Effect of auditory-motor training on auditory processing of school children

ABSTRACT Objective To compare performance in Avaliação Simplificada do Processamento Auditivo Central and Scale of Auditory Behaviors scores before and after auditory and motor training. Methods Sample comprising 162 children aged 9 to 11 years and attending public schools in the city of São Paulo (SP), Brazil; 122 out of 162 children were allocated to one of three experimental groups: Multisensory; Auditory/Motor and Motor/Auditory. Experimental groups were submitted to 8 hours of auditory, visuospatial and motor stimulation over the course of 8 weeks. The remaining 40 children formed the Control Group and received no stimulation. Results Relation between child behavior as perceived by school teachers and auditory test responses revealed that the better the performance in auditory processing assessment, the higher the Scale of Auditory Behaviors scores. Conclusion Auditory and motor training led to improvements in auditory processing skills as rated by Avaliação Simplificada do Processamento Auditivo Central and Scale of Auditory Behaviors; this intervention model proved to be a good tool for use in school settings.


❚ INTRODUCTION
Around 50% of children attending public primary schools begin high school with significant reading and writing problems, if not illiterate, and 30% present with some kind of learning disorder or difficulty. (1) These indices often reflect learning difficulties, writing and logical mathematical reasoning deficits in particular. Learning difficulties have been the focus of recent research, given the significance of learning to full human sociocultural and emotional development. (2,3) Auditory processing is the ability of central auditory pathways to use auditory input effectively, and includes several auditory mechanisms associated with different skills, such as sound localization, temporal resolution and sound sequencing. (4) Temporal resolution is critical for speech intelligibility and a requirement for linguistic and reading skills. (5) Likewise, sound localization impacts mobility and communication, with significant contributions to selective attention -a vital skill for acquisition of new learning content. (6) Studies investigating auditory changes associated with learning disorders (3,(7)(8)(9)(10) revealed that most affected children have compromised auditory processing. (3,10,11) Reduced ability to use auditory stimuli in speech perception may contribute to reading and writing deficits. Therefore, auditory processing assessment plays a key role in identification of school children with learning difficulties and in further interventions. (12)(13)(14) Major complaints in children with central auditory processing disorder (CAPD) include inability to follow complex verbal instructions; poor verbal compared to nonverbal cognitive performance; reading and writing difficulties; speech delay; impaired processing of verbal input in noisy environments, and selected auditory attention deficits. (15) Functional central nervous system plasticity, the existence of critical periods for learning, and strengthening of synaptic connections via repetition have been demonstrated in cognitive neuroscience research. (16) Also, auditory stimulation and auditory-verbal training are thought to promote functional and structural changes in the central auditory nervous system. (7,(16)(17)(18) This concept has led to the implementation of CAPDspecific interventions aimed at school children, with particular emphasis on speech therapy, including environmental changes, the therapeutic process per se and compensatory strategies. (19,20) Behavioral tests play a significant role in screening for central auditory processing changes and identification of school children with hearing loss, and evidence of learning disabilities in school settings. (7,12,13,21) The Avaliação Simplificada do Processamento Auditivo Central (ASPAC) [Simplified Central Auditory Processing Assessment] is a user-friendly screening tool for hearing impairment in school children, which comprises sound localization and verbal and nonverbal sequence memory tests with three to four sounds. Poor performance in ASPAC may indicate auditory perceptual impairment. Early detection of such impairments (i.e., at school) may contribute to referral of affected children for comprehensive auditory processing assessment and proper therapeutic intervention. (7,14,21) Since 2010, the American Academy of Audiology (AAA) (22) recommends the use of self-perception questionnaires for auditory complaint investigation and qualitative analysis, and to complement behavioral tests in CAPD diagnosis. The Scale of Auditory Behaviors (SAB) in one such questionnaires (23) available in Portuguese, (24) and allows the quantification of child behaviors associated with auditory processing in everyday life according to parent/teacher perception. Questionnaire items interrogate behaviors such as understanding of verbal instructions, attention quality, speech-sound discrimination, self-organization skills in everyday life and reading, to screen for detectable signs of dysfunction.
A Portuguese study investigated the correlation between SAB scores and performance in behavioral hearing tests, and suggested this tool can be used to screen school children with auditory processing-related learning difficulties. (13) This study proposes a therapeutic and educational approach based on auditory and motor stimulation of groups of school children, in school settings, to improve auditory perceptual ability. This study shall contribute to health/education partnerships via therapeutic, educational, multisensory intervention programs aimed at children with learning complaints and no immediate access to specialized therapy. The sample comprised 162 children (86 females) aged 9 to 11 years, who met all inclusion criteria (age group, proper cognitive function, lack of neurologic and/or psychiatric disorders and informed consent for participation).

❚ OBJECTIVE
All participants completed initial (IA, pre-training) and final (T2, post-training) assessment procedures. The training program in this trial was named Multisensory Stimulation.

Avaliação Simplificada do Processamento Auditivo Central (ASPAC)
This simplified central auditory processing assessment comprises exclusively auditory, sound localization and verbal and nonverbal memory sequence tasks. The test for sound localization in five directions consisted of diotic tasks involving high frequency sounds presented in five directions (front, back, above, right and left); participants were asked to point in the direction of sound. This test was used to assess sound localization skills and the physiologic mechanism underlying sound source direction discrimination. Normal auditory processing was defined as four or more correct hits, provided these included the lateral plane.
The Memory Test For Verbal Sequence (MSV) consisted of verbal stimuli (four syllables; "pa", "ta", "ca" and "fa") presented in different sequences. Participants were first asked to repeat each syllable alone, then in the sequence they were spoken. Four instruments (rattle, coco, agogo and bell) played in different sequences were used in the memory test for nonverbal sequence. Following a demonstration, participants were asked to close their eyes and point to instruments as they were played. Participants achieving two or more correct hits out of three attempts were defined as normal. Participants failing in this test were exposed to three-sound sequences and the same assessment criterion applied.

Scale of Auditory Behaviors
The SAB (13,23,24) consists of a 12-item questionnaire intended for parents and/or school teachers for data collection and CAPD diagnostic support purposes. School teachers in this sample provided answers to questionnaire items (Portuguese version) related to everyday life events reflecting child behavior in the auditory and attentional domains. Behaviors were scored 1.0, 2.0, 3.0, 4.0 and 5.0 (behaviors occurring frequently, most of the time, sometimes, sporadically and never, respectively). Item scores were added up to form a final score ranging from 12 to 60 (total score). In this analysis, SAB scores of 46, 45 to 36 and ≤35 corresponded to normal, suggestive of CAPD and evidence of CAPD, respectively. (13) The Multisensory Stimulation training program was designed to provide auditory, visuospatial and motor stimulation to groups of children in school settings. The program comprised 16 biweekly 30-minute sessions (total stimulation time, 8 hours), divided according to stimulation type (single or combined) and applied to three randomly selected groups per classroom. Children were reassessed at the end of each eightsession phase and the type of intervention changed in groups submitted to single stimulation. Groups were named as follows: Auditory/Motor Group (AMG) -40 children submitted to single stimulation (eight auditory stimulation sessions followed by eight visuospatial and motor stimulation sessions); Motor/Auditory Group (MAG) -41 children submitted to single stimulation in the opposite order (visuospatial and motor stimulation followed by auditory stimulation); Multisensory Group (MSG) -41 children submitted to combined auditory, visuospatial and motor stimulation (16 sessions) and Control Group (CG) -40 non-stimulated children who served as reference for typical development in this environment and age group, and comparison with experimental groups.
The informal training program described was based on Pereira et al., (25) Stimulation procedures employed in each group are described in appendix 1.
Data were expressed as descriptive statistics, with a 0.05 level of significance. Scale of Auditory Behaviors scores consist of small numerical values; however, such values represent a conversion of ordinal variables and allow the distinction between elements in the sample based on element qualities/differences. Therefore, preand post-training (IA and T2) intergroup differences were investigated using the non-parametric Wilcoxon test. Correlations between instruments (i.e., positive associations between SAB scores and performance in ASPAC -the higher the SAB score, the higher the number of correct responses in ASPAC tests) were investigated using the non-parametric Spearman correlation test. Parametric tests were used and the T value (lowest summed score) calculated to investigate score differences per ASPAC test, per group and calculated p value, to compare different time points (IA versus T2) and groups ( Pre-training assessment revealed warning signs of CAPD in the MAG, while remaining groups fell within normal ranges (normal SAB scores). All groups scored higher in post-(T2) compared to IA assessments. However, significant differences (T=61; n=41; p<0.001) were limited to the MAG.
Descriptive statistics of sound localization tests (ASPAC MSV4 and MSnV4 tests) per group per time point are given in table 2.
Pre-and post-training sound localization performance did not differ significantly between groups. Experimental groups had higher positive MSV and MSnV variations at T2 compared to the CG.
Intergroup pre-and post-training comparisons are shown in table 3.
ANOVA of IA data failed to reveal differences between groups. Therefore, potential biases (i.e., groups with comparatively good or poor pre-training performance in auditory processing tasks) were excluded. Interactions (p<0.05) between SAB scores and ASPAC performance in different groups and at different time points (IA and T2) are shown in table 4 and figures 1 to 4.
No interactions between performance in ASPAC and SAB scores were noted in the MAG or CG at any of the time points. In contrast, interactions were detected in the AMG (MSnV4s test) at both time points, i.e., SAB scores increased as performance in ASPAC improved. Interactions between variables were also detected in the MSG (SL test, negative correlation at IA; MSV test, positive correlation at T2). Pre-and post-training (IA and T2) differences in experimental groups were not detected in the CG.
❚ DISCUSSION Experimental groups in this study achieved higher SAB scores following training, with significant preand post-training differences in the MAG. Therefore, auditory and motor training seems to have promoted positive auditory behavior changes, as rated by school teachers. (13,23,24) Mean MAG pre-training scores are suggestive of CAPD. (13) However, improved auditory behavior in treated groups following 8 hours of stimulation points to training effectiveness and emphasizes the significance of tools aimed at assisting school teachers with recognition of behaviors associated with learning dysfunction, i.e., observational tools beyond traditional pedagogical assessment methods. According to previous studies, school teachers are often ill-informed about reading and writing disorders and related causes, possibly due to lack of specific higher education training. (26,27) All groups performed well in ASPAC SL test at IA. Low variability in test responses may have reflected the fact that mean IA scores were within normal ranges. Lack of changes in sound localization skills in school children with reading and writing disabilities has been reported. (12) Changes detected in MSV and MSnV-4 sound tests at IA in this study have been described in school children with learning difficulties, with and without CAPD. (12,14) Therefore, lack of temporal ordering skills is vital for language processing. Children in the experimental groups in this trial showed normal temporal ordering skills at T2, with significant differences between IA and T2.        At the age of three years, children are already capable of repeating three-syllable sequences, and can handle longer sequences at seven years, with improved performance as they grow. At the age of six years, children are capable of memorizing four musical (nonverbal) sounds played in a given sequence, with successful performance in at least two out of three attempts. (7) Intergroup IA comparisons revealed similar performance in auditory processing tasks and groups submitted to training performed significantly better in the MSnV test compared to the CG. Improved temporal ordinance performance in school children submitted to auditory stimulation has been reported. (20) Initial changes in temporal ordinance tests in this study may be a predictor of academic difficulties. Improved skills after stimulation T2 of experimental groups demonstrate positive effects of the therapeutic program proposed, with relevant contribution to better neurobiological learning in school settings.
Hence, according to the neuroplasticity concept, stimulation and experience led to activation and reinforcement of specific neural pathway, thereby supporting children in the recognition of novel patters and acquisition of new context and skills. (15)(16)(17)(18)28) This finding is consistent with the idea of motor and sensory system improvement in response to experience and learning. These systems connect recognition of environmental stimuli with a wide range of motor responses. It can therefore be argued that reading and writing disabilities are not limited to the verbal domain. (28) In this study, auditory and motor stimulation in school settings led to rapid changes in auditory behavior. Avaliação Simplificada do Processamento Auditivo Central was thought to be a sensible tool for detection of such behavioral variations and may be effectively applied to screen for CAPD in school children. (7,13,19,21) Avaliação Simplificada do Processamento Auditivo Central variables were significantly correlated with SAB questionnaire responses given by school teachers in the AMG (MSnV test) and MSG (MSnV and SL tests), both at IA and T2. As regards other significantly correlated skills at IA, school teachers failed to notice effects of stimulation.
Correlations between experimental group SAB scores and ASPAC performance revealed small but positive variations in IA and T2 means, suggesting beneficial effects of training. The lack of positive variations in the CG should be emphasized.
Relations between child behavior as perceived by school teachers and corrauditory test responses in this study are consistent with findings of Nunes et al., -i.e., the better results auditory processing tests, the higher the SAB scores. (13) Findings from this study suggest the therapeutic program proposed (25) and implemented in school settings can be used to characterize and dinstinguish school children with actual CAPD evidence, who need specialized therapy. (13) Also, aplication of behavioral tests in scholl settings may help teachers recognize signs of auditory changes in children. (7,(22)(23)(24) Self-assessment questionnaires and the Portuguese version of the SAB have been employed in recent studies; still, validation for the Brazilian population is lacking and may be regarded as a limitation of this study.
Multisensory experiences contribute to the development of perception mechanisms, with widely demonstrated impacts on cognition. Multisensory integration between motor and sensory systems reach maturity around the age of 11 years; (16,28) hence the relevance of stimulation programs focusing on primary education and amenable to implementation in school settings as a means to support children with reading and writing difficulties. Interdisciplinary approaches for greater inclusion of children with learning disabilities should be encouraged.
The sample in this study was selected at random. However, stimulation programs aimed at children with special educational needs, including longer sessions and teacher capacitation, may contribute to rehabilitation and development of the reading and writing skills.

❚ CONCLUSION
School children in this study performed similarly when first submitted to the Avaliação Simplificada do Processamento Auditivo Central. Auditory and motor training led to significant auditory and motor skill improvements, which were also perceived by school teachers, as shown by Scale of Auditory Behaviors scores. The intervention model described proved to be an effective tool amenable to application in school settings. Supine position, arms along the body. Word sequence (semantic class and background noise). Ignore noise, repeat sequence in the same order with arms raised, then relax arms. Repeat with legs and arms using number sequence. Sequence dictated by mediator in silent conditions and repeated by child in noisy conditions Two parallel lines (4m long each). Familiar songs and background noise. Hold a tennis ball between body parts. Walk between lines while holding ball. Stop and complete background song In circle, with a ball. Child sings a nursery rhyme and, at mediator's command, throws the ball to a friend, who then resumes singing Expose child to different environmnet sounds (e.g., crumbling paper, key, ball kicking). Reproduce sounds heard (in different order) and increase sequence progressively.
Write down the number of stimuli the child is able to reproduce Sitting in circle, each child adds an item to a supermarket list in sequence repeat item sequence and name the child who added the item Repeat nonverbal sound (musical) sequence and name instruments in the sequence they were played Movable alphabet letters and semantic class labels. The child picks a letter and a class, then says one word beginning with that letter within that semantic class Temporal ordinance -AMG/ MAG 3/7 5 and 6/13 and 14 Instruments played in different directions with background noise (e.g., out of tune radio). Ignore noise and point to the direction of sound source Four-word (fruits) sequence dictated with radio playing at moderate intensity. Repeat sequence adding one word to sequence (up to ten words per sequence) Four-number sequences dictated in silent conditions; child repeats in noisy conditions. Change numbers in sequence Play familiar songs with rhymes (e.g., nursery rhymes) in full. In circle, passing a ball; when music stops the one holding the ball must complete song Play two sound stimuli on a keyboard with different time intervals. Say whether one or two sounds were heard. Gradually reduce interval between sounds Use consonant cluster words (e.g., plate, flute, plan, white, light etc.). Present words in two manners: correct manner, then adding one vowel before consonant (e.g., plate and palate); indicate sound heard saying whether the correct form was the first or second Sentence read by mediator. Child must indicate the number of words in each sentence.
Gradually increase In circle. Mediator reads a story; when mediator stops selected child must complete sentence to make sense Sit quietly on a chair while manipulating ball (throw ball up into the air and catch it) On the floor, (throw ball up into the air while moving to the right, left, front and back as requested by mediator Masking tape line on the floor (1.5m). Walk on line placing one foot in front of the other while kicking ball to the right or left as opposite front foot hits the ground Feet on the wall, hands on the floor. Sustain position for 10 seconds then relax. Increase time by 10 seconds per round up to five rounds. Unsuccessful round may be repeated once Using a tennis ball, child must throw ball with right and left hand in sequence, touching the floor, ceiling, right and left walls and not letting the ball drop on the floor One ball in each hand; throw ball up into the air and down with the right or left hand (e.g., right hand throws ball up, left hand throws ball down) Two parallel lines (5m long each; walk from one side to the other while counting steps required. Cover the same distance with varying step count, as requested by mediator.
Shorten or lengthen stride Walk between lines with metronome; walk from one side to the other at metronome beat pattern. Once completed, repeat with faster beat pattern -Visuomotor coordination and space-time perception