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Background: A large group of young children are exposed to repetitive middle ear infections but the effects of the fluctuating hearing sensations on immature central auditory system are not fully understood. The present study inves‑ tigated the consequences of early childhood recurrent acute otitis media (RAOM) on involuntary auditory attention switching. Methods: By utilizing auditory event‑ related potentials, neural mechanisms of involuntary attention were studied in 22–26 month‑ old children (N = 18) who had had an early childhood RAOM and healthy controls (N = 19). The earlier and later phase of the P3a (eP3a and lP3a) and the late negativity (LN) were measured for embedded novel sounds in the passive multi‑ feature paradigm with repeating standard and deviant syllable stimuli. The children with RAOM had tympanostomy tubes inserted and all the children in both study groups had to have clinically healthy ears at the time of the measurement assessed by an otolaryngologist. Results: The results showed that lP3a amplitude diminished less from frontal to central and parietal areas in the children with RAOM than the controls. This might reflect an immature control of involuntary attention switch. Further ‑ more, the LN latency was longer in children with RAOM than in the controls, which suggests delayed reorientation of attention in RAOM. Conclusions: The lP3a and LN responses are affected in toddlers who have had a RAOM even when their ears are healthy. This suggests detrimental long‑ term effects of RAOM on the neural mechanisms of involuntary attention. Keywords: Otitis media, Involuntary attention, Orienting, ERPs, P3a, Late negativity episodes per year . After an episode of AOM, mid- Background dle ear fluid is present for few days to over 2 months [ 4]. About 30 % of children have recurrent middle ear infec- Fluid in the middle ear causes about 20–30 dB conduc- tions (recurrent acute otitis media, RAOM) in their early tive hearing loss , and, especially when asymmetric, childhood [1, 2]. Due to challenges in diagnosing and it affects interaural temporal and level difference cues classifying middle ear status, otitis media (OM) is com- compromising binaural sound localization . Fluctuat- monly used as a general term for various forms of mid- ing hearing sensations during the development of central dle ear fluid and inflammation. A general definition for auditory system has been connected to atypical auditory RAOM has been three or more episodes of acute oti- processing [7–11], which can lead to problems in lan- tis media (AOM) per 6 months or four or more AOM guage acquisition . Therefore, it is necessary to get a better understanding of the consequences of early child- hood RAOM on immature central nervous system. *Correspondence: email@example.com Department of Speech and Language Pathology, Faculty of Social Behavioral studies in children with OM have shown Sciences, Publicum, University of Turku, 20014 Turku, Finland problems in regulation of auditory attention [13–18]. Full list of author information is available at the end of the article © 2016 Haapala et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Haapala et al. Behav Brain Funct (2016) 12:1 Page 2 of 8 Involuntary orientation to environmental events as adults but the scalp topography of children’s P3a is more well as selective maintenance of attention is essential anterior than that of adults . The eP3a may mature for speech processing and language learning. Involun- earlier than lP3a, which continues to enhance frontally tary attention accounts for the detection and selection during development . Hence, processing of acoustic of potentially biologically meaningful information of novelty in the childhood resembles that in the adulthood events unrelated to the ongoing task . For example, although some underlying neural networks still continue a screeching noise of a braking car causes an attention to develop. Atypical P3a responses have been connected switch of a pedestrian who is talking on the phone, and to abnormal involuntary attention, for example, parietally leads to the distraction of the ongoing activity. After the enhanced lP3a was found in children with attention defi - evaluation of the irrelevant novel stimulus, the reorienta- cit hyperactivity disorder (ADHD) . tion back to the recent activity takes place. Involuntary The ERP waveform also reflects reorienting of attention attention is a bottom-up (stimulus-driven) process  back to the primary task after recognizing and evaluating but during maturation the developing top-down mecha- a distracting stimulus [35, 36]. In adults, P3a is followed nisms start to inhibit distractors which are not meaning- by reorienting negativity (RON) . A counterpart of ful, in other words, children learn to separate relevant RON in children was suggested to be the late negativ- from irrelevant stimuli [20, 21]. An excessive tendency ity (LN, also called as negative component, Nc) [28–31]. to orient to the irrelevant stimuli requiring a lot of atten- The LN latency, peaking at around 400–700 ms after the tional resources makes goal-directed behavior harder onset of a novel stimulus, reflects reorienting time . . The LN has the maximal amplitude at fronto-central School-aged children with OM history were shown to scalp areas . Large LN reflects enhanced neural effort have deficits of selective auditory attention in dichotic to reorienting  or more attention paid to the surpris- listening tasks [13–15]. They also showed increased reor - ing event . During maturation, the LN amplitude has ientation time of attention during behavioral tasks . been suggested to decrease [30, 34]. Rated by their teachers, school-children with OM his- The aim of this study was to compare the involuntary tory were suggested to be less task-oriented  but not attentional mechanisms in 2-year-old healthy children in all studies . Studies in toddlers are scarce, prob- with RAOM history and their healthy age-matched con- ably due to the weak co-operation skills in children at trols by recording auditory ERPs. For that purpose, novel this age. However, toddlers with chronic OM were shown stimuli were embedded in the multi-feature paradigm to express reduced attention during book reading at the with syllables to elicit eP3a, lP3a, and LN. It was hypoth- time of middle ear effusion and, according the question - esized that children with RAOM would show atypically naire, their mothers rated them as easily distractible . enhanced and/or short latency P3a reflecting enhanced The neural mechanisms beyond these findings are still distractibility for the intrusive novel sounds and to have unknown. larger amplitude and/or longer latency of LN indicating Event-related potentials (ERPs) are a feasible approach more neural effort to reorienting and/or longer re-orien - for studying non-invasively neural mechanisms of invol- tation time of attention than their healthy peers. Studies untary auditory attention without tasks requiring co- of P3a and novelty-related LN in toddlers are scarce and operation skills . The auditory P3a is a large positive to our knowledge, this is the first study measuring these deflection elicited by unexpected, novel sounds which responses in children with RAOM. substantially differ from other sounds, for example slam of the door or human cough. The P3a reflects involuntary Methods attention mechanisms and orientation of attention . Participants It peaks fronto-centrally at 200–300 ms after the onset of Twenty-four children with a middle ear infection history a distracting stimulus [22, 25, 26]. were recruited to the RAOM group (at least three AOM P3a was often found to be biphasic [22, 27]. Two per 6 months or four AOM per 1 year) from the Ear, phases, early and late, have been identified in children Nose and Throat clinic of Oulu University hospital. Dur - [28–30] already at the age of 2 years . Early P3a (eP3a) ing 1 year in 2009–2010, all children aged 22–26 months was suggested to reflect the automatic detection of vio - fulfilling the criteria of this study with a tympanostomy lation in the neural model of existing world and thus, to tube insertion participated (for a more detailed AOM represent the orientation of attention . It is maximal history see ). The EEG recording was done on aver - at vertex and diminishes posteriorly and laterally . In age 33 days (range 20–56 d) after the tympanostomy contrast, late P3a (lP3a) was suggested to reflect actual tube insertion. Twenty-two age matched control children attention switch and it is maximal frontally . Mor- with 0–2 AOM were recruited with public advertise- phology of these responses is quite similar in children and ments. All families participated voluntarily to the study Haapala et al. Behav Brain Funct (2016) 12:1 Page 3 of 8 and an informed written consent was obtained from the the final groups in gender (RAOM: 10 boys; controls 11 parents of children. Families were paid 15€ for travelling boys), age (RAOM: mean 24 months, min–max 22–26; costs. The study was in accordance of Declaration of Hel - controls: mean 24 months, min–max 22–26), or mother’s sinki and approved by the Ethics Committee of North- education (RAOM: 4 low, 13 middle or high; controls 2 ern Osthrobotnia Hospital District (reference number low, 17 middle or high). The educational information of 6/2009). one mother in the RAOM group was not available. Participants were from monolingual Finnish-speaking families. They were born full-term with normal birth Stimuli and experimental design weight, and developing typically in their sensory, cogni- ERPs were recorded in a passive condition with the tive, and motor skills according to parental question- multi-feature paradigm (“Optimum-1”), which was naires and the examinations at the family and health care shown to be a fast and eligible method for obtaining clinics during the first 2 years of life. No family history several ERPs reflecting different stages of auditory pro - of speech, language, or other developmental impair- cessing in adults [40–42], school-aged children [43, 44], ments or severe neuropsychiatric diseases was allowed. and toddlers [45, 46]. In the multi-feature paradigm, The standardized Finnish version of Reynell Develop - the standard and the deviant sounds are presented in mental Language Scales III, the Comprehension scale the same sequence so that every other stimulus is the [38, 39] was applied to exclude developmental language standard and every other stimulus is one of the several disorders. At the time of the EEG recording, transient deviants. In the deviants, only one sound feature (e.g., evoked otoacoustic emissions (TEOAEs; nonlinear click vowel or frequency) of the standard stimulus is changed sequence 1.5–4.5 kHz, 73 dB SPL, pass/refer result; at a time while the other features remain the same and MADSEN AccuScreen pro, GN Otometrics, Taastrup, strengthen the memory representation of the standard Denmark) were checked. Four children with RAOM and stimulus. To study attentional mechanisms, distracting six control children did not co-operate in the TEOAE novel sounds may also be embedded in the same sound measurement, but all the children had passed a TEOAE stream [42, 45, 46]. screening at a postnatal period in Oulu University Hos- The standards were Finnish semisynthetic consonant– pital. Right before the EEG recording, all children were vowel syllables/ke:/or/pi:/(duration 170 ms). Every other assessed with pneumatic otoscopy and if needed by tym- stimulus sequence included standard/ke:/and every other panometry and/or otomicroscopy by an otolaryngologist included standard/pi:/. The deviants (duration 170 ms) to ensure that they had clinically healthy ears at the time were five different deviations in these syllables (frequency of the measurement. F0 ± 8 Hz, intensity ± 7 dB, consonant from/ke:/to/pe:/ In the RAOM group, one child was excluded because and from/pi:/to/ki:/, vowel from/ke:/to/ki:/and from/pi:/ of a family history of dyslexia and one because the results to/pe:/, and vowel duration from syllable length of 170 ms of the Reynell III did not meet the criteria for normal to 120 ms) [42, 47]. The obligatory and MMN responses speech comprehension, and an additional examination elicited by standards and deviants were reported earlier of speech-language pathologist showed signs of severe . In addition, there were totally differing novel sounds language disorder. Two children with RAOM had atypi- (duration 200 ms, including a fall and a rise time of cally enhanced P3a responses (24.07 and 23.20 µV), and 10 ms), which were non-synthetic, environmental human the statistical analysis indicated them to be outliers, i.e., (e.g. coughs and laughs) or non-human (e.g. door slam- their responses being at abnormal distance from the ming and telephone ringing) sounds . In the stimulus other ones (2.51–17.63 µV). Because we hypothesized sequence, every other stimulus was a standard (probabil- that the children with RAOM would have enhanced P3a ity 50 %) and every other was one of the deviants (proba- responses, we decided to exclude these two children from bility 8.3 % for each) or a novel sound (probability 8.3 %). the further analysis to avoid the bias of these extreme The presentation of stimuli was pseudo-randomized so values on the results of the RAOM group. Furthermore, that all five deviants and one novel stimulus appeared two children did not arrive to the measurement at the once among 12 successive stimuli, and the same deviant appointed time. In the control group, two children had to or novel was never repeated after the standard stimulus be excluded from the analysis because of a large amount following it. The stimulus onset asynchrony was 670 ms. of alpha activity in their EEG leading to low signal-to- The stimuli were in the sequences lasting for about noise ratio. One control children was excluded because 6 min., each starting with 10 standards, and including of acute OM diagnosed at the time of measurement. 540 stimuli from which 275 were standards and 44 were The total number of children in this study was 18 in the novels sounds, the rest being deviant syllables (44 of each RAOM group and 19 in the control group after these deviant type). Three to four stimulus sequences were pre - exclusions. There were no significant differences between sented to each participant. Haapala et al. Behav Brain Funct (2016) 12:1 Page 4 of 8 Stimuli were presented in an electrically shielded and of epochs for standard and novel stimuli in the RAOM sound-attenuated room (reverberation time .3 s, back- group was 675 (min–max 373–856) and 133 (min–max ground noise level 43 dB) with the sound pressure level 75–170), respectively, and in the control group 719 (min– of 75 dB via two loudspeakers (Genelec 6010A, Genelec max 517–856) and 143 (min–max 99–171), respectively. Ltd., Iisalmi, Finland). The loudspeakers were in front of To identify the P3a and LN, ERPs for standards were the child at a distance of 1.3 m and in a 40-degree angle subtracted from those for novels. The grand average dif - from the child’s head. ference waves showed the biphasic P3a elicited by novel stimuli. Hence, eP3a and lP3a were separately analyzed. EEG recording The channel selection for the peak detection was done The EEG (.16–1000 Hz, sampling rate 5000 Hz) was after visual inspection, which showed the most promi- recorded with 32 channel electro-cap with Ag–AgCl nent eP3a at the Cz electrode and lP3a and LN at the Fz electrodes placed according to the international 10/20 electrode. The peak detection was done individually for system (ActiCAP 002 and Brain Vision BrainAmp sys- each child within time windows of 180–300 ms for eP3a, tem and software; Brain Products GmbH, Gilching, 300–440 ms for lP3a, and 420–600 ms for LN. The peak Germany). The FCz electrode served as online reference latencies were determined from the most positive (eP3a and impedances were kept below 20 kΩ. Additional elec - and lP3a) or the most negative (LN) peak within those trodes placed above the outer canthus of the right eye windows, and the mean peak amplitudes were calculated and below the outer canthus of the left eye with bipolar from ±20 ms time window around the peak latencies. montage were used for electro-oculogram. The statistical analyses were done for the F3, Fz, F4, Toddlers sat in a chair or in their parent’s lap, watch- C3, Cz, C4, P3, Pz, and P4 electrodes. The existence of ing voiceless cartoons or children’s books, or played with each ERP was determined by comparing its amplitude to silent toys. The parents were instructed to be as quiet as zero with a two-tailed t-test. The amplitude differences possible. The recording was camera monitored from the between the groups were examined with repeated meas- next room and an experienced EEG technician moni- ures analysis of variance (ANOVA) and the Fisher’s least tored the quality of the EEG signal during recording. significant difference (LSD) post hoc test. In ANOVA, During the same recording session, the children partici- between-subject factor was group (RAOM vs. control) pated in an EEG recording with three to four stimulus and within-subject factors were anterior-posterior (AP; sequences with background noise . The total exami - F3-Fz-F4 vs. C3-Cz-C4 vs. P3-Pz-P4) and right-left (RL; nation time for each participant was about two and F3-C3-P3 vs. Fz-Cz-Pz vs. F4-C4-P4) electrode positions. half hours, from which the EEG registration took about The Huynh–Feldt correction was applied when appro - 45 min. There were breaks with refreshments between priate. One-way ANOVA was used for studying latency the stimulus sequences. differences between the groups. For the effect-size esti - mation, the partial eta squared (ƞ ) was calculated. Analysis Brain Vision Analyzer 2.0 (BrainProducts, GmpH) was Results used for offline analysis. Data were down sampled to The eP3a significantly differed from zero in the chil - 250 Hz and re-referenced to the average of the mastoid dren with RAOM and in the controls (two tailed t-test; electrodes. Band pass filtering of .5–45 Hz, 24 dB/oct was p ≤ .001; Table 1, Fig. 1) with no group differences in applied to avoid aliasing and signals not originated from the amplitude, amplitude scalp distribution, or latency. the brain . After visual inspection, channels Fp1, Fp2, In both groups, the eP3a amplitude was stronger at the PO9, PO10, O1, Oz, and O2 were disabled from further frontal and central electrodes than at the parietal elec- analyzis because of artefacts. Ocular correction was done trodes (F [2, 57] = 42.09, p < .001, ƞ = .53; LSD post hoc with an independent component analysis. Extracerebral p < .001). artefacts with voltage exceeding ±150 μV at any elec- There was a significant lP3a in both groups (two tailed trode were removed and data were filtered with band pass t-test; p ≤ .001; Table 1, Fig. 1). A repeated measures of 1–20 Hz, 48 dB/oct. ERPs for standard and novel stim- ANOVA for the lP3a amplitude indicated a significant AP uli were averaged from baseline corrected EEG epochs x group interaction (F [2, 59] = 3.94, p = .03, ƞ = .10). of –100 ms prestimulus to 670 ms after stimulus onset. According to the LSD post hoc test, the children with The first 10 standard stimuli in each recorded sequence RAOM showed a more even AP distribution than the and the standard stimuli right after the novel stimuli were control children who had a clear frontally maximal and excluded from the analysis. Two-tailed t-test indicated no posteriorly diminishing amplitude scalp distribution significant group differences in the mean number of aver - (mean amplitudes frontally 8.99 vs. 9.67 µV, centrally 7.12 aged epochs for standards or novels. The mean number vs. 6.04 µV, and parietally 3.64 vs. 2.17 µV in the RAOM Haapala et al. Behav Brain Funct (2016) 12:1 Page 5 of 8 Table 1 Mean amplitude and latency of ERPs elicited by The amplitude, distribution, or latency of the eP3a did novel stimuli in children in both groups not differ between the groups. This suggests the similar automatic detection of a novel stimulus and the early Electrode Amplitude µV Latency ms stages of the orientation of attention  in the groups. RAOM Control RAOM Control The eP3a was larger frontally and centrally than pari - etally in both groups being in line with earlier studies in eP3a Cz 6.66 (4.30) 6.97 (3.44) 244 (26) 248 (25) typically developed school-aged children [28, 34] and in lP3a Fz 9.30 (3.69) 9.67 (3.74) 348 (36) 341 (22) adults . LN Fz –2.82 (3.38) –2.34 (3.04) 599 (40) 526 (43) In contrast, a significant group difference was found Standard deviations are in parentheses in the lP3a reflecting the actual attention switch . A significant group difference is italized The lP3a amplitude diminished less in the children with RAOM recurrent acute otitis media RAOM than in the controls from frontal to central and parietal areas, which may indicate an immature control of attention switch in children with RAOM. A frontally and control groups, respectively). Furthermore, a signifi - prominent lP3a has been linked to the neural matura- cant AP x RL interaction with no group difference was tion of the frontal cortex and attention control [28, 34]. found (F [4, 140] = 4.98, p < .001, ƞ = .13). LSD post Likewise, an enhanced lP3a at the posterior scalp areas hoc test indicated an even RL amplitude distribution at has earlier been found in easily distractible children with frontal electrodes, but stronger left hemispheric activa- ADHD . The current result supports the behavioural tion compared to the vertex and the right line at central finding on the distractibility of toddlers with OM . electrodes (p < .001) and also stronger left than right line Distractibility can lead to weak utilization of the auditory responses at parietal electrodes (p = .03). There was no channel in learning [29, 50], since it limits the ability to group difference for the lP3a latency. ignore irrelevant auditory stimuli. At 2 years of age, this In both groups, a significant LN was found (two tailed may contribute to the emerging language by disrupting t-test; RAOM: p = .001; control: p = .004; Table 1, Fig. 1). child’s engagement with social-communicative actions A repeated measures ANOVA for the LN amplitude indi- critical for language learning. cated a significant AP × RL interaction (F [4, 148] = 2.96, The LN latency was longer in the children with RAOM p = .02). This was due to the weakest amplitude at F3 than in the controls suggesting delayed reorienting back (LSD post hoc; p = .001–.03) and the strongest ampli- to the ongoing activity [30, 34]. This corresponds with tude at Cz (LSD post hoc; p = .001–.002). There were previous results suggesting delayed reorienting in school- no group differences in the amplitude or amplitude scalp children in a behavioral test  and might indicate that distribution of LN. However, one-way ANOVA indicated children with RAOM have an abnormally low resistance a significant group difference in the LN latency (F [1, to auditory distraction. This is supported by our previous 37] = 32.76, p < .001, ƞ = .47), which peaked later in the results suggesting neural sensitivity to sound loudness children with RAOM than in the controls. changes in these same 2-year-old children with RAOM . The result is also consistent with the elevated audi - Discussion tory sensitivity to sounds described in adolescents with This study examined the effects of early childhood childhood OM . RAOM on neural mechanisms of involuntary attention Our results show that RAOM has long-term effects at the age of 2 years. For that purpose, the P3a and LN leading to abnormal attention control at the age of 2 years elicited by distracting novel sounds were measured in when rapid developmental neural changes are involved. the linguistic multi-feature paradigm at the time when all Studies on attentional neural mechanisms in older chil- the participants had healthy ears and their sound encod- dren with early childhood RAOM would be pertinent ing reflected by obligatory ERPs was found to be intact since they would disclose whether the neural changes in an earlier study . Both the children with RAOM observed are transient or still persisting at the later stages and the controls showed a clearly identifiable P3a with of development. two phases (eP3a and lP3a) and a LN, the morphology of There were two children in the RAOM group who which was found to be consistent with earlier studies in were excluded from the group analysis because of their children [28–31, 45, 46]. However, the topography and abnormally enhanced P3a responses. The exclusion was timing of these responses were distinct in the two groups. done to avoid the bias of these statistically confirmed These findings suggest different maturational trajectories outliers on the results of the RAOM group. However, we in the two groups of children and suggest that the conse- should notice that these extreme P3a responses might quences of OM are not limited to the middle ear effusion reflect a genuine effect of RAOM and indicate enhanced period but the effects are long-lasting. Haapala et al. Behav Brain Funct (2016) 12:1 Page 6 of 8 Fig. 1 ERPs (eP3a, lP3a, and LN) elicited by novel stimuli in children with recurrent acute otitis media (RAOM) and their controls; a grand average standard and novel ERP waves, b grand average difference (novel minus standard ERP) waves, and c scalp topographies distractibility of these children, but this should be studied However, there were six children in the RAOM group further in the future. and four children in the control group who could not When interpreting the results, it should be taken into tolerate the TEOAE measurement at the time of EEG. account that the accurate hearing thresholds were not Because these children had passed the TEOAE screen- available at the time of the measurement. Accurate hear- ing at the postnatal period, we decided to include them in ing thresholds can be reliably measured from the age of the study. However, there is a possibility that a child who three onwards . Because the participants in the cur- has passed the TEOAE screening at birth may develop rent study were 22–26 months old we decided to use hearing deficit later. Hearing levels were assumed to be TEOAE screening to exclude congenital hearing losses. at normal levels in all participants while the children Haapala et al. Behav Brain Funct (2016) 12:1 Page 7 of 8 Academy of Finland, grant number 276414 ( TeK). We are grateful for EEG with RAOM had had tympanostomy tubes inserted and, technician Raija Remes (Clinical Neurophysiology, Oulu University Hospital) according the parental reports, there were no concerns for her invaluable help in data collection, and all the families participating in of hearing in the screenings at the family and health care the study. clinics where Finnish children are followed up regularly. Competing interests Furthermore, these same children showed age-typical The authors declare that they have no competing interests. cortical sound encoding with no group differences in our Received: 30 September 2015 Accepted: 24 December 2015 earlier study . This refers to hearing levels within the normal range at the time of the EEG. Conclusions To conclude, this study showed abnormal neural mecha- References 1. Sipilä M, Pukander J, Karma P. Incidence of acute otitis media up to the nisms of involuntary attention in 2-year-old children with age of 1 ½ years in urban infants. Acta Otolaryngol. 1987;104:138–45. RAOM. For the distracting novel sounds, the RAOM 2. Teele DW, Klein JO, Rosner B. Epidemiology of otitis media during the group showed atypical neural organization signified by first seven years of life in children in greater Boston: a prospective, cohort study. J Infect Dis. 1989;160:83–94. a more even lP3a scalp distribution in anterior-posterior 3. 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Behavioral and Brain Functions – Springer Journals
Published: Dec 1, 2015
Keywords: neurosciences; neurology; behavioral therapy; psychiatry
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