Do auditory brainstem implants favor the development of sensory integration and cognitive functions?

Abstract

Background
Information about the development of cognitive skills and the effect of sensory integration in children using auditory brainstem implants (ABIs) is still limited.

Objective
This study primarily aims to investigate the relationship between sensory processing skills and attention and memory abilities in children with ABI, and secondarily aims to examine the effects of implant duration on sensory processing and cognitive skills in these children.

Methods
The study included 25 children between the ages of 6 and 10 years (mean age: 14 girls and 11 boys) with inner ear and/or auditory nerve anomalies using auditory brainstem implants. Visual‐Aural Digit Span Test B, Marking Test, Dunn Sensory Profile Questionnaire were applied to all children.

Results
The sensory processing skills of children are statistically significant and positive, and moderately related to their cognitive skills. As the duration of implant use increases, better attention and memory performances have been observed (p < .05).

Conclusion
The study demonstrated the positive impact of sensory processing on the development of memory and attention skills in children with ABI. It will contribute to evaluating the effectiveness of attention, memory, and sensory integration skills, and aiding in the development of more effective educational strategies for these children.

Full text

Received: 18 November 2023 Revised: 22 April 2024 Accepted: 5 July 2024
DOI: 10.1002/brb3.3637
ORIGINAL ARTICLE
Do auditory brainstem implants favor the development of
sensory integration and cognitive functions?
Banu BA¸S1Nuriye Yıldırım Gökay2Zehra Aydo˘
gan3Esra Yücel4
1Faculty of Health Sciences, Department of
Audiology, Ankara Yıldırım Beyazıt University,
Ankara, Turkey
2Faculty of Health Sciences, Department of
Audiology, Gazi University, Ankara, Turkey
3Faculty of Health Sciences, Department of
Audiology, Ankara University, Ankara, Turkey
4Faculty of Health Sciences, Department of
Audiology, Hacettepe University, Ankara,
Tur key
Correspondence
Banu BA ¸S, Faculty of Health Sciences,
Department of Audiology, Ankara Yıldırım
Beyazıt University,Ankara, Turkey.Email:
fzt_banu@hotmail.com
Abstract
Background: Information about the development of cognitive skills and the effect of
sensory integration in children using auditory brainstem implants (ABIs) is still limited.
Objective: This study primarily aims to investigate the relationship between sensory
processing skills and attention and memory abilities in children with ABI, and secondar-
ily aims to examine the effects of implant duration on sensory processing and cognitive
skills in these children.
Methods: The study included 25 children between the ages of 6 and 10 years (mean
age: 14 girls and 11 boys) with inner ear and/or auditory nerve anomalies using audi-
tory brainstem implants. Visual-Aural Digit Span Test B, Marking Test, Dunn Sensory
Profile Questionnaire were applied to all children.
Results: The sensory processing skills of children are statistically significant and pos-
itive, and moderately related to their cognitive skills. As the duration of implant use
increases, better attention and memory performances have been observed (p<.05).
Conclusion: The study demonstrated the positive impact of sensory processing on the
development of memory and attention skills in children with ABI. It will contribute to
evaluating the effectiveness of attention, memory, and sensory integration skills, and
aiding in the development of more effective educational strategies for these children.
KEYWORDS
auditory brainstem implants, cognitive, sensory integration
1INTRODUCTION
Development is a dynamic process that reflects the rapid growth of
interrelated functions in the cognitive, physical, and socio-emotional
areas. Cognitive abilities refer to a range of skills including language,
memory, attention, reasoning, visualization, and perceptual function
(Almomani et al., 2021). Cognitive development is a multidimensional
process intertwined with the development of sensory systems. Chal-
lenges or limitations in the reception/perception of one sense can
detrimentally impact children’s overall cognitive growth. Relevantly
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2024 The Author(s). Brain and Behavior published by Wiley Periodicals LLC.
here, hearing loss has been strongly linked to cognitive deficits. The
majority of the population with congenital or early acquired hearing
impairment has a similar cognitive developmental picture. The differ-
ent pictures are not caused by the hearing impairment itself but by
difficult language learning and the lack of a developed communica-
tion system. Sensory theories claim that early auditory deprivation
changes neuronal networks across different brain areas, and this leads
to serial effects on various functions. For example, lack of exposure to
sounds during early development negatively impacts the cognitive abil-
ities, speech and language skills, and social development of affected
Brain Behav. 2024;14:e3637. wileyonlinelibrary.com/journal/brb3 1of10
https://doi.org/10.1002/brb3.3637

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children (Kral et al., 2007,2013). These theories are not sensory in
the sense that it refers to sensory integration per se, but is related
to the limited reception of speech features that must be received in
order to be able to identify word meanings. Sensory integration and
deafness are more connected by the so-called cognitive theory in the
field of language habilitation in deaf children, which states that due to
congenital or early deafness, a series of cascading perceptual and cog-
nitive consequences occurs (Conway et al., 2009). Differences in the
development of deaf children compared to hearing children have been
attributed to language learning difficulties, but there is also research
showing that the brain may develop differently. Deafness has a direct
and indirect impact on neurocognitive development. The brain devel-
opment of these children can be viewed through the interrelationships
of sensory and cognitive theory (Conway et al., 2009;Kral,2007,2019).
The research idea of the current study originates from this idea. In
particular, auditory deprivation has significant effects on children’s
neurocognitive development (de Giacomo et al., 2013). When children
are deprived of hearing the speech sounds, they need to learn the lan-
guage, language problems primarily emerge. The absence of fully verbal
communication leads to socioemotional and other cognitive issues.
In general, the auditory deficit experienced by children with hearing
impairment can negatively affect the normal development of cogni-
tive, psychomotor, and behavioral skills and can subsequently lead to
neurodevelopmental changes (Peñeñory et al., 2018). Hearing assis-
tive devices used in the rehabilitation of hearing loss can not only
improve communication abilities but also positively affect cognitive
and other functions (Almomani et al., 2021; Colletti, 2007; Pisoni et al.,
2016). Cochlear implants (CI) can be used to intervene in hearing loss
in people with severe to profound sensorineural hearing loss. How-
ever, CIs may be contraindicated in cases of anatomical malformation
in the inner ear and/or auditory nerve. Auditory brainstem implanta-
tion (ABI) is a preferred intervention option in these cases. Thus, ABIs
are placed in the cochlear nuclei in the brainstem, bypassing the inner
ear (Yildirim Gökay & Yücel, 2024; Yıldırım Gökay et al., 2024). This
study delves into the pivotal question of whether sensory integration
plays a role in shaping cognitive skills among children with auditory
brainstem implants (ABIs). Here, sensory integration refers to the pro-
cess by which the brain organizes and interprets sensory information
from the environment. It encompasses information from the senses
such as touch, taste, smell, sight, and hearing, along with proprioception
and vestibular input (Dunn, 1997). The study also examines the dura-
tion of implant use to evaluate the effect of early access to auditory
stimulation on sensory integration and some cognitive skills.
Auditory brainstem implants (ABIs) are among hearing assistive
devices that are used in patients experiencing severe or very severe
hearing loss due to lack of a cochlea and/or a dysfunctional cochlear
nerve (Sennaroglu et al., 2013). In individuals where the use of ABIs
is recommended, auditory perception development might be con-
strained. Moreover, these children may experience additional neuro-
logical, psychological, and physical disorders, such as attention deficit
hyperactivity disorder (ADHD). Fortunately, there is evidence that
early use of assistive devices (e.g., ABI or cochlear implants) and
their consistent use significantly impact the auditory, speech and lan-
guage, cognitive, academic, and social development of children who
receive these devices (Aslan et al., 2022). Studies have shown that
early auditory implantation (cochlear implantation or auditory brain-
stem implantation) and its careful use in children have a significant
effect on their auditory, language, and speech skills, cognitive skills,
and academic and social development (Glaubitz et al., 2021; Hassan-
zadeh et al., 2021). Besides, sensory integration skills are also crucial
for the development of these skills in children with ABIs. For example,
to achieve a goal, a person should be able to make changes in his/her
emotions and behaviors through self-management (Ayres & Robbins,
2005). This process, which is under the management of the prefrontal
cortex, is called self-regulation. Functions such as attention, memory,
planning, reasoning, mood regulation, and problem solving, which are
among the executive functions, are in the self-regulation process. For
sensory integration skills to be full and complete, self-regulation skills
must function properly (Steinberg, 2010).
Functional sensory systems are needed to establish intraneuronal
connections with cognitive areas. Sensory integration, our ability to
interact with the world, depends on the ability of the cognitive system
to consistently identify, use, and integrate a variety of sensory inputs
(Ayres & Robbins, 2005). This process involves different steps in which
the central nervous system recognizes, organizes, perceives, inter-
prets, and responds appropriately to sensory information (Williamson
& Anzalone, 2001). Model of Sensory Processing, known as Winnie
Dunn Model, emphasizes how individuals process and respond to sen-
sory information in their surroundings. To explain how individuals
perceive and respond to sensory stimuli, which affect their behav-
ior, emotions, and overall functioning, this model categorizes sensory
processing into four patterns based on neurological thresholds and
behavioral response including low registration, sensory seeking, sen-
sory sensitivity, and sensory avoiding. For example, some individuals
have high sensory thresholds, meaning they need a lot of stimulation
to detect a stimulus and respond to it, while others have low sensory
thresholds, and they respond even to small amounts of stimulation
(Dunn, 1997). Deficits in the processing or integration of sensory input
during periods of ongoing development can affect age-appropriate
memory, learning, attention, motor development, academic achieve-
ment, and social relationships (Bharadwaj et al., 2012; Dunn, 2001). A
limited number of studies have indicated that sensory integration skills
may be adversely affected in children with ABIs (Ba¸s&Yücel,2023;
Ertugrul et al., 2021; Yildirim Gökay & Yücel, 2023).
This study aims to assess sustainable attention and memory skills
in children with ABIs (Colletti et al., 2015; Colletti et al., 2005;Sen-
naro˘
glu et al., 2016; Colletti et al., 2009) and sensory integration
abilities. Memory is the power to store what has been experienced and
learned in the mind, a repertoire (Baddeley, 2007). According to Bad-
deley and Hitch’s memory model, memory has three main components:
the central executive, which acts as the control system and controls
the flow of information from auxiliary systems; the phonological loop,
which stores the verbal content in the stimulus; and the visual–spatial
sketchpad, which stores the visual–spatial data (Atkinson & Shiffrin,
1968). This process involves encoding, storing, and retrieving incom-
ing sensory stimuli. In Atkinson and Shiffrin’s (1968) sensory memory
model, incoming stimuli are transferred to short-term memory (STM),
which forms a crucial part of the system. STM not only transfers

BA¸SET AL.3of10
information to long-term storage but also acts as a working memory,
which is responsible for selecting processing strategies and manipulat-
ing information (Atkinson & Shiffrin, 1968). It has been reported that
children with auditory implants exhibit weak performance in short-
term and working memory-based skills (da Silva Lima et al., 2023;Köse
et al., 2022; Pisoni et al., 2016). Furthermore, a weakness in memory
skills has been observed in children with ABIs compared with their nor-
mally hearing or other auditory implanted peers (Herbert et al., 2023;
Yildirim Gökay & Yücel, 2023).
Attention involves the choice of one or more than one possible stim-
ulus or thought at a given moment (Cohen et al., 1993; Fawcett et al.,
2015). It is controlled by the dynamic interactions of multiple neural
systems. Specialized attention areas are located within the parietal and
temporal lobe structures. In the literature, there are additional findings
on the contribution of temporal lobe areas, which are central to audi-
tory processing skills, to auditory attention (Berninger & Nagy, 2008;
Karaka¸s, 2013; Koppitz, 1981). Similar to memory skills, weaknesses
in sustained attention, selective attention, and attention-related cor-
tical responses have been identified in children with auditory implants
(Edwards et al., 2006; Nicastri et al., 2023; Saksida et al., 2022;Schier-
holz et al., 2021). Despite the limited number of studies on children
with ABIs, similar weaknesses have been observed (Colletti, 2007;
Yildirim Gökay & Yücel, 2023).
Furthermore, according to Dunn’s model, children who use ABIs are
affected in their sensory processing skills, particularly in the aspects of
inattention/distractibility (Ba¸s&Yücel,2023). However, to the best of
the authors’ knowledge, while there are a limited number of studies on
sensory processing in children using ABIs in the literature (Ba¸s&Yücel,
2023), no study has yet investigated its effect on cognitive skills. There-
fore, this study primarily aims to explore the positive effect of sensory
processing skills assessed with the Dunn Sensory Profile questionnaire,
specifically on cognitive abilities, such as attention and memory, in chil-
dren with ABIs. It also investigates whether the duration of ABI use
affects cognitive and sensory integration skills. This study may shed
light on future studies evaluating how these skills affect children with
ABIs also allows us to assess their quality of life and the effects on their
daily activities.
2MATERIALS AND METHODS
The study was found appropriate in terms of medical ethics by
the Ankara Yıldırım Beyazıt University Non-Interventional Clinical
Research Ethics Committee. The children and their parents participat-
ing in the study were informed about the purpose and scope of the
study, and written consent forms were obtained from both the children
and their parents.
2.1 Participants
Twenty-five children aged 6−10 years (14 girls and 11 boys) with inner
ear and/or auditory nerve anomalies who used ABIs participated in
the study. These children met the inclusion criteria and were grouped
according to their mean value of duration of implant use. Group 1 con-
sisted of 12 children with duration of 63.25 ±5.20 months, and Group 2
comprised 13 children with duration of 76.38 ±2.95 months (p<.001).
Children who had their first implantation before the age of 4 years,
used bilateral implants regularly for at least 3 years after implant
activation, had an auditory implant fitting and audiological follow-up
within the last 6 months, and had hearing thresholds with ABIs of
30−45 dB HL (within the speech field) at frequencies of 500−4000 Hz
were included in the study. As the current assessment tools are appli-
cable to children aged 6 and above, the participants in the study were
selected from this specific age range. Since it is hypothesized that
long-term auditory deprivation could potentially affect cognitive and
sensory scores (Kral, 2013), all of children received their implants
before their fourth birthdays. All tests were conducted at the nor-
mal conversational level, with a defined threshold set to a minimum
of 45−60 dB HL hearing thresholds. The etiologies of hearing loss
in children, mostly comprising idiopathic hearing loss, include histo-
ries of anoxia, hyperbilirubinemia, consanguinity, prematurity and low
birth weight. All children were diagnosed with hearing loss through
newborn hearing screening and used hearing aids by the age of 6
months at the latest. In addition, all children diagnosed with hearing
loss received regular auditory rehabilitation and used auditory com-
munication methods. Children who were diagnosed with additional
disabilities in the cognitive, psychological, motor, social, and mental
areas who were not age appropriate, who were not cooperative with
the tests, and who did not volunteer to participate in the study were
excluded.
2.2 Assessment tools
The children were initially informed about the test instructions. A trial
module was initially applied for each test. To avoid confounding vari-
ables, all tests were administered by a single researcher using live
speech at a normal conversational level. The durationof the entire test-
ing session was approximately 30 min, and no cooperation difficulties
were observed in any child. The tests described below were used in this
study because of their specificity, validity, and reliability in reflecting
hearing-related cognitive skills.
2.2.1 Visual-Aural Digit Span Test B (VADS-B) form
This test was developed by Koppitz in 1977 to measure attention
and/or short-term memory. It is a neuropsychological test that com-
prehensively measures visual and auditory modalities and verbal and
written responses, and it also provides a measure of sequencing ability
(Koppitz, 1981). In the VADS-B, the numbers are presented audi-
tory or visually, and the responses are verbal or written. With this
structure, VADS-B measures sensation–response integration ability
as intrasensory (auditory–verbal (AV), visual–written (VW)) and inter-
sensory (auditory–written (AW), visual–verbal (VV)). It reflects the

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functions of the prefrontal cortex related to attention skills and the hip-
pocampus because of its relationship with short-term memory capacity
(Karaka¸s, 2013). The administration of the test consists of four stages:
AV, VV, AW, and VW (Berninger & Nagy, 2008). In the AV (Adam-
Darque et al., 2020) subtest, the sequences of numbers starting from a
sequence of 3, one number per second, are read to the participants, and
they are asked to repeat what they hear in order. In the VV subtest, the
numbers are shown one by one from a booklet, and the participants are
expected to say what they see in order. In the AW subtest, the children
are asked to write the number sequences they hear on a piece of paper
in order. In the VW (Berninger & Nagy, 2008) subtest, they are asked to
write the number sequences shown in the booklet in order. The high-
est number of correctly repeated sequences is recorded as the score.
This short-term memory capacity (i.e., memory span) varies at 7 ±2
units (Karaka¸s, 2013; Koppitz, 1981). The maximum score that can be
obtained from each of the subtests is 9.
2.2.2 Marking Test (MT)
This test was developed by Weintraub and Mesulam, and it measures
visual and spatial scanning and/or perception skills, attention, reaction
speed, and attack time (Karaka¸s, 2013). In MT performance, there is a
sensory component related to perceptual errors, a motor component
related to scanning and finding stimuli, and a motivational compo-
nent, including affective features (Karaka¸s, 2013). It is a visual–spatial
task involving sensory, motor, and affective components, as well as
sustained attention. MT findings are considered to reflect the right
cerebral hemisphere, especially parietal lobe functions (Lezak, 2004).
The MT consists of four test forms: regular letters, regular shapes,
irregular letters, and irregular shapes. Each MT form contains 60 tar-
get stimuli, 15 in each quarter of the page. The individual is expected
to encircle the target letter or shape as soon as possible without any
errors. Every time the individual marks 10 letters or shapes, the tester
gives a different color pen, and the marking continues with the new
color. The purpose of this is to map the direction and flow of visual–
spatial scanning. The best score for each form is 60. The completion
times are compared with the norm values according to age. The admin-
istration time of the test takes approximately 20 min (Karaka¸s, 2013).
In this study, the scanning time score was analyzed based on the MT
findings.
2.2.3 Dunn sensory profile questionnaire
This test was developed by Winnie Dunn in 1999 to measure sensory
processing skills and to determine their effect on the child’s daily life.
The Sensory Profile Questionnaire, whose Turkish validity and reliabil-
ity were confirmed by Kayıhan et al. (2015), is a standardized method
for evaluating a child’s functions in a wide range. It consists of 125 ques-
tions describing children’s responses to sensory input. The questions
are grouped into the sensory processing section, modulation section,
and behavioral and emotional responses section. A five-point Likert
scale is used, which is filled in according to the frequency of these
responses. As a result of the evaluation of the questionnaire, the raw
scores are given verbal categorical equivalents, such as definite differ-
ence, probable difference, and typical performance. The questionnaire
is completed by the parent or primary caregiver (Dunn, 1997;Dunn&
Daniels, 2002).
2.3 Statistical analysis
Statistical analysis was performed using the SPSS (statistical package
for the social sciences) version 26.0 software (IBM Corp.; Armonk,
NY, USA). The sample size was determined using the G*Power version
3.1 software (with the parameters: correlation of interest ρH1 =0.5,
αerror rate =0.05, power =0.85). Whether the data fit the normal
distribution was evaluated with histogram curves and bell curves. Per-
centage values for categories variables such as gender were used for
the descriptive statistics. The mean ±standard deviation values were
used in the descriptive statistics of age variable. Twenty-five children
with ABI satisfying the inclusion criteria were grouped according to
the duration of implant use. Group 1 consisted of 13 children with an
implant usage period of 60–75 months and Group 2 consisted of 12
children with a usage period of 75–90 months. The values of VADS-B
and MT were compared between groups. Student’s t-test or Mann–
Whitney Utest was used for two-group comparisons. In addition, the
correlation between sensory profile and VADS-B and the correlation
between sensory profile and Marking tests were examined. A p-value
of .05 was considered statistically significant.
3RESULTS
The mean age of the children in the Group 1 (7 female, 5 male) was
104.16 months (SD =7.42), and it was 99.61 months (SD =7.90) in the
Group 2 (6 female, 7 male). There was no statistically significant differ-
ence between the two groups in terms of chronological age (p=.136).
All children were diagnosed with hearing loss before 6 months and
started using bilateral hearing aids. Table 1presents the demographic
information of children. Accordingly, there was a statistically signifi-
cant difference between the groups in terms of duration of implant use
(p<.001).
The scores of Groups 2, which had been using the implant for
a longer time, were higher in the AV (p=.002), AW (p=.003),
auditory stimulation (p=.048), and verbal response (p=.045) cate-
gories of the VADS-B test and a statistically significant difference was
found between the groups. According to the sensory profile, Group 2
had higher scores and better sensory processing skills in registration
(p=.043), seeking (p=.001), inattention/distraction(p=.037), and per-
ceptual fine motor (p=.047), and a statistically significant difference
was found between the groups. In the marking test, Group 1 completed
the irregular letter (p=.003) and irregular shape (p=.009) steps in
a much longer time and a statistically significant difference was found
between the groups (Table 2).

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TAB LE 1 Demographic characteristics (N=25).
Group 1 Group 2
Mean ±standard deviation Mean ±standard deviation p
Age of hearing loss diagnosis (months) 4.25 ±1.35 5.00 ±1.08 .138
Onset age of hearing aid (months) 5.50 ±0.90 5.46 ±0.87 .915
Age of first implantation (months) 18.81 ±2.78 19.00 ±3.31 .887
Age of initial aural rehabilitation (months) 6.00 ±1.50 5.90 ±0.97 .850
Duration of implantation (months) 63.25 ±5.20 76.38 ±2.95 <.001
Gender 7 females (58%)5 males (42%) 6 females (46%)7 males (54%)
Note:p<.05 is statistically significant.
TAB LE 2 Comparison of VADS-B, MT, and DP according to duration of implant use.
Group 1
Mean/standard deviation
(n=13)
Group 2
Mean/standard deviation
(n=12) p
VADS-B auditory-verbal 3.41 ±0.66* 4.30 ±0.63* .002*
VADS-B auditory-written 2.58 ±0.79* 3.46 ±0.51* .003*
VADS-B auditory stimulation 96.69 ±8.93* 104.16 ±7.42* .048*
VADS-B verbalresponse [4.00–9.00]** [5.00–9.00]** .045*
VADS-B total 12.03 ±1.54 11.16 ±1.85 .066
MT regular letter duration 86.21 ±23.91 109.75±27.85 .057
MT regular shape duration 252.86 ±105.87 218.08 ±55.03 .066
MT irregular letter duration 309.00 ±89.40* 221.53 ±36.25* .003*
MT irregular shape duration 288.2580.75* 211.38 ±40.35* .009*
Registration [46.00–54.00]** [44.00–62.00]** .043**
Seeking 90.33 ±3.39 91.23 ±5.59 .001*
Sensitivity 101.92 ±7.63 101.16 ±6.46 .066
Avoidance 65.92 ±4.46 66.08 ±4.07 .787
Sensory input search 57.38 ±3.94 59.83 ±2.32 .787
Emotional response [51.00–63.00] [48.00–66.00] .787
Low endurance/tone 33.76 ±2.61 31.83 ±3.53 .395
Oral sensory sensitivity 33.23 ±4.06 31.08 ±4.60 .100
Inattention/distraction 13.91 ±1.03* 17.15 ±2.11* .037*
Poor registration [24.00–31.00] [23.00–31.00] .787
Sensory sensitivity 13.46 ±2.43 14.08 ±2.35 .653
Motionless [9.00–16.00]** [8.00–16.00]** .395
Perceptual fine motor 6.92 ±0.86* 8.00 ±0.85* .047*
Note: *Independent t-test, **Mann–Whitney Utest, p<.05 is statistically significant. Bolded areas indicate that the statistical analysis is significantly different.
In the study group consisting of 25 children using ABI, the rela-
tionships between sensory processing and attention and memory skills
were evaluated and shown in Tables 3and 4. The lower the scores
obtained by the children in the sensory profile evaluation, the greater
the difference between them and their peers. There is a significant pos-
itive correlation between the sensory profile and the subparameters of
VAD S-B (p<.05). There is a significant positive correlation between
registration and auditory verbal, auditory written and general scores
(respectively r=.356, r=.427, r=.355, and p<.005). There is a positive
correlation between sensitivity and auditory stimulation; positive cor-
relation between sensory input seeking and auditory stimulation and
general score; positive correlation between inattention and auditory
verbal, auditory written; positive correlation between perceptual fine
motor and auditory written (Table 3).
Among the subparameters of sensory profile and MT, there is a neg-
ative correlation between seeking and MT regular letter duration, MT
regular shape duration, MT regular shape duration, MT irregular shape
duration; there is a negative correlation between inattention/attention

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TAB LE 3 Correlation between sensory profile and VADS-B.
VAD S- B
auditory-verbal
VAD S- B au di to ry
stimulation
VAD S- B
auditory-written
VADS-B verbal
response
VAD S- B
total
Registration r
p
.356*
.037
−178
.395
.427*
.040
.099
.637
.355*
.039
Seeking r
p
.115
.585
.020
.923
.211
.311
−.139
.506
.269
.193
Sensitivity r
p
.013
.951
.047
.824
−065
.758
−.117
.579
.086
.682
Avoidance r
p
.038
.856
.456*
.022
.050
.811
−.283
.171
−.282
.172
Sensory input search r
p
.197
.346
.348*
.028
.237
.254
−.287
.165
.362*
.036
Emotional response r
p
−.104
.622
−.108
.608
.037
.860
.059
.781
−.021
.919
Low endurance/tone r
p
−.176
.401
−.127
.544
−.130
.536
−.185
.375
−.148
.480
Oral sensory sensitivity r
p
−.346
.090
−.008
.971
.010
.964
.091
.666
.039
.854
Inattention/distraction r
p
.460*
.021
−.007
.973
.374*
.046
.033
.877
.127
.545
Poor registration r
p
.088
.676
.098
.641
.183
.381
.125
.552
.038
.856
Sensory sensitivity r
p
.051
.807
.006
.976
.340
.097
.252
.224
−.014
.946
Motionless r
p
.168
.304
.094
.709
.214
.656
.079
.593
.000
.421
Perceptual fine motor r
p
.017
.936
−.048
.820
.382*
.037
.010
.963
−.150
.475
Note: Spearman’s/Pearson’s correlation; *correlation is significant at the .05 level. Bolded areas indicate that the statistical analysis is significantly different.
deficit and MT regular shape duration, MT irregular shape duration, MT
irregular letter duration (Table 4).
4DISCUSSION
Auditory deprivation at an early age can have complex effects on the
brain’s remodeling and the processing abilities of other intact senses
(Bharadwaj et al., 2012; Finney & Dobkins, 2001; Heming & Brown,
2005). The processing of environmental and body senses is important
in the development of cognitive skills that are effective in all devel-
opmental areas of children. Children with severe/profound hearing
loss have difficulty recording and using information because they can-
not receive auditory stimuli with all their acoustic properties (Kutlu
et al., 2021). This condition causes limitations in short-term mem-
ory and working memory and affects children’s language development
and social and cognitive skills (Abraham et al., 2016; Yildirim Gökay
&Yücel,2023; Yıldırım Gökay & Yücel, 2021). Moreover, as children
with hearing loss cannot fully receive auditory stimuli, they spend more
effort listening and their attention span is shortened (Hicks & Tharpe,
2002). Thus, the cognitive skills and sensory processing skills of chil-
dren with hearing loss should be supported, and these children should
be included in rehabilitation programs.
Early initial auditory input is important because it provides plasticity
and remodeling of the brain and supports sensory integration. Stud-
ies have shown that children with early initial and long-term use of
cochlear implants (CIs) have better language development and social
and cognitive skills (Yıldırım Gökay & Yücel, 2021). In these studies,
some of children using CIs caught up with their peers, those using
ABIs showed a significant improvement in some cognitive parame-
ters related to selective visual attention and multisensory executive
functions over time, although they could not catch up with their
peers (Almomani et al., 2021; Colletti, 2007). Moreover, it has been
recommended that children with cochlear anomalies associated with
cognitive impairments should not be deprived of ABI intervention
(Colletti & Zoccante, 2008). Colletti (2007) evaluated the nonverbal
cognitive skills and hearing performance of children using ABIs and
found that improvement in auditory perception caused a significant
improvement in cognitive parameters. Another study emphasized that
children using ABIs needed more improvement in terms of memory and
attention processes (Yücel et al., 2015).
When we grouped the participants in the study according to the
duration of ABI use, the children who used implants for a shorter
period of time had lower scores in auditory presentation verbal
response, visual presentation verbal response, auditory presentation
written response, and verbal response steps in the VADS-B test. In this

BA¸SET AL.7of10
TAB LE 4 Correlation between sensory profile and marking test.
MT regular letter
duration
MT regular shape
duration
MT irregular letter
duration
MT irregular shape
duration
Registration r
p
−.044
.836
−.098
.643
−.062
.769
−.100
.635
Seeking r
p
−.391*
.032
−.439*
.038
−.079
.707
−.339*
.024
Sensitivity r
p
.464*
.020
.079
.708
.076
.717
−.117
.579
Avoidance r
p
.261
.207
−.178
.396
.256
.217
−.014
.949
Sensory input search r
p
−.132
.531
−.153
.625
−.292
.156
−.088
.677
Emotional response r
p
.363
.074
.006
.977
.172
.412
.016
.940
Low endurance/tone r
p
.177
.397
.304
.140
.392
.053
.134
.523
Oral sensory sensitivity r
p
.192
.357
.080
.702
.297
.149
.140
.460
Inattention/distraction r
p
−.481*
.025
−.308*
.034
−.399*
.043
−.408*
.048
Poor registration r
p
.246
.235
−.048
.820
.368
.071
.177
.397
Sensory sensitivity r
p
−.041
.847
−.248
.232
.049
.815
.096
.647
Motionless r
p
.259
.212
−.154
.462
−.108
.606
.129
.537
Perceptual fine motor r
p
−.050
.813
.134
.523
−137
.512
.168
.423
Note: Spearman’s/Pearson’s correlation; *correlation is significant at the .05 level. Bolded areas indicate that the statistical analysis is significantly different.
situation, the participants had more difficulty in auditory and verbal
tasks in which hearing, and language skills intensified. On the contrary,
when intersensory interaction was required, no difference was found
in the different task combinations, especially in the visual and written
substeps. It could be that children using ABIs have weakerauditory per-
ception and develop visual skills because they mostly use lip reading
and sign language (Yildirim Gökay & Yücel, 2024).
The difference between the two groups in terms of visual and spatial
scanning and/or perception visual selectivity and visual–motor syn-
chronization skills measured by the MT in terms of irregular letter and
shape durations may be due to the weaker sensory integration skills
of children who used ABIs for shorter period of time. In this task, the
children were asked to mark the targets in an organized manner using
fine motor skills in a form containing confusing stimuli along with the
target shape or letter. Differences were found between the groups in
sensory processing parameters in terms of registration, searching, and
fine motor skills.
Sensory integration is a process that requires continuity. Propri-
oceptive, vestibular, and tactile systems constitute the basic senses
of this integration in developmental stages (Ayres & Robbins, 2005).
In sensory integration studies of children with hearing loss, the cur-
rent situation has been linked to the degree of hearing loss of the
child, the duration of amplification use, the duration of rehabilita-
tion, and the presence of additional disabilities rather than the device
used (Coulson-Thaker, 2020; Veronese et al., 2023). According to a
study in which children using ABI were compared with those using
CIs, children using ABIs were weaker in the vestibular system, move-
ment modulation, and inattention substeps in the sensory profiles and
more successful in visual processing (Ba¸s&Yücel,2023). In the cur-
rent study, the duration of use affected sensory integration, which is
consistent with the literature. Children with short-term use showed
weaker performance in the Dunn sensory profile substeps of regis-
tration, inattention, and fine motor skills, while children in this group
were more mobile and sensory seeking. The sensory profiles of children
affect all stages of academic, social, and cognitive development as well
as communication and learning skills (Dunn, 1997).
The registration parameters of the sensory profile are the percep-
tion of the sensory stimulus and the recording of the sensory stimulus
(Dunn & Daniels, 2002). Children who fail to meet the norm values
in this area do not react because they cannot perceive the stimuli
and have difficulty fulfilling the tasks. When the relationship between
the sensory profile and the VADS-B, in which short-term memory and
working memory skills are evaluated, there is a positive correlation
between registration and AV, AW, and general scoring. This may be

8of10 BA ¸SET AL.
due to the children’s limitations, especially in perceiving and recording
auditory stimuli. Sensory input seeking refers to the need for differ-
ent sensory stimuli to regulate children’s senses, ensure concentration,
and control behavior (Ayres & Robbins, 2005). We find that the pos-
itive correlation between sensory seeking and auditory stimulation
and overall scores is due to children’s regulation skills, low concen-
tration, and high listening effort. It has been shown that inattention
in the sensory profiles of children using ABIs may be related to dif-
ficulties in sensory seeking, registration, and listening skills. There is
a negative correlation between regular shape and letter duration and
between irregular shape and letter duration, which are evaluated in the
MT findings that specifically measure selective attention and sustained
attention skills and search and inattention/distraction from the sen-
sory profile substeps. To provide sensory and emotional regulation, to
express themselves at the point of communication, or to attract atten-
tion by showing themselves, individuals behave veryactively, show that
they are in a sensory search, and have difficulty recording the sensa-
tions they obtain. Although it cannot be generalized with the current
sample size, it is considered that their concentration time is short, and
the time required to complete the test is longer due to their sensory
search and recording limitations.
The limitations in attention and memory skills and the behaviors
and attitudes of children using ABIs may be confused with conditions
such as attention deficit hyperactivity disorder and autism. Another
limitation of the study is the diverse brands of devices used by the chil-
dren. All ABI-using children who participated in the study had inner ear
anomalies, but the inability to make a specific classification due to the
small number of participants is one limitation of the study. The sample
size should be expanded by considering etiologies. There is a need for a
more rigorous methodological approach and further research on this
topic. Although the applied tests yielded excellent results, definitive
conclusions could not be drawn based solely on correlations. Con-
founding variables, such as the duration of ABI usage, age at hearing
loss diagnosis, and the etiologies of hearing loss, need to be considered.
Understanding the sensory sensitivity and reactions of a child is also
important for the rehabilitation process.
5CONCLUSIONS
This study demonstrated the importance of auditory and sensory pro-
cessing in the development of cognitive and executive functions. The
effects of sensory profiles and sensory processing skills on the reha-
bilitation of children with ABIs should be taken into consideration. In
this process, a holistic and early evaluation is needed to prevent prob-
lems that children may experience. A multidisciplinary team should
determine the unique needs and strengths of children and develop
appropriate support and intervention strategies.
AUTHOR CONTRIBUTIONS
Banu BA¸S: Software; methodology; conceptualization; resources;
project administration; writing—original draft; writing—review and
editing; investigation. Nuriye Yıldırım Gökay: Visualization; writing—
review and editing. Zehra Aydo˘
gan: Formal analysis. Esra Yücel:
Supervision; conceptualization.
ACKNOWLEDGMENTS
Open acess funding provided by Türkiye Bilimsel ve Teknolojik
Ara¸stırma Kurumu.
FUNDING
The authors declare that they were not funded for this study.
CONFLICT OF INTEREST STATEMENT
The authors have no conflict of interest to declare.
DATA AVAILABILITY STATEMENT
All data generated or analyzed during this study are included in this
article. Further enquiries can be directed to the corresponding author.
ORCID
Banu BA ¸Shttps://orcid.org/0000-0002-2521-4545
PEER REVIEW
The peer review history for this article is available at https://publons.
com/publon/10.1002/brb3.3637.
REFERENCES
Abraham, A., George, V. M., & Kunnath, S. (2016). Auditory short term
memory and academic achievement in normal school going children.
International Journal of Health Sciences & Research,6(1), 480–483.
Adam-Darque, A., Pittet, M. P., Grouiller, F., Rihs, T. A., Leuchter, R. H.-V.,
Lazeyras, F., Michel, C. M., & Hüppi, P. S. (2020). Neural correlates of
voice perception in newborns and the influence of preterm birth. Cerebral
Cortex,30(11), 5717–5730.
Almomani, F., Al-Momani, M. O., Garadat, S., Alqudah, S., Kassab, M.,
Hamadneh, S., Rauterkus, G., & Gans, R. (2021). Cognitive functioning in
Deaf children using Cochlear implants. BMC Pediatrics,21, 1–13.
Aslan, F., Yücel, E., Sennaroglu, G., Yaralı, M., & Sennaroglu, L. (2022). Audi-
ological outcome with ABI. In L. Sennaroglu (Ed.),Inner ear malformations:
Classification, evaluation and treatment (pp. 349–361). Springer.
Atkinson, R. C., & Shiffrin, R. M. (1968). Human memory: A proposed system
and its control processes. In K. W. Spence & J.T. Spence (Eds.), Psychology
of learning and motivation (Vol. 2, pp. 89–195). Elsevier.
Ayres, A. J.,& Robbins, J. (2005). Sensory integration and the child: Understand-
ing hidden sensory challenges. Western Psychological Services.
Baddeley, A. (2007). Working memory, thought, and action (Vol. 45). Oxford
University Press.
Ba¸s, B., & Yücel, E. (2023). Sensory profiles of children using cochlear
implant and auditory brainstem implant. International Journal of Pediatric
Otorhinolaryngology,170, 111584.
Berninger, V., & Nagy, W. (2008). Flexibility in word reading: Multiple levels
of representations, complex mappings, partial similarities and cross-
modal connections. In K. B. Cartwright (Ed.),Literacy processes: Cognitive
flexibility in learning and teaching. The Guilford Press.
Bharadwaj, S. V., Matzke, P. L., & Daniel, L. L. (2012). Multisensory process-
ing in children with cochlear implants. International Journal of Pediatric
Otorhinolaryngology,76(6), 890–895.
Cohen, R. A., Sparling-Cohen, Y. A., & O’Donnell, B. F. (1993). The neuropsy-
chology of attention. Springer.

BA¸SET AL.9of10
Colletti, L. (2007). Beneficial auditory and cognitive effects of auditory
brainstem implantation in children. Acta Oto-Laryngologica,127(9), 943–
946.
Colletti, L., Shannon, R. V.,& Colletti, V. (2015). The development of auditory
perception in children after auditory brainstem implantation. Audiology
and Neurotology,19(6), 386–394.
Colletti, L., & Zoccante, L. (2008). Nonverbal cognitive abilities and audi-
tory performance in children fitted with auditory brainstem implants:
Preliminary report. The Laryngoscope,118(8), 1443–1448.
Colletti, V.,Carner, M., Miorelli, V., Guida, M., Colletti, L., & Fiorino, F.(2005).
Auditory brainstem implant (ABI): New frontiers in adults and children.
Otolaryngology—Head and Neck Surgery,133(1), 126–138.
Colletti, V., Shannon, R. V., Carner, M., Veronese, S., & Colletti, L. (2009).
Progress in restoration of hearing with the auditory brainstem implant.
Progress in Brain Research,175, 333–345.
Conway, C. M., Pisoni, D. B., & Kronenberger, W. G. (2009). The impor-
tance of sound for cognitive sequencing abilities: The auditory scaf-
folding hypothesis. Current Directions in Psychological Science,18(5),
275–279.
Coulson-Thaker, K. (2020). Exploring sensory processing among hear-
ing impaired and culturally deaf children. PhD Thesis, University of
Hertfordshire.
da Silva Lima, J. V., de Morais, C. F. M., Zamberlan-Amorim, N. E., Mandrá,
P. P., & Reis, A. C. M. B. (2023). Neurocognitive function in children with
cochlear implants and hearing aids: A systematic review. Fronti ers in
Neuroscience,17, 1242949.
De Giacomo, A., Craig, F., D’Elia, A., Giagnotti, F., Matera, E., & Quaranta,
N. (2013). Children with cochlear implants: Cognitive skills, adaptive
behaviors, social and emotional skills. International Journal of Pediatric
Otorhinolaryngology,77(12), 1975–1979.
Dunn, W.(1997). The impact of sensory processing abilities on the daily lives
of young children and their families: A conceptual model. Infants & Young
Children,9(4), 23–35.
Dunn, W. (2001). The sensations of everyday life: Empirical, theoretical, and
pragmatic considerations. The American Journal of Occupational Therapy,
55(6), 608–620.
Dunn, W., & Daniels, D. B. (2002). Initial development of the infant/toddler
sensory profile. Journal of Early Intervention,25(1), 27–41.
Edwards, L., Khan, S., Broxholme, C., & Langdon, D. (2006). Exploration
of the cognitive and behavioural consequences of paediatric cochlear
implantation. Cochlear Implants International,7(2), 61–76.
Ertugrul, G., Aslan, F., Sennaroglu, G., & Sennaroglu, L. (2021). Children with
auditory brainstem implant: How do they perform in motor and language
skills? Audiology and Neurotology,26(3), 173–181.
Fawcett, J., Risko, E., & Kingstone, A. (2015). The handbook of attention.MIT
Press.
Finney, E. M., & Dobkins, K. R. (2001). Visual contrast sensitivity in deaf
versus hearing populations: Exploring the perceptual consequences of
auditory deprivation and experience with a visual language. Cognitive
Brain Research,11(1), 171–183.
Glaubitz, C., Liebscher, T., & Hoppe, U. (2021). Age-related language per-
formance and device use in children with very early bilateral cochlear
implantation. International Journal of Pediatric Otorhinolaryngology,147,
110780.
Hassanzadeh, S., Ajalloueyan, M., Mirdeharbab, A., Arjmandnia, A. A.,
Hasanalifard, M., Saeedi, M., & Aghaz, A. (2021). Long-term effects
of cochlear implantation on language skills-and speech intelligibility in
early-implanted versus late implanted deaf children. International Journal
of Pediatrics,9(10), 14663–14671.
Heming, J. E., & Brown, L. N. (2005). Sensory temporal processing in adults
with early hearing loss. Brain and Cognition,59(2), 173–182.
Herbert, C. J., Kronenberger, W. G., Wolfert, K., Nelson, R. F., Yates, C. W., &
Pisoni, D. B. (2023). Extraordinary speech and language outcomes after
auditory brainstem implantation: Guidance from a case study. American
Journal of Audiology,32(4), 761–778.
Hicks, C. B., & Tharpe, A. M. (2002). Listening effort and fatigue in school-
age children with and without hearing loss. Journal of Speech, Language,
and Hearing Research,45(3), 573–584.
Karaka¸s, S. (2013). Bilnot-Yeti ¸skin (2 Cilt Takım).E˘
gitim Yayinevi.
Kayihan, H., Akel, B. S., Salar, S., Huri, M., Karahan, S., Turker, D., & Korkem,
D. (2015). Developmentof a Turkish version of the sensory profile: Trans-
lation, cross-cultural adaptation, and psychometric validation. Perceptual
and Motor Skills,120(3), 971–986.
Koppitz, E. M. (1981). The visual aural digit span test for seventh graders: A
normative study. Journal of Learning Disabilities,14(2), 93–95.
Köse, B., Karaman-Demirel, A., & Çiprut, A. (2022). Psychoacoustic abili-
ties in pediatric cochlear implant recipients: The relation with short-term
memory and working memory capacity. International Journal of Pediatric
Otorhinolaryngology,162, 111307.
Kral, A. (2007). Unimodal and cross-modal plasticity in the ‘deaf’auditory
cortex. International Journal of Audiology,46(9), 479–493.
Kral, A. (2013). Auditory critical periods: A review from system’s perspec-
tive. Neuroscience,247, 117–133.
Kral, A., Dorman, M. F., & Wilson, B. S. (2019). Neuronal development of
hearing and language: Cochlear implants and critical periods. Annual
Review of Neuroscience,42, 47–65.
Kutlu, S., Ozkan, H. B., & Yucel, E. (2021). A study on the association of
functional hearing behaviors with semantics, morphology and syntax in
cochlear-implanted preschool children. International Journal of Pediatric
Otorhinolaryngology,148, 110814.
Lezak, M. D. (2004). Neuropsychological assessment.Oxford University Press.
Nicastri, M., Giallini, I., Inguscio, B. M. S., Turchetta, R., Guerzoni, L., Cuda,
D., Portanova, G., Ruoppolo, G., Dincer D’Alessandro, H., & Mancini, P.
(2023). The influence of auditory selective attention on linguistic out-
comes in deaf and hard of hearing children with cochlear implants.
European Archives of Oto-Rhino-Laryngology,280(1), 115–124.
Peñeñory, V. M., Manresa-Yee, C., Riquelme, I., Collazos, C. A., & Fardoun,
H. M. (2018). Scoping review of systems to train psychomotor skills in
hearing impaired children. Sensors,18(8), 2546.
Pisoni, D. B., Kronenberger, W. G., Chandramouli, S. H., & Conway, C. M.
(2016). Learning and memory processes following cochlear implanta-
tion: The missing piece of the puzzle. Frontiers in Psychology,7, 493.
Saksida, A., Ghiselli, S., Picinali, L., Pintonello, S., Battelino, S., & Orzan,
E. (2022). Attention to speech and music in young children with bilat-
eral Cochlear implants: A Pupillometry study. Journal of Clinical Medicine,
11(6), 1745.
Schierholz, I., Schönermark, C., Ruigendijk, E., Kral, A., Kopp, B., & Büchner,
A. (2021). An event-related brain potential study of auditory attention in
cochlear implant users. Clinical Neurophysiology,132(9), 2290–2305.
Sennaro˘
glu, L., Colletti, V., Lenarz, T., Manrique, M., Laszig, R., Rask-
Andersen, H., Göksu, N., Offeciers, E., Saeed, S., Behr, R., Bayazıt,
Y., Casselman, J., Freeman, S., Kileny, P., Lee, D. J., Shannon, R. V.,
Kameswaran, M., Hagr, A., Zarowski, A., .. . Behr, R. (2016). Consen-
sus statement: Long-term results of ABI in children with complex inner
ear malformations and decision making between CI and ABI. Cochlear
Implants International,17(4), 163–171.
Sennaroglu, L., Sennaroglu, G., & Atay, G. (2013). Auditory brainstem
implantation in children. Current Otorhinolaryngology Reports,1, 80–91.
Steinberg, L. (2010). Commentary: A behavioral scientist looks at the
science of adolescent brain development. Brain and Cognition,72(1), 160.
Veronese, S., Cambiaghi, M., Tommasi, N., Sbarbati, A., & Galvin III, J. J.
(2023). Ten-year follow-up of auditory brainstem implants: From intra-
operative electrical auditory brainstem responses to perceptual results.
PLoS ONE,18(3), e0282261.
Williamson, G. G., & Anzalone, M. E. (2001). Sensory integration and self-
regulation in infants and toddlers: Helping very young children interact with
their environment.ERIC.
Yıldırım Gökay, N., Demirta¸s, B., Özbal Batuk, M., Yücel, E., & Sennaro ˘
glu,
G. (2024). Auditory performance and language skills in children with
auditory brainstem implants and cochlear implants. European Archives of

10 of 10 BA¸SET AL.
Oto-Rhino-Laryngology,10.1007/s00405-024-08594-0. Advance online
publication.
Yıldırım Gökay, N., & Yücel, E. (2021). Bilateral cochlear implantation:
An assessment of language sub-skills and phoneme recognition in
school-aged children. European Archives of Oto-Rhino-Laryngology,278,
2093–2100.
Yildirim Gökay, N., & Yücel, E. (2023). Evaluation of language, attention,
and memory skills in children with auditory brainstem implants. European
Archives of Oto-Rhino-Laryngology,281(4), 1683–1692.
Yildirim Gökay, N., & Yücel, E. (2024). Evaluation of language, attention,
and memory skills in children with auditory brainstem implants. European
Archives of Oto-Rhino-Laryngology,281(4), 1683–1692.
Yücel, E., Aslan, F., Özkan, H. B., & Sennaro˘
glu, L. (2015). Recent rehabil-
itation experience with pediatric ABI users. The Journal of International
Advanced Otology,11(2), 110–113.
How to cite this article: BA¸S,B.,Gökay,N.Y.,Aydo˘
gan, Z., &
Yücel, E. (2024). Do auditory brainstem implants favor the
development of sensory integration and cognitive functions?
Brain and Behavior,14, e3637.
https://doi.org/10.1002/brb3.3637