characterize the inter-individual variability of individuals with SLD.
Although further studies with larger samples and more extensive neuropsychological
investigations may be conducted to confirm these findings, our study is the first attempt
to understand how the cognitive profile mediates emotional-behavioral phenotype in
SLD subjects.

Supplementary Materials: The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/jcm12051882/s1, Table S1: t statistics for Bonferroni post-hoc
corrections for multiple comparisons, on the Wechsler indices; Table S2: t statistics for Bonferroni
post-hoc corrections for multiple comparisons on the CBCL DSM-oriented sub-scales; Table S3: t
statistics for Bonferroni post-hoc corrections for multiple comparisons on the CBCL syndrome scales.
Author Contributions: Conceptualization, P.C., M.C.D.L., A.M.C. and A.M.; Methodology, P.C.,
M.C.D.L., C.P., O.P., A.M.C. and A.M.; Formal Analysis, M.C.D.L., F.G. and C.P.; Investigation,
P.C., M.C.D.L., F.G., M.B.D.L. and M.B.(Mariaelisa Bartoli); Data Curation, O.P., M.B.D.L., P.C.,
M.B.(Mariaelisa Bartoli) and C.P.; Writing—Original Draft Preparation, P.C., M.B. (Matteo Baroncini),
M.C.D.L., C.C. and C.P.; Writing—Review & Editing, A.M., A.M.C., C.C., F.G., M.B.(Matteo Baroncini)
and M.B.D.L.; Supervision, C.P., C.C., A.M. and A.M.C. All authors have read and agreed to the
published version of the manuscript.
Funding: This work has been partially supported by grant from the IRCCS Stella Maris Foundation
(Ricerca Corrente 2019, and the 5 × 1000 voluntary contributions, Italian Ministry of Health).
Institutional Review Board Statement: The study was conducted according to the guidelines of
the Declaration of Helsinki and approved by the Paediatric Ethics Committee of the Tuscany Re-
gion (248/2020).
Informed Consent Statement: Written informed consent has been obtained from the all parents of
children involved to publish this paper.
Data Availability Statement: The datasets generated for this study are available on request to the
corresponding author.
Acknowledgments: We would like to thank the children and parents who participated in this study.
We also thank Alessia Martucci for english revision.
Conflicts of Interest: The authors declare no conflict of interest.

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