Gross, Fine and Visual-Motor Skills in Children with Language Disorder, Speech Sound Disorder and Their Combination

Increasing evidence shows that children with Communication Disorders (CDs) may show gross, fine, and visual-motor difficulties compared to children with typical development. Accordingly, the present study aims to characterize gross, fine and visual-motor skills in children with CDs, distinguishing children with CDs into three subgroups, i.e., with Language Disorders (LD), Speech Sound Disorders (SSD), and LD + SSD. In Experiment 1, around 60% of children with CDs (4 to 7 years; 21 with LD, 36 with SSD, and 90 with LD + SSD) showed clinical/borderline scores in balance skills, regardless of the type of communication deficit. However, children with LD, SSD, and LD + SSD did not differ in gross and fine motor skills. In Experiment 2, a higher percentage of children with CDs (4 to 7 years; 34 with LD, 62 with SSD, 148 with LD + SSD) obtained clinical/borderline scores in Visual Perception skills. Moreover, children with LD + SSD performed significantly worsen in Visual Perception and Fine Motor Coordination skills compared to children with SSD only. Our results underlined that CDs are generally associated with gross motor difficulties and that visual-motor difficulties are related to the type of communication deficit. Paying earlier attention to the motor skills of children with CDs could help clinicians design effective interventions.


Introduction
Language development in childhood is usually associated with a variety of cognitive functions, such as working memory [1][2][3], auditory perception [4,5], and sustained attention [6][7][8]. Studies have found that motor and language development are closely related. One of the foremost pieces of evidence of the intertwined development of motor and language skills is represented by the onset of gestures during infancy [9,10]. Before mastering a language, infants usually use gestures with communicative intentionality in order to properly interact with their parents and share experiences or elicit requests. In a certain sense, motor gestures could be considered the precursors of language [9,10]. Theories of embodied cognition are in line with this theoretical background and state that the development of motor skills can influence the development of language skills, such as language comprehension [11,12].
Neuroimaging findings have also documented the intertwining of motor and language skills in the left motor and premotor areas, including the primary motor cortex [13], the ventral premotor cortex [14,15], the dorsal premotor cortex [13,14,16], the supplementary motor area, the pre-supplementary motor area [13,14], the inferior frontal cortex [17], and Second, in the considered studies, the relationship between language and motor aspects has been documented in groups of children with a heterogeneous and wide age range (e.g., from 24 months to 6 years), and this may have influenced previous results. In fact, age is a factor that affects the development of motor skills. Accordingly, the motor skills of a 2-year-old child are different from those expected at 6 years of age. Furthermore, it should be considered that as children grow, the demands of the environment (e.g., selfcare and school work) gradually increase, and motor skills become an important means by which children interact with the external environment. Deficits in this area can, therefore, differently impact children's functioning, including also the development of language, depending on their age [39].
Starting from these considerations, the present study aims to investigate whether children with CDs, with a narrow age range (from 4 to 7 years) and distinguished into subgroups according to the type of communication deficit, have different motor impairments. In particular, we compared subgroups of children with LD, SSD, and LD + SSD in gross, fine, and visual-motor abilities.

Clinical Eligibility Assessment
The cohort was retrospectively selected through a comprehensive database made of several hundred outpatients assessed at the Child and Adolescent Neuropsychiatry Unit of the Bambino Gesù Children's Hospital (Italy).
The clinical diagnosis of CDs (LD, SSD, LD + SSD) was made according to the Diagnostic and Statistical Manual of Mental Disorders, 5th ed. (DSM-5) criteria [23] based on the developmental history, extensive clinical examination, and language assessment by expert developmental psychiatrists, neuropsychologists, and speech therapists.
To evaluate cognitive level, the brief-IQ scales from the Leiter International Performance Scale-Third Edition (Leiter-3) [40]-were administered. Language skills were assessed via the Batteria per la Valutazione del Linguaggio in bambini dai 4 ai 12 anni (BVL 4-12) [41], including lexical processing (i.e., Naming and Lexical Comprehension subtests, respectively), grammatical processing (i.e., Sentence Repetition and Grammatical Comprehension subtests), and articulation processing. In Naming subtest, children were asked to name a series of stimuli depicted in sheets. In Lexical Comprehension subtest, children were asked to point to a series of black and white target pictures after experimenter pronounced a word illustrating one of the four pictures. For each correct answer, one point was assigned. In the Sentence Repetition subtest, children were asked to listen to a sentence and then repeat the sentence they heard. In the Grammar Comprehension subtest, after hearing each stimulus sentence (e.g., "the girl pushes the boy"), children were shown a sheet with four pictures: one represented the meaning of the target sentence, whereas the remaining three pictures represented grammatical distractors (e.g., "the girl pushes the boys", "the girls push the boy", or "the girls push the boys", respectively). Children were asked to point to the picture target. One point was assigned for each correct answer. In each subtest, one point was assigned for each correct answer. The total raw score was converted into standard deviation scores.
For both Experiment 1 and 2, participants' anonymity and data confidentiality were ensured. All procedures performed in the study involving human participants were in accordance with the 1964 Declaration of Helsinki and its subsequent amendments or comparable ethical standards.

Experiment 1 2.2.1. Participants and Procedures
The cohort was composed of 147 Italian-speaker children (Females, F/ Males, M = 30/117), including 21 with LD, 36 with SSD, and 90 with the combined disorders.
Criteria for inclusion in the study were the followings: (1) Clinical diagnosis of CDs (for details, see Table 1); (2) non-verbal intelligence quotient (nvIQ) above 85; (3) age Brain Sci. 2023, 13, 59 4 of 12 range from 4 to 7 years included; (4) not having medical/neurological disorders (e.g., blindness, deafness or genetic syndromes); (5) not presenting comorbidities with other neurodevelopmental disorders, such as Attention Deficit Hyperactivity Disorder or Autism Spectrum Disorder, except with DCD. The percentages refer to the number of children who showed impairment in the single subtest. Each participant may show more than one impairment in more than one subtest. Figure 1 presents the percentage of children with CDs and comorbid DCD regardless of subgroups. Specifically, 42.9% of children with LD also presented DCD, 38.9% of participants with SSD also had DCD as well as 48.9% of children with LD + SSD. comparable ethical standards.

Participants and Procedures
The cohort was composed of 147 Italian-speaker children (Females, F/ Males, M = 30/117), including 21 with LD, 36 with SSD, and 90 with the combined disorders.
Criteria for inclusion in the study were the followings: (1) Clinical diagnosis of CDs (for details, see Table 1); (2) non-verbal intelligence quotient (nvIQ) above 85; (3) age range from 4 to 7 years included; (4) not having medical/neurological disorders (e.g., blindness, deafness or genetic syndromes); (5) not presenting comorbidities with other neurodevelopmental disorders, such as Attention Deficit Hyperactivity Disorder or Autism Spectrum Disorder, except with DCD. Figure 1 presents the percentage of children with CDs and comorbid DCD regardless of subgroups. Specifically, 42.9% of children with LD also presented DCD, 38.9% of participants with SSD also had DCD as well as 48.9% of children with LD+SSD. The percentages refer to the number of children who showed impairment in the single subtest. Each participant may show more than one impairment in more than one subtest.

Gross and Fine Motor Skills
The Movement Assessment Battery for Children 2 (MABC-2) was used to assess gross and fine motor skills [37]. This battery, intended for assessment of children aged 3-16 years, consists of 8 subtests that produce a Total Score and 3 component scores: Manual Dexterity, Aiming and Catching, and Balance. Manual Dexterity component evaluates 46% 54%

Measures Gross and Fine Motor Skills
The Movement Assessment Battery for Children 2 (MABC-2) was used to assess gross and fine motor skills [37]. This battery, intended for assessment of children aged 3-16 years, consists of 8 subtests that produce a Total Score and 3 component scores: Manual Dexterity, Aiming and Catching, and Balance. Manual Dexterity component evaluates fine motor skills and consists of three tasks: a one-hand posting task, a timed bimanual assembly task, and an untimed drawing task. The Aiming and Catching component aims at assessing the coordination of fine and gross motor skills and includes tasks requiring the throwing of an object to a target and the catching of an object using both hands. The Balance component assesses gross motor skills and comprises a static balance task and two dynamic balance tasks that involve sustained, controlled movement and more explosive action. For each test item, experimenters recorded designated measures (e.g., time taken to complete the task, number of successful throws/catches, and number of failures). For the Total Score and for the score of each component, the raw performance scores were then converted into standard scores (mean ± SD: 10 ± 3). The standard scores are considered problematic, i.e., clinical/borderline scores, when they are equal or below 6 (2 SDs below the mean).

Experiment 2 2.3.1. Participants and Procedures
After clinical eligibility assessment, the selected cohort was composed of 244 Italianspeaker children (F/M = 63/181) divided into three subgroups (see Table 2): 34 with LD, 62 with SSD, and 148 with LD+. Of all children, 43 children have participated in Experiment 1. Procedures, as well as inclusion criteria in the study, were the same as in Experiment 1. Figure 2 presents the percentage of children with CDs and comorbid DCD regardless of subgroups. Specifically, 11.8% of children with LD also presented DCD, 4.9% of participants with SSD also had DCD as well as 13.5% of children with LD + SSD. explosive action. For each test item, experimenters recorded designated measures (e.g., time taken to complete the task, number of successful throws/catches, and number of failures). For the Total Score and for the score of each component, the raw performance scores were then converted into standard scores (mean ± SD: 10 ± 3). The standard scores are considered problematic, i.e., clinical/borderline scores, when they are equal or below 6 (2 SDs below the mean).

Participants and Procedures
After clinical eligibility assessment, the selected cohort was composed of 244 Italianspeaker children (F/M = 63/181) divided into three subgroups (see Table 2): 34 with LD, 62 with SSD, and 148 with LD+. Of all children, 43 children have participated in Experiment 1.
Procedures, as well as inclusion criteria in the study, were the same as in Experiment 1. Figure 2 presents the percentage of children with CDs and comorbid DCD regardless of subgroups. Specifically, 11.8 % of children with LD also presented DCD, 4.9 % of participants with SSD also had DCD as well as 13.5 % of children with LD+SSD. The percentages refer to the number of children who showed impairment in the single subtest. Each participant may show more than one impairment in more than one subtest.

Measures Visual-Motor Skills
The Beery-Buktenica Developmental Test of Visual Motor Integration (VMI) was used to assess visual-motor skills [42]. This test, intended for assessment of children aged from 2 years old, consists of 3 components: Visual Motor Integration, Visual Perception, and Fine Motor Coordination. The Visual Motor Integration component requires participants to imitate and copy a series of progressively more complex forms. The Visual Perception component requires children to identify matching forms when presented with similarly shaped forms, and the Fine Motor Coordination component involves children's ability to connect dots and stay within lines of the forms. For each component, the raw performance scores were then converted into composite scores (mean ± SD: 100 ± 15) based on the normative data. The composite scores are considered problematic, i.e., clinical/borderline scores, when they are equal or below 85 (2 SDs below the mean).

Statistical Analysis
In Experiment 1 and Experiment 2, differences among the three subgroups (LD, SSD, LD + SSD) on chronological age and nvIQ were tested separately by two Analyses of Variance (ANOVAs), while difference in gender was verified by means of a Chi-square (χ 2 ).
In Experiment 1, subgroups with CDs (LD vs SSD vs LD + SSD) were compared on the MABC-2 components (Manual Dexterity vs Aiming and Catching vs The Balance) using the Kruskal-Wallis ANOVA because the assumption of normality was not fulfilled. Multiple Comparisons p values (2-tailed) were applied to account for the comparisons of subgroups.
Children with LD, SSD, or LD + SSD were further classified as children with clinical/borderline scores (when standard scores on MABC-2 were equal or below 6) or children with no clinical scores (when standard scores were above 6). For all analyses, a p value < 0.05 was considered statistically significant. In order to evaluate a potential relation between individual factors (i.e., age, nvIQ) and motor skills, Spearman's rank correlations (rho) were performed separately for LD, SSD, and LD + SSD on significant results identified by the Kruskal-Wallis ANOVA. Bonferroni's correction was applied for multiple comparisons.
The percentage of children with clinical/borderline scores for each MABC-2 component, regardless of the subgroups with CDs (LD, SSD, LD + SSD), was 53% in Manual Dexterity, 47.6% in Aiming and Catching, and 62.6% in Balance components. No significant difference emerged across the three subgroups in the distribution of children with clinical/borderline scores (see Table 3

Experiment 2
The three subgroups did not differ for chronological age (age range As shown in Table 4, Kruskal-Wallis ANOVA analysis indicated that the three subgroups did not differ in Visual Motor Integration (p = 0.12). However, a significant difference emerged in the Visual Perception component among the three subgroups (p = 0.0015). Post hoc documented significantly worse scores in LD + SSD than in SSD (p = 0.004).  In the LD + SSD group, significant correlations were found between nvIQ and Visual Motor Integration (rho = 0.21, p = 0.012), Visual Perception (rho = 0.29, p = 0.0003), whereby as nvIQ increased, greater scores in VMI components were observed. No significant correlations between nvIQ and the Motor Coordination component (rho = 0.05, p = 0.51). Moreover, a significant correlation was found between age and the Visual Perception component (rho = 0.18, p = 0.024). However, no significant correlations were found between age and Visual Motor Integration (rho = −0.13, p = 0.11) and Motor Coordination components (rho = 0.15, p = 0.07).

Discussion
We assessed motor skills in a large group of 391 children aged 4 to 7 years according to the type of communication deficit, distinguishing between LD, SSD, and LD + SSD.
Looking at the percentages of children with clinical/borderline scores in MABC-2, around 60% obtained clinical/borderline scores in the Balance component as well as around half of the participants showed clinical/borderline in the remaining components (i.e., Manual Dexterity and Aiming and Catching). Therefore, 1:2 children with CDs-regardless of the type of deficits-may show gross and/or fine motor difficulties.
Our results are consistent with previous studies in which children with CDs tend to perform poorly on motor tasks showing difficulties in stepping, running, stair climbing, and finger gait [35,43]. Furthermore, balancing on one leg has been shown to be one of the tasks in which children with CDs have more difficulty than children with typical development [38].
Of interest, when considering gross motor skills, we observed that children with LD, SSD, and LD + SSD did not differ in MABC-2, generally obtaining clinical/borderline scores (≤6). This result further underlined that gross motor impairment is not specific to a subgroup of CDs but this aspect is compromised in children with CDs.
From a neurobiological perspective, the comorbidity between CDs and gross motor deficits could be the result of shared motor and language neuroanatomical networks [44]. Accordingly, it has been observed that cortical and subcortical regions (prefrontal cortex, basal ganglia, cerebellum) implicated in balance control are also involved in language production [45,46], and that alterations in these regions may affect motor execution and language [47].
Considering neuropsychological processes, motor and cognitive-linguistic deficits could be the result of a common procedural learning deficit [48][49][50]. The procedural memory system underlies language learning and, when impaired, gives rise to motor and language deficits that affect the acquisition of new sequential skills for word and movement production [51,52].
When considering fine and visual-motor skills, we observed that children with LD + SSD performed lower in the Visual Perception and Fine Motor Coordination components of VMI than the group with SSD alone, but not compared with the group with LD alone. Consistent with our findings, it was documented that children with comorbid LD + SSD are more impaired compared to children with SSD alone in terms of discrimination and Fine Motor Coordination (i.e., writing) [53].
Evidence demonstrated that perceptual and behavioral judgments pertaining to the auditory domain could be influenced by visual information. Specifically, auditory perceptual performance can be enhanced when the auditory information is paired with spatially and temporally coincident visual information. Conversely, pairing visual information that differs from auditory information in certain stimulus characteristics such as space, time, and semantics often results in the perception of multisensory illusions [54]. Moreover, results suggested a greater reliance on visual cues during speech perception and that visual cues can influence speech processing [55,56]. The complex interplay that occurs between the senses not only affects ongoing processing and perception but also likely plays an important role in future processes through its impact on learning and brain plasticity.
The results of the combined research suggest that there is significant facilitation of auditory comprehension and learning in the presence of salient visual cues, as well as an improvement in speech production [57,58]. The presence of clinical/borderline scores on gross motor skills and the worst performance on Visual Perception and Fine Motor Coordination in the comorbid LD and SSD compared to SSD only could mirror a greater global impairment, as supported by previous studies demonstrating a worse impact of the comorbid disorders in several areas of functioning (i.e., learning difficulties, poorer school achievement, severe deficits on all measures of language) [27,28].
However, it is worth considering that nvIQ was found to be positively correlated with performance in the LD + SSD group (higher nvIQ, better performance). Therefore, although our groups did not differ significantly in demographic variables, some aspects (for instance, nvIQ) may still have affected the results previously discussed and need to be taken into consideration for the next studies.
The co-occurrence of motor problems and language impairment may have important consequences for a child's academic performance [27,28]. Moreover, inadequate fine and gross motor skills in children who already presented a diagnosis of CDs may further limit the child's ability to interact socially and physically with peers, as the communication difficulties experienced by these children may negatively influence social acceptance and presumably cause them to participate less in play with peers [59,60]. Early motor skill development predicts important variability in social-communicative functioning and also in typical development [61,62].
Currently, several studies have supported the idea that rehabilitation based on audiovisual training may be the future of therapeutic interventions for individuals with CDs [54,[63][64][65]. Utilizing training methods that couple meaningful, complementary auditory and visual stimuli can drastically improve performance in speech identification and learning. Indeed, speech is inherently multimodal, and redundant visual and auditory information provides salient cues about the speaker and speech content [66].
In line with the suggestions of the American Academy of Pediatrics Council on Children With Disabilities, overall results encourage screening children with CDs also for motor difficulties [67] and vice versa; children with motor impairments should be referred for a linguistic assessment. Such assessments would allow early identification of associated developmental disorders and appropriate referral to needed therapeutic services.

Conclusions
Overall, our results underlined that CDs are generally associated with gross motor difficulties and that visual-motor difficulties are related to the type of communication deficit.
Thus, early identification of motor deficits and the specific characteristics of subgroups of children with CDs might help the clinicians to provide cues for effective interventions, suggesting proposing motor rehabilitation such as psychomotricity. This is a very important finding considering that many children with CDs will later develop a specific learning disorder, such as in writing.
Future research is needed to better investigate the role of motor skills in the development of CDs in order to identify the most appropriate therapy and to improve the quality of life of children and their families.  Institutional Review Board Statement: All procedures were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Ethical review and approval were waived for this study, due to its retrospective nature.

Informed Consent Statement: Not applicable.
Data Availability Statement: The data presented in this study are available on request from the corresponding author.