International Journal of Psychophysiology 95 (2015) 94–100
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Asymmetry of temporal auditory T-complex: Right ear–left hemisphere advantage in Tb timing in children Nicole Bruneau a,b,⁎, Aurélie Bidet-Caulet d, Sylvie Roux a,b, Frédérique Bonnet-Brilhault a,b,c, Marie Gomot a,b a
UMR U930, INSERM, Tours, France Université François-Rabelais de Tours, France CHRU de Tours, France d INSERM, U1028, CNRS, UMR5292, Lyon Neuroscience Research Center, Brain Dynamics and Cognition Team, Lyon F-69500, France b c
a r t i c l e
i n f o
Article history: Received 10 January 2014 Received in revised form 18 July 2014 Accepted 27 July 2014 Available online 2 August 2014 Keywords: Event-related potentials (ERPs) Auditory T-complex Tones Children Interhemispheric asymmetry Stimulation rate Right ear–left hemisphere advantage
a b s t r a c t Objective: To investigate brain asymmetry of the temporal auditory evoked potentials (T-complex) in response to monaural stimulation in children compared to adults. Methods: Ten children (7 to 9 years) and ten young adults participated in the study. All were right-handed. The auditory stimuli used were tones (1100 Hz, 70 dB SPL, 50 ms duration) delivered monaurally (right, left ear) at four different levels of stimulus onset asynchrony (700–1100–1500–3000 ms). Latency and amplitude of responses were measured at left and right temporal sites according to the ear stimulated. Results: Peaks of the three successive deflections (Na–Ta–Tb) of the T-complex were greater in amplitude and better defined in children than in adults. Amplitude measurements in children indicated that Na culminates on the left hemisphere whatever the ear stimulated whereas Ta and Tb culminate on the right hemisphere but for left ear stimuli only. Peak latency displayed different patterns of asymmetry. Na and Ta displayed shorter latencies for contralateral stimulation. The original finding was that Tb peak latency was the shortest at the left temporal site for right ear stimulation in children. Amplitude increased and/or peak latency decreased with increasing SOA, however no interaction effect was found with recording site or with ear stimulated. Conclusion: Our main original result indicates a right ear–left hemisphere timing advantage for Tb peak in children. The Tb peak would therefore be a good candidate as an electrophysiological marker of ear advantage effects during dichotic stimulation and of functional inter-hemisphere interactions and connectivity in children. © 2014 Published by Elsevier B.V.
1. Introduction Cortical auditory evoked potentials (AEPs) provide a very suitable electrophysiological tool to study temporal aspects of auditory processing asymmetry. Because the ascending auditory pathway is complex and information is transferred from each ear to both ipsilateral and contralateral auditory cortices, asymmetry of auditory cortical responses have to be considered according to the recording hemisphere and to the ear being stimulated. Such studies have been performed in adults and mainly focused on asymmetry of the prominent fronto-central N100 peak (see Naatanen and Picton, 1987; Hine and Debener, 2007 for reviews), a peak which emerges at around 8–10 years. AEPs in children provide a valuable source of information about the maturation of cortical areas involved in auditory processing. In contrast to fronto-central responses the morphology of which drastically evolves
⁎ Corresponding author at: UMR U930, INSERM, Child Psychiatry Centre, CHU Bretonneau, 2 Boulevard Tonnellé, 37044 Tours Cedex 9, France. Tel.: +33 2 47 47 85 19; fax: +33 2 47 47 38 46. E-mail address: [email protected] (N. Bruneau).
http://dx.doi.org/10.1016/j.ijpsycho.2014.07.012 0167-8760/© 2014 Published by Elsevier B.V.
with age during childhood, AEPs recorded at temporal sites display similar waveforms in children and adults (Bruneau et al., 1997; Bruneau and Gomot, 1998; Ponton et al., 2002). These similarities make it possible to study age-related differences in auditory processing asymmetry occurring in the cortical regions involved in the generation of these temporal deflections. The temporal auditory response, also named the T-complex, consists of a sequence of three successive deflections recorded maximally at lateral temporal sites, i.e., first a negative peak Na followed by the two successive positive–negative deflections named Ta–Tb, respectively. The “Ta–Tb” terminology was originally used by Wolpaw and Penry (1975) in their initial description of the Tcomplex. Note that another denomination has also been used, with N1a and N1c corresponding to Na and Tb, respectively (McCallum and Curry, 1980a,b; Picton et al., 1999). These temporal AEPs display greater amplitude and are much more well-defined in children than in adults, thus making them reliable responses with which to study auditory processing in children. Several studies have suggested that these temporal deflections, particularly the Tb peak, are markers of language disorders in children because smaller peak amplitudes and delayed peak latencies have been found in children with such disorders (Tonnquist-Uhlen, 1996; Bruneau et al., 2003; Groen et al., 2008; Shafer et al., 2011).
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Some of these studies also reported abnormal patterns of T-complex asymmetry. However, as well as those describing the T-complex in normal children, only partial information on auditory processing asymmetry was provided in these studies since stimuli were delivered either binaurally (Bruneau et al., 2003; Shafer et al., 2011) or monaurally to the left ear (Ponton et al., 2002; Tonnquist-Uhlen et al., 2003) or the right ear (Groen et al., 2008). Moreover, the rate of stimulation has been extensively demonstrated to affect the fronto-central N100 in both adults and children aged 8–11 years (e.g. Alcaini et al., 1994; Coch et al., 2005; Shelley et al., 1999; Sussman et al., 2008). Only one study has reported the influence of rate of stimulation on the Tb peak in children (Ceponiene et al., 1998). It indicated that the amplitude of the temporal negative peak corresponding to Tb increased with increasing inter-stimulus interval (350, 700, 1400, 2000 ms) thus indicating long refractoriness period for the underlying generator. Moreover in our initial work (Bruneau et al., 1997) comparing temporal responses of children and adults, long interstimulus intervals (between 3 and 5 s.) were used. It therefore appears that low rates of stimulation are favorable conditions for an accurate identification of the successive peaks of T-complex and of their asymmetry. The present study was performed in normally developing children and adults. The aim was to investigate asymmetry of the temporal Tcomplex peaks elicited by tonal stimuli delivered monaurally to each ear at different rates of stimulation corresponding to four stimulus asynchrony (SOA) conditions (from 700 to 3000 ms). 2. Methods 2.1. Subjects Twenty right-handed subjects participated in the study: 10 children (5 male) aged from 6 years 10 months to 8 years 9 months (mean ± SD: 7 years 11 months ± 8 months) and 10 adults (6 males) aged from 21 to 29 years (22 years 9 months ± 2 years 5 months). Participants were recruited from the immediate medical/research community and from local schools. All procedures were approved by the Ethics Committee (CCP) of the University Hospital of Tours. Adult participants and parents gave informed consent, and children gave assent after the experimental protocol had been explained to them. Participants (a parent for children) were interviewed to exclude previous and current diagnoses of learning, speech/language, hearing, emotional/behavioral, and neurological disorders. All the children were in age-appropriate grade at school. All participants were checked audiometrically for normal hearing in both ears before AEP recordings. 2.2. Stimuli and procedure The auditory stimuli used were 1100 Hz tone bursts of 50 ms duration (5 ms rise/fall times), calibrated to 70 dB SPL. They were delivered monaurally to the left ear (LE) and right ear (RE) through a TDH 39 headphone. Tones were presented with SOAs (onset-to-onset) of 700, 1100, 1500, and 3000 ms in separate conditions. A recording session consisted of 8 runs (4 SOA for RE and LE stimuli), each composed of 155 stimuli, separated by short breaks (1–3 min). 2.3. Procedure During the recording session, each subject was seated comfortably in a sound-treated room and watched a self-chosen silent movie during electroencephalography (EEG) recording. The order of presentation of the different runs was counterbalanced across participants. The total recording session was 45 min.
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2.4. EEG recordings The EEG was recorded from 28 Ag/AgCl scalp electrodes referenced to the tip of the nose. The ground electrode was placed on the forehead. Seventeen of the electrodes (including T3 and T4) were placed according to the international 10–20 system (Jasper, 1958). Additional electrodes were placed at intermediate positions and over the left and right mastoid sites. The ground electrode was on the forehead. The impedance value of each electrode was less than 10 kΩ. Horizontal and vertical electro-oculograms (EOG) were recorded differentially from 2 electrodes placed above and below the right ear for vertical EOG and at the outer canthus of each eye for horizontal EOG. The EEG and EOG were amplified with a bandpass filter (0.5–70 Hz; slope 6 dB/octave) and digitized at a sampling rate of 256 Hz. Epochs with movements or eye blinks exceeding ± 100 μV were discarded. Automatic correction of the deviations due to ocular activity was then applied (Anderer et al., 1989). EEG epochs were averaged separately for each SOA and each ear stimulated over a 500-ms analysis period, including a 100-ms prestimulus baseline, and were filtered digitally (0–30 Hz). 2.5. Data analysis AEP measurements were performed using ELAN software (Aguera et al., 2011). The study focused on AEPS recorded at the left and right temporal sites (T3 and T4, respectively). Temporal waveforms displayed the successive negative–positive–negative peaks Na, Ta, and Tb. Amplitudes and latencies of each peak were analyzed using repeatedmeasures analysis of variance (ANOVA) (Statistica — Version 10) with Group (children, adults) as the between-subject factor and hemisphere (Hem, T3 vs T4), ear stimulated (RE vs LE) and stimulus rate (4 SOA conditions) as the within-subject factors. When more than two levels (or one degree of freedom) were considered, the Greenhouse–Geisser epsilon correction was applied. F ratios with uncorrected degrees of freedom and corrected p values are reported. Post-hoc comparisons were made using Newman–Keuls tests. 3. Results Grand average AEP waveforms recorded in children and adults in the four SOA conditions at the right and left temporal sites are shown in Fig. 1. Temporal responses displayed similar waveforms in both groups, with the successive Na–Ta–Tb peaks. However, the Tb peak was the only peak which was well individualized and measurable in all children and adult subjects and allowed comparisons according to age. For both amplitude and latency of each deflection of the T-complex in children and of the Tb deflection in adults, no significant interaction was found between SOA and ear stimulated or hemisphere recorded, or between SOA and Hemisphere × Ear interaction. The effects of SOA on peak latency and amplitude are therefore presented separately from the effects of the other factors. The AEPs obtained in the four SOA conditions were pooled in order to provide better visualization of the effects of hemisphere and stimulated ear on peak latency and amplitude (Figs. 2 and 3). Results of the ANOVA analyses performed on latency and amplitude of each deflection are detailed in Table 1. 3.1. Peak latency asymmetry (Fig. 3, top; Table 1) 3.1.1. Na and Ta peak latencies in children Patterns of asymmetry were considered for the successive Na and Ta peaks only in children, with measurements obtained in all conditions for 8 out of 10 children for the Na peak and all children for the Ta peak. There were significant Hem × Ear interactions for Na and Ta peak latencies, without a significant main effect of ear stimulated or hemisphere recorded. Stimulation of either ear resulted in inter-hemispheric
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Fig. 1. Mean T-complex waveforms – consisting of successive Na, Ta and Tb peaks – recorded at the left (T3) and right (T4) temporal sites in children and adults in response to tones elicited at different rates of stimulation (four SOA conditions: 700, 1100, 1500 or 3000 ms).
asymmetry, with substantially earlier responses at the contralateral temporal site for both peaks. Considering each temporal site, both Na and Ta peaks occurred earlier for the contralateral than for the ipsilateral ear stimulation. These findings correspond to the classic asymmetry pattern of contralateral advantage for Na and Ta peak latencies.
left temporal site was 10 ms shorter for contralateral than for ipsilateral stimulation (p = .0007) and 10 ms shorter than the latency of Tb peak recorded at the right temporal site for both ipsi (p = .0005) and contralateral (p = .001) stimulation. The auditory processing underlying the Tb peak was therefore fastest in the right ear–left hemisphere condition.
3.1.2. Tb peak latency — children versus adults There was a significant main effect of group [F(1,18) = 35; p b .00002] due to significantly longer Tb peak latency in children (around 160 ms) than in adults (around 135 ms) and a significant Group × Hem × Ear interaction [F(1,18) = 7.2; p b .02]. ANOVA was then performed in each group separately and showed that Hem × Ear interaction was significant in children only, with a significant main effect of ear stimulated (Table 1). The asymmetry pattern was different for the Tb peak than for the preceding Na and Ta peaks in children, as indicated by the results of the Newman–Keuls post-hoc tests. Right ear stimulation resulted in substantially earlier Tb peak in the contralateral hemisphere, which was not the case for left ear stimulation. The Tb peak latency at the
3.2. Peak amplitude asymmetry (Fig. 3, bottom; Table 1) 3.2.1. Na peak amplitude asymmetry in children There was a significant main effect of hemisphere due to greater Na amplitude at the left than the right temporal site (mean ± s.e.m. = −3.1 ± 0.2 μV at T3; −1.9 ± 0.4 μV at T4) irrespective of the ear stimulated. 3.2.2. Ta peak amplitude asymmetry in children The Ta peak amplitude displayed a significant Hem × Ear interaction, without a significant main effect of ear stimulated or hemisphere recorded. A significant inter-hemispheric asymmetry was found for left ear stimulation only, with greater Ta peak amplitude at the right than
Fig. 2. Grand average T-complex waveforms recorded at the left (T3) and right (T4) temporal sites in children and adults according to ear stimulated (RE: right ear; LE: left ear). Responses were pooled for the four SOA conditions.
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Fig. 3. Mean (±standard error) peak latencies and amplitudes (absolute value) at the left (T3) and right (T4) temporal sites for the three successive peaks of the T-complex in children (negative Na, positive Ta and negative Tb peaks) and for the Tb peak in adults elicited by left ear (LE) or right ear (RE) stimulation. Stars indicated significant results at Newman–Keuls tests.
at the left temporal site. Only Ta peak at the right temporal site displayed a significant contralateral effect with greater amplitude for contralateral ear than for ipsilateral ear stimulation. 3.2.3. Tb peak amplitude — children versus adults The ANOVA indicated a significant main effect of group (F(1,18) = 16.4; p b .001) due to significantly greater Tb peak amplitude in children (around 5 μV) than in adults (around 3 μV) and a significant Group × Hem × Ear interaction [F(1,18) = 4.4; p b .05]. ANOVA
Table 1 Results of ANOVA performed on each peak of the T-complex using hemisphere (Hem: measures at T3 and T4), ear stimulated (left/right) and SOA (4 conditions) as within subject factors. Tb peak was the only peak measurable in all conditions in both groups. The interactions other than those indicated were non-significant. Results of post hoc comparisons are shown in Fig. 3. Children
Adults
Na
Ta
Tb
Tb
ns
ns
ns
ns F(1,7) = 22; p b .01 F(3,21) = 40; p b .0001 ε = 0.62
ns F(1,9) = 40; p b .001 F(3,27) = 5; p b .01 ε = 0.83
F(1,9) = 12; p b .01 ns F(1,9) = 24; p b .001 ns
ns
ns ns
ns ns
ns ns
Ear × Hem
ns F (1,7) = 6; p b .05 ns
SOA
ns
F(1,9) = 6; p b .05 F(3,27) = 5; p b .01 ε = 0.46
F(1,9) = 11; p b .01 F(3,27) = 6; p b .01 ε = 0.53
F(1,9) = 20; p b .011 ns
Latency Ear Hem Ear × Hem SOA
Amplitude Ear Hem
ns ns
performed in each group separately indicated a significant Hem × Ear interaction in both groups which was thereafter considered separately. In both children and adults, a significant inter-hemispheric asymmetry was found for left ear stimulation only, with greater Tb peak amplitude at the right than at the left temporal site. In children, as found for Ta, Tb peak at the right temporal site displayed a significant contralateral effect with greater amplitude for contralateral ear than for ipsilateral ear stimulation whereas in adults the contralateral effect was found significant at the left temporal site.
3.3. SOA effect (Fig. 1; Table 1) 3.3.1. Latency A significant main effect of SOA was found for Na and Ta peak latencies in children due to peak latency decrease with increasing SOA (mean ± SD: Na: 83 ± 1 ms, 79 ± 1 ms, 77 ± 1 ms, 76 ± 1 ms; Ta: 116 ± 2 ms, 114 ± 2 ms, 112 ± 2 ms, 110 ± 3 ms for SOA: 700, 1100, 1500, and 3000 ms, respectively). In contrast, there was no significant main effect of SOA on Tb peak latency in children or adults.
3.3.2. Amplitude Na peak amplitude in children did not display any significant main effect of SOA. In contrast, Ta peak amplitude displayed a significant main effect of SOA due to an increase in Ta peak amplitude with increasing SOA (from 2.3 ± 0.9 μV to 5.2 ± 1.7 μV for SOA 700 and 3000 ms, respectively). Tb peak amplitude of children and adults showed a main effect of SOA [F(3,54) = 7.9; ε = 0.55; p b .003] and a significant SOA × Group interaction [F(3,54) = 3.9; ε = 0,55; p b .04]. ANOVA performed in each group separately (Table 1) showed that the SOA effect was significant in children only. This was due to an increase in Tb peak amplitude with increasing SOA (from 4.2 ± 0.9 μV to 7.4 ± 1.2 μV for SOA = 700 ms and 3000 ms, respectively).
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4. Discussion We studied the asymmetry of the temporal-recorded auditory evoked potentials, named the T-complex, in 7- to 9-year-old children and in adults. The overall waveforms with the successive Na–Ta–Tb peaks were similar in both groups but were greater in amplitude and better defined in children than in adults. Amplitude and latency were measurable for the three peaks in children but only for Tb peak in adults. Amplitude measurements in children showed that the Na culminates in the left hemisphere, and the Ta and the Tb in the right hemisphere but for left ear stimulation only. In adults, the Tb peak amplitude was greater in the hemisphere contralateral to the stimulated ear. Patterns of asymmetry were different for the latency of the different peaks. Whereas the Na and Ta peaks of children displayed a classic contralateral latency effect (shorter latency on temporal site contralateral to the stimulated ear), the Tb peak displayed a right ear–left hemisphere timing advantage. This last result has important implications in view of previous data suggesting that neurophysiological mechanisms underlying Tb peak may be involved in language processes. 4.1. Effects of SOA on T-complex The SOA was found to influence the latency and amplitude of the Tcomplex peaks, irrespective of the ear stimulated and the temporal site being recorded. Na and Ta peak latencies decreased with increasing SOA in children, whereas Tb peak latency remained unchanged in both children and adults. Moreover, Ta and Tb peak amplitudes increased with increasing SOA in children, whereas the amplitudes of the Na in children and the Tb in adults were not affected, probably because the responses were too small and too variable in amplitude. Our results regarding the effects of SOA on the Tb peak in children are in accordance with those previously reported by Ceponiene et al. (1998) indicating increased amplitude and no modification of latency when SOA increased in the same range as that used in our study. Increase in amplitude with increasing SOA has been extensively reported for the fronto-central N1 response in adults and older children (e.g. Alcaini et al., 1994; Budd et al., 1998; Ceponiene et al., 2002; Coch et al., 2005; Roder et al., 1999; Shelley et al., 1999; Sussman et al., 2008), while discrepant results have been reported for modification of latency. Only two of these studies reported decreased latency with increasing SOA (Roder et al., 1999; Shelley et al., 1999). All of these authors interpreted the increase in amplitude with lengthening SOA as resulting from the refractory period of the neural assemblies involved in generation of the response. This explanation fits well with a decrease in peak latency with increasing SOA, as we found for Na and Ta peaks. However, increased amplitude might be associated with no effect on latency, as we found for Tb and as reported by Ceponiene et al. (2002), Coch et al. (2005) and Sussman et al. (2008) for the frontocentral N1 peak. The present findings therefore indicated a long refractory period for the generators underlying the different peaks of the T-complex since the effects of SOA were still present for the longest SOA used in our study (i.e., 3 s). 4.2. Maturation of the T-complex Temporal-recorded auditory responses were of greater amplitude and successive peaks are better defined in children than in adults, in agreement with previous findings on the T-complex (Bruneau et al., 1997; Tonnquist-Uhlen et al., 2003). In particular, the Tb peak recorded in all participants displayed longer latency and greater amplitude in children than in adults. These age-related latency differences might be related to maturation processes occurring throughout childhood in both auditory pathways and auditory cortical areas, such as maturation of the superficial cortical
layers (III and II) and their intracortical connections (Moore and Linthicum, 2007), as well as marked changes in axonal myelination and synaptic efficiency (Eggermont, 1992; Moore and Guan, 2001). The age-related amplitude differences might also be dependent on the evolution of location and/or orientation of neural generators contributing to scalp-recorded potentials which may be linked to changes in the relative geometry of the brain and skull during development (Dekaban, 1970). Moreover, the signal-to-noise ratio might be better in children than in adults partly due to the thinner temporal bone, resulting in greater responses from the temporal associative cortex in children. 4.3. Asymmetry of T-complex amplitudes Amplitude measurements indicated left hemisphere dominance of the Na peak. Predominance of Na(N1a) in the left hemisphere irrespective of the ear stimulated was reported in earlier studies in adults (Knight et al., 1988; Woods, 1995), whereas no findings have been reported in children. The subsequent Ta and Tb peaks of children displayed rightward lateralization but for left ear stimulation only. Responses were fairly symmetrical for right ear stimulation. Using left ear stimulation only, Tonnquist-Uhlen et al. (2003) found the same pattern of amplitude asymmetry for these two peaks. Our results on asymmetry of Tb peak amplitude are in accordance with results from a previous research examining asymmetry of AEP to monaural tones with source analysis of the radial activity recorded in the 140 ms latency range, corresponding to the Tb peak in adults (Picton et al., 1999; Hine and Debener, 2007). Several explanations can be proposed to justify such results. The temporal cortical regions involved in the generation of these deflections display anatomical asymmetry. The leftward asymmetry of the planum temporale surface and rightward asymmetry of the superior temporal sulcus (STS) and of the sulcal depth previously reported in adults (Geschwind and Levitsky, 1968; Ochiai et al., 2004; Van Essen, 2005), already present in infants (Dubois et al., 2010; Glasel et al., 2011; Hill et al., 2010), were recently reported in 8- to 9-year-old children (Bonte et al., 2013). These authors also described asymmetry in the slope of the Sylvian Fissure, with a steeper slope in the right than in the left hemisphere. Such anatomical asymmetry could conceivably produce hemispheric differences in the orientation and/or location of the generators underlying the different peaks, predominant in the left hemisphere for Na, and in the right hemisphere for Ta and Tb. Interhemispheric differences in the cortical folding of the auditory cortex have also to be considered. In a recent MEG study (Shaw et al., 2013), it was demonstrated that rightward lateralization of MEG auditory responses might be due to a greater degree of cortical folding in the left auditory cortex. Sources in an extended area of activation might then generate magnetic fields with varying polarity that superpose or cancel each other, depending on the local geometry of the cortex. A similar explanation might also be proposed for rightward lateralization of auditory evoked potentials, such as Ta and Tb peaks and for their sensitivity to ear stimulated, recorded on the right and not on the left temporal site. Moreover our results indicate dissociated patterns of asymmetry for peak amplitude and latency; this fits well with this explanation since folding can be hypothesized to influence amplitude but not latency. Interestingly, in children, only responses on the right temporal site seemed to be sensitive to the ear stimulated. This result is consistent with specialization of the lateral right auditory cortex for spatial sound processing as previously demonstrated by Zatorre and Penhune (2001). Indeed sound localization mostly relies on the differences in acoustic input reaching the cortex, and therefore on the differential processing of input from the left and right ears. This sensitivity of the right hemisphere to the stimulated ear indicates that T-complex amplitude recorded at the right temporal site also reflects asymmetry of ear-to-hemisphere connectivity. Indeed, each ear sends a larger number of fibers to the contralateral cortex than to the ipsilateral cortex
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(Rosenzweig, 1951). This asymmetrical connectivity was not observed in the T-complex recorded at the left temporal site since its amplitude was not dependent on the ear stimulated. We might therefore hypothesize that this left T-complex is more dependent on cortical processing occurring at the left temporal site than on auditory input associated with asymmetry of ear-to-hemisphere connectivity. 4.4. Asymmetry of T-complex latencies In children, Na and Ta peak latencies displayed a typical contralateral effect at both temporal sites (shorter latency on contra than on ipsilateral temporal site). Although nothing has been reported on asymmetry of Na peak latency, a similar contralateral Ta peak latency effect has been reported in children by Tonnquist-Uhlen et al. (2003) for left ear stimulation only. In addition to the greater number of fibers, contralateral afferents cross the midline at the brainstem with a more direct pathway, and fewer synapses to the cortex (Adams, 1979; Brunso-Bechtold et al., 1981; Coleman and Clerici, 1987). This could explain the shorter latency of contra- compared to ipsilateral responses. This does not explain the results obtained for Tb peak latency which displayed a right ear–left hemisphere (RE–LH) timing advantage: the Tb peak occurred earlier at the left temporal site for contra- than for ipsilateral stimulation and earlier than the Tb peak recorded at the right temporal site regardless of ear stimulated. Early intracranial recordings and lesion studies have suggested that Tb reflects activity from the lateral surfaces of the superior temporal gyrus (Celesia, 1968; Celesia and Puletti, 1969). Studies using dipole modeling in adults have attributed the Tb response to bilateral radial dipoles located in the secondary auditory cortex in the lateral aspects of the temporal lobes (Scherg and Von Cramon, 1985, 1986; Albrecht et al., 2000; Ponton et al., 2002). The faster RE–LH processing might be related to the properties of the left auditory cortex allowing faster auditory processing and greater sensitivity to rapid acoustic changes as is required for speech processing. Possible microstructural asymmetry of auditory cortical areas has been proposed to explain such lateralized processing (Zatorre and Belin, 2001; Zatorre and Gandour, 2008). Faster temporal processing in the left hemisphere is suggested to be related to the greater volume of white matter tissue in the left than in the right hemisphere, due to greater myelin sheath thickness in the left hemisphere as shown by post mortem analysis of the posterior temporal lobe (Anderson et al., 1999). Moreover, several studies have indicated that the auditory processing reflected in the Tb peak may be critical for language. Delayed, deviant or absent Tb peaks have been reported in clinical populations with language impairments such as children with SLI (Tonnquist-Uhlen, 1996; Shafer et al., 2011), children with autism (Bruneau et al., 1999, 2003), and children with Down syndrome (Groen et al., 2008). The shorter RE–LH Tb latency might thus be due to faster neuronal communication between auditory areas involved in Tb generation and in language processing in the left hemisphere. The present study shows for the first time that both the Na and the Ta peak occur earlier at the temporal site contralateral to the stimulated ear in children whereas the Tb peak latency presented a particular pattern, with the shortest latency in the left hemisphere after right ear stimulation suggesting faster neuronal communication within the left auditory cortex. 4.5. Asymmetry in Tb peak latency and right ear advantage The present results on Tb peak latency could reflect fundamental auditory processes, such as those related to superiority of the dominant hemisphere in dichotic listening (Hellige, 1993; Davisdson and Hugdahi, 1998 for reviews). Dichotic listening is a standard task which is mainly used to study auditory lateralization. Using verbal material in right-handed subjects, stimuli presented to the right ear are more efficiently processed than those presented to the left ear. This right ear advantage (REA) has been widely attributed to the left hemisphere
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supremacy in language perception and the contralateral pathway dominance in auditory signal transmission. Whereas the input of the right ear is immediately transferred to the left-hemisphere language receptive areas, the input of the left ear entering the right hemisphere requires callosal transfer to the left hemisphere in order to be processed, and thus needs extra transfer time. According to this structural model, termed “callosal relay” model (Zaidel, 1983), the magnitude of the ear advantage would be directly related to the functional properties of the corpus callosum (Westerhausen and Hugdahl, 2008). Only one study was performed in adults in order to relate asymmetry of auditory evoked potentials and REA in dichotic listening (Eichele et al., 2005). It focused on the N100 peak asymmetry measured at left and right temporal sites in response to two different syllables presented dichotically. A relationship was found between the individual differences in asymmetry of the N100 peak and the ear advantage evaluated with dichotic listening. Since the significant measurements were those from temporal sites, the authors suggested a possible influence of the T-complex in the effect observed. Our findings suggest that in children interhemispheric differences in Tb peak latency at temporal sites could reflect the right ear advantage. Moreover, our results provide an approximation of the duration of callosal transfer in children since right-ear input seemed to reach the left auditory cortex 10 ms earlier than auditory information from the left ear. Therefore, the present results not only provide extensive information on the asymmetry of latency and amplitude of the different peaks of the T-complex in children, but also, more importantly, indicate that the Tb peak in children would be a good candidate marker of ear preference in dichotic listening in children. Besides being a marker of lateralized temporal lobe language function, the Tb peak would be a marker of functional inter-hemispheric interaction and connectivity in children. 5. Disclosure statement All authors declare they have no financial interest, and no current or potential conflicts of interest. Acknowledgments We thank all of the participants for their cooperation, Rémy Magné for preparation of the figures and Doreen Raine for correction of the English language. References Adams, J.C., 1979. Ascending projections to the inferior colliculus. J. Comp. Neurol. 183, 519–538. Aguera, P.E., Jerbi, K., Caclin, A., Bertrand, O., 2011. ELAN: a software package for analysis and visualization of MEG, EEG, and LFP signals. Comput. Intell. Neurosci. 2011, 158970. Albrecht, R., Suchodoletz, W., Uwer, R., 2000. The development of auditory evoked dipole source activity from childhood to adulthood. Clin. Neurophysiol. 111, 2268–2276. Alcaini, M.,Giard, M.H.,Thevenet, M.,Pernier, J., 1994. Two separate frontal components in the N1 wave of the human auditory evoked response. Psychophysiology 31, 611–615. Anderer, P., Semlitsch, B., Saletu, B., 1989. Ein Korrekturverfahren zur Reduktion okulärer Artefakte in der EEG- und ERP- Topographie. In: Saletu, B. (Ed.), Fortschritte in der Biologischen Psychiatrie. Thieme, Stuttgart, New York. Anderson, B.,Southern, B.D.,Powers, R.E., 1999. Anatomic asymmetries of the posterior superior temporal lobes: a postmortem study. Neuropsychiatry Neuropsychol. Behav. Neurol. 12, 247–254. Bonte, M., Frost, M.A.,Rutten, S., Ley, A.,Formisano, E., Goebel, R., 2013. Development from childhood to adulthood increases morphological and functional inter-individual variability in the right superior temporal cortex. Neuroimage 83, 739–750. Bruneau, N.,Gomot, M., 1998. Auditory evoked potentials (N1 wave) as indices of cortical development throughout childhood. In: Garreau, B. (Ed.), Neuroimaging in Child Neuropsychiatric Disorders. springer, pp. 113–124. Bruneau, N., Roux, S., Guerin, P., Barthelemy, C., Lelord, G., 1997. Temporal prominence of auditory evoked potentials (N1 wave) in 4–8-year-old children. Psychophysiology 34, 32–38. Bruneau, N.,Roux, S.,Adrien, J.L.,Barthelemy, C., 1999. Auditory associative cortex dysfunction in children with autism: evidence from late auditory evoked potentials (N1 wave-T complex). Clin. Neurophysiol. 110, 1927–1934.
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Asymmetry of temporal auditory T-complex: Right ear–left hemisphere advantage in Tb timing in children Nicole Bruneau a,b,⁎, Aurélie Bidet-Caulet d, Sylvie Roux a,b, Frédérique Bonnet-Brilhault a,b,c, Marie Gomot a,b a
UMR U930, INSERM, Tours, France Université François-Rabelais de Tours, France CHRU de Tours, France d INSERM, U1028, CNRS, UMR5292, Lyon Neuroscience Research Center, Brain Dynamics and Cognition Team, Lyon F-69500, France b c
a r t i c l e
i n f o
Article history: Received 10 January 2014 Received in revised form 18 July 2014 Accepted 27 July 2014 Available online 2 August 2014 Keywords: Event-related potentials (ERPs) Auditory T-complex Tones Children Interhemispheric asymmetry Stimulation rate Right ear–left hemisphere advantage
a b s t r a c t Objective: To investigate brain asymmetry of the temporal auditory evoked potentials (T-complex) in response to monaural stimulation in children compared to adults. Methods: Ten children (7 to 9 years) and ten young adults participated in the study. All were right-handed. The auditory stimuli used were tones (1100 Hz, 70 dB SPL, 50 ms duration) delivered monaurally (right, left ear) at four different levels of stimulus onset asynchrony (700–1100–1500–3000 ms). Latency and amplitude of responses were measured at left and right temporal sites according to the ear stimulated. Results: Peaks of the three successive deflections (Na–Ta–Tb) of the T-complex were greater in amplitude and better defined in children than in adults. Amplitude measurements in children indicated that Na culminates on the left hemisphere whatever the ear stimulated whereas Ta and Tb culminate on the right hemisphere but for left ear stimuli only. Peak latency displayed different patterns of asymmetry. Na and Ta displayed shorter latencies for contralateral stimulation. The original finding was that Tb peak latency was the shortest at the left temporal site for right ear stimulation in children. Amplitude increased and/or peak latency decreased with increasing SOA, however no interaction effect was found with recording site or with ear stimulated. Conclusion: Our main original result indicates a right ear–left hemisphere timing advantage for Tb peak in children. The Tb peak would therefore be a good candidate as an electrophysiological marker of ear advantage effects during dichotic stimulation and of functional inter-hemisphere interactions and connectivity in children. © 2014 Published by Elsevier B.V.
1. Introduction Cortical auditory evoked potentials (AEPs) provide a very suitable electrophysiological tool to study temporal aspects of auditory processing asymmetry. Because the ascending auditory pathway is complex and information is transferred from each ear to both ipsilateral and contralateral auditory cortices, asymmetry of auditory cortical responses have to be considered according to the recording hemisphere and to the ear being stimulated. Such studies have been performed in adults and mainly focused on asymmetry of the prominent fronto-central N100 peak (see Naatanen and Picton, 1987; Hine and Debener, 2007 for reviews), a peak which emerges at around 8–10 years. AEPs in children provide a valuable source of information about the maturation of cortical areas involved in auditory processing. In contrast to fronto-central responses the morphology of which drastically evolves
⁎ Corresponding author at: UMR U930, INSERM, Child Psychiatry Centre, CHU Bretonneau, 2 Boulevard Tonnellé, 37044 Tours Cedex 9, France. Tel.: +33 2 47 47 85 19; fax: +33 2 47 47 38 46. E-mail address: [email protected] (N. Bruneau).
http://dx.doi.org/10.1016/j.ijpsycho.2014.07.012 0167-8760/© 2014 Published by Elsevier B.V.
with age during childhood, AEPs recorded at temporal sites display similar waveforms in children and adults (Bruneau et al., 1997; Bruneau and Gomot, 1998; Ponton et al., 2002). These similarities make it possible to study age-related differences in auditory processing asymmetry occurring in the cortical regions involved in the generation of these temporal deflections. The temporal auditory response, also named the T-complex, consists of a sequence of three successive deflections recorded maximally at lateral temporal sites, i.e., first a negative peak Na followed by the two successive positive–negative deflections named Ta–Tb, respectively. The “Ta–Tb” terminology was originally used by Wolpaw and Penry (1975) in their initial description of the Tcomplex. Note that another denomination has also been used, with N1a and N1c corresponding to Na and Tb, respectively (McCallum and Curry, 1980a,b; Picton et al., 1999). These temporal AEPs display greater amplitude and are much more well-defined in children than in adults, thus making them reliable responses with which to study auditory processing in children. Several studies have suggested that these temporal deflections, particularly the Tb peak, are markers of language disorders in children because smaller peak amplitudes and delayed peak latencies have been found in children with such disorders (Tonnquist-Uhlen, 1996; Bruneau et al., 2003; Groen et al., 2008; Shafer et al., 2011).
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Some of these studies also reported abnormal patterns of T-complex asymmetry. However, as well as those describing the T-complex in normal children, only partial information on auditory processing asymmetry was provided in these studies since stimuli were delivered either binaurally (Bruneau et al., 2003; Shafer et al., 2011) or monaurally to the left ear (Ponton et al., 2002; Tonnquist-Uhlen et al., 2003) or the right ear (Groen et al., 2008). Moreover, the rate of stimulation has been extensively demonstrated to affect the fronto-central N100 in both adults and children aged 8–11 years (e.g. Alcaini et al., 1994; Coch et al., 2005; Shelley et al., 1999; Sussman et al., 2008). Only one study has reported the influence of rate of stimulation on the Tb peak in children (Ceponiene et al., 1998). It indicated that the amplitude of the temporal negative peak corresponding to Tb increased with increasing inter-stimulus interval (350, 700, 1400, 2000 ms) thus indicating long refractoriness period for the underlying generator. Moreover in our initial work (Bruneau et al., 1997) comparing temporal responses of children and adults, long interstimulus intervals (between 3 and 5 s.) were used. It therefore appears that low rates of stimulation are favorable conditions for an accurate identification of the successive peaks of T-complex and of their asymmetry. The present study was performed in normally developing children and adults. The aim was to investigate asymmetry of the temporal Tcomplex peaks elicited by tonal stimuli delivered monaurally to each ear at different rates of stimulation corresponding to four stimulus asynchrony (SOA) conditions (from 700 to 3000 ms). 2. Methods 2.1. Subjects Twenty right-handed subjects participated in the study: 10 children (5 male) aged from 6 years 10 months to 8 years 9 months (mean ± SD: 7 years 11 months ± 8 months) and 10 adults (6 males) aged from 21 to 29 years (22 years 9 months ± 2 years 5 months). Participants were recruited from the immediate medical/research community and from local schools. All procedures were approved by the Ethics Committee (CCP) of the University Hospital of Tours. Adult participants and parents gave informed consent, and children gave assent after the experimental protocol had been explained to them. Participants (a parent for children) were interviewed to exclude previous and current diagnoses of learning, speech/language, hearing, emotional/behavioral, and neurological disorders. All the children were in age-appropriate grade at school. All participants were checked audiometrically for normal hearing in both ears before AEP recordings. 2.2. Stimuli and procedure The auditory stimuli used were 1100 Hz tone bursts of 50 ms duration (5 ms rise/fall times), calibrated to 70 dB SPL. They were delivered monaurally to the left ear (LE) and right ear (RE) through a TDH 39 headphone. Tones were presented with SOAs (onset-to-onset) of 700, 1100, 1500, and 3000 ms in separate conditions. A recording session consisted of 8 runs (4 SOA for RE and LE stimuli), each composed of 155 stimuli, separated by short breaks (1–3 min). 2.3. Procedure During the recording session, each subject was seated comfortably in a sound-treated room and watched a self-chosen silent movie during electroencephalography (EEG) recording. The order of presentation of the different runs was counterbalanced across participants. The total recording session was 45 min.
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2.4. EEG recordings The EEG was recorded from 28 Ag/AgCl scalp electrodes referenced to the tip of the nose. The ground electrode was placed on the forehead. Seventeen of the electrodes (including T3 and T4) were placed according to the international 10–20 system (Jasper, 1958). Additional electrodes were placed at intermediate positions and over the left and right mastoid sites. The ground electrode was on the forehead. The impedance value of each electrode was less than 10 kΩ. Horizontal and vertical electro-oculograms (EOG) were recorded differentially from 2 electrodes placed above and below the right ear for vertical EOG and at the outer canthus of each eye for horizontal EOG. The EEG and EOG were amplified with a bandpass filter (0.5–70 Hz; slope 6 dB/octave) and digitized at a sampling rate of 256 Hz. Epochs with movements or eye blinks exceeding ± 100 μV were discarded. Automatic correction of the deviations due to ocular activity was then applied (Anderer et al., 1989). EEG epochs were averaged separately for each SOA and each ear stimulated over a 500-ms analysis period, including a 100-ms prestimulus baseline, and were filtered digitally (0–30 Hz). 2.5. Data analysis AEP measurements were performed using ELAN software (Aguera et al., 2011). The study focused on AEPS recorded at the left and right temporal sites (T3 and T4, respectively). Temporal waveforms displayed the successive negative–positive–negative peaks Na, Ta, and Tb. Amplitudes and latencies of each peak were analyzed using repeatedmeasures analysis of variance (ANOVA) (Statistica — Version 10) with Group (children, adults) as the between-subject factor and hemisphere (Hem, T3 vs T4), ear stimulated (RE vs LE) and stimulus rate (4 SOA conditions) as the within-subject factors. When more than two levels (or one degree of freedom) were considered, the Greenhouse–Geisser epsilon correction was applied. F ratios with uncorrected degrees of freedom and corrected p values are reported. Post-hoc comparisons were made using Newman–Keuls tests. 3. Results Grand average AEP waveforms recorded in children and adults in the four SOA conditions at the right and left temporal sites are shown in Fig. 1. Temporal responses displayed similar waveforms in both groups, with the successive Na–Ta–Tb peaks. However, the Tb peak was the only peak which was well individualized and measurable in all children and adult subjects and allowed comparisons according to age. For both amplitude and latency of each deflection of the T-complex in children and of the Tb deflection in adults, no significant interaction was found between SOA and ear stimulated or hemisphere recorded, or between SOA and Hemisphere × Ear interaction. The effects of SOA on peak latency and amplitude are therefore presented separately from the effects of the other factors. The AEPs obtained in the four SOA conditions were pooled in order to provide better visualization of the effects of hemisphere and stimulated ear on peak latency and amplitude (Figs. 2 and 3). Results of the ANOVA analyses performed on latency and amplitude of each deflection are detailed in Table 1. 3.1. Peak latency asymmetry (Fig. 3, top; Table 1) 3.1.1. Na and Ta peak latencies in children Patterns of asymmetry were considered for the successive Na and Ta peaks only in children, with measurements obtained in all conditions for 8 out of 10 children for the Na peak and all children for the Ta peak. There were significant Hem × Ear interactions for Na and Ta peak latencies, without a significant main effect of ear stimulated or hemisphere recorded. Stimulation of either ear resulted in inter-hemispheric
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Fig. 1. Mean T-complex waveforms – consisting of successive Na, Ta and Tb peaks – recorded at the left (T3) and right (T4) temporal sites in children and adults in response to tones elicited at different rates of stimulation (four SOA conditions: 700, 1100, 1500 or 3000 ms).
asymmetry, with substantially earlier responses at the contralateral temporal site for both peaks. Considering each temporal site, both Na and Ta peaks occurred earlier for the contralateral than for the ipsilateral ear stimulation. These findings correspond to the classic asymmetry pattern of contralateral advantage for Na and Ta peak latencies.
left temporal site was 10 ms shorter for contralateral than for ipsilateral stimulation (p = .0007) and 10 ms shorter than the latency of Tb peak recorded at the right temporal site for both ipsi (p = .0005) and contralateral (p = .001) stimulation. The auditory processing underlying the Tb peak was therefore fastest in the right ear–left hemisphere condition.
3.1.2. Tb peak latency — children versus adults There was a significant main effect of group [F(1,18) = 35; p b .00002] due to significantly longer Tb peak latency in children (around 160 ms) than in adults (around 135 ms) and a significant Group × Hem × Ear interaction [F(1,18) = 7.2; p b .02]. ANOVA was then performed in each group separately and showed that Hem × Ear interaction was significant in children only, with a significant main effect of ear stimulated (Table 1). The asymmetry pattern was different for the Tb peak than for the preceding Na and Ta peaks in children, as indicated by the results of the Newman–Keuls post-hoc tests. Right ear stimulation resulted in substantially earlier Tb peak in the contralateral hemisphere, which was not the case for left ear stimulation. The Tb peak latency at the
3.2. Peak amplitude asymmetry (Fig. 3, bottom; Table 1) 3.2.1. Na peak amplitude asymmetry in children There was a significant main effect of hemisphere due to greater Na amplitude at the left than the right temporal site (mean ± s.e.m. = −3.1 ± 0.2 μV at T3; −1.9 ± 0.4 μV at T4) irrespective of the ear stimulated. 3.2.2. Ta peak amplitude asymmetry in children The Ta peak amplitude displayed a significant Hem × Ear interaction, without a significant main effect of ear stimulated or hemisphere recorded. A significant inter-hemispheric asymmetry was found for left ear stimulation only, with greater Ta peak amplitude at the right than
Fig. 2. Grand average T-complex waveforms recorded at the left (T3) and right (T4) temporal sites in children and adults according to ear stimulated (RE: right ear; LE: left ear). Responses were pooled for the four SOA conditions.
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Fig. 3. Mean (±standard error) peak latencies and amplitudes (absolute value) at the left (T3) and right (T4) temporal sites for the three successive peaks of the T-complex in children (negative Na, positive Ta and negative Tb peaks) and for the Tb peak in adults elicited by left ear (LE) or right ear (RE) stimulation. Stars indicated significant results at Newman–Keuls tests.
at the left temporal site. Only Ta peak at the right temporal site displayed a significant contralateral effect with greater amplitude for contralateral ear than for ipsilateral ear stimulation. 3.2.3. Tb peak amplitude — children versus adults The ANOVA indicated a significant main effect of group (F(1,18) = 16.4; p b .001) due to significantly greater Tb peak amplitude in children (around 5 μV) than in adults (around 3 μV) and a significant Group × Hem × Ear interaction [F(1,18) = 4.4; p b .05]. ANOVA
Table 1 Results of ANOVA performed on each peak of the T-complex using hemisphere (Hem: measures at T3 and T4), ear stimulated (left/right) and SOA (4 conditions) as within subject factors. Tb peak was the only peak measurable in all conditions in both groups. The interactions other than those indicated were non-significant. Results of post hoc comparisons are shown in Fig. 3. Children
Adults
Na
Ta
Tb
Tb
ns
ns
ns
ns F(1,7) = 22; p b .01 F(3,21) = 40; p b .0001 ε = 0.62
ns F(1,9) = 40; p b .001 F(3,27) = 5; p b .01 ε = 0.83
F(1,9) = 12; p b .01 ns F(1,9) = 24; p b .001 ns
ns
ns ns
ns ns
ns ns
Ear × Hem
ns F (1,7) = 6; p b .05 ns
SOA
ns
F(1,9) = 6; p b .05 F(3,27) = 5; p b .01 ε = 0.46
F(1,9) = 11; p b .01 F(3,27) = 6; p b .01 ε = 0.53
F(1,9) = 20; p b .011 ns
Latency Ear Hem Ear × Hem SOA
Amplitude Ear Hem
ns ns
performed in each group separately indicated a significant Hem × Ear interaction in both groups which was thereafter considered separately. In both children and adults, a significant inter-hemispheric asymmetry was found for left ear stimulation only, with greater Tb peak amplitude at the right than at the left temporal site. In children, as found for Ta, Tb peak at the right temporal site displayed a significant contralateral effect with greater amplitude for contralateral ear than for ipsilateral ear stimulation whereas in adults the contralateral effect was found significant at the left temporal site.
3.3. SOA effect (Fig. 1; Table 1) 3.3.1. Latency A significant main effect of SOA was found for Na and Ta peak latencies in children due to peak latency decrease with increasing SOA (mean ± SD: Na: 83 ± 1 ms, 79 ± 1 ms, 77 ± 1 ms, 76 ± 1 ms; Ta: 116 ± 2 ms, 114 ± 2 ms, 112 ± 2 ms, 110 ± 3 ms for SOA: 700, 1100, 1500, and 3000 ms, respectively). In contrast, there was no significant main effect of SOA on Tb peak latency in children or adults.
3.3.2. Amplitude Na peak amplitude in children did not display any significant main effect of SOA. In contrast, Ta peak amplitude displayed a significant main effect of SOA due to an increase in Ta peak amplitude with increasing SOA (from 2.3 ± 0.9 μV to 5.2 ± 1.7 μV for SOA 700 and 3000 ms, respectively). Tb peak amplitude of children and adults showed a main effect of SOA [F(3,54) = 7.9; ε = 0.55; p b .003] and a significant SOA × Group interaction [F(3,54) = 3.9; ε = 0,55; p b .04]. ANOVA performed in each group separately (Table 1) showed that the SOA effect was significant in children only. This was due to an increase in Tb peak amplitude with increasing SOA (from 4.2 ± 0.9 μV to 7.4 ± 1.2 μV for SOA = 700 ms and 3000 ms, respectively).
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4. Discussion We studied the asymmetry of the temporal-recorded auditory evoked potentials, named the T-complex, in 7- to 9-year-old children and in adults. The overall waveforms with the successive Na–Ta–Tb peaks were similar in both groups but were greater in amplitude and better defined in children than in adults. Amplitude and latency were measurable for the three peaks in children but only for Tb peak in adults. Amplitude measurements in children showed that the Na culminates in the left hemisphere, and the Ta and the Tb in the right hemisphere but for left ear stimulation only. In adults, the Tb peak amplitude was greater in the hemisphere contralateral to the stimulated ear. Patterns of asymmetry were different for the latency of the different peaks. Whereas the Na and Ta peaks of children displayed a classic contralateral latency effect (shorter latency on temporal site contralateral to the stimulated ear), the Tb peak displayed a right ear–left hemisphere timing advantage. This last result has important implications in view of previous data suggesting that neurophysiological mechanisms underlying Tb peak may be involved in language processes. 4.1. Effects of SOA on T-complex The SOA was found to influence the latency and amplitude of the Tcomplex peaks, irrespective of the ear stimulated and the temporal site being recorded. Na and Ta peak latencies decreased with increasing SOA in children, whereas Tb peak latency remained unchanged in both children and adults. Moreover, Ta and Tb peak amplitudes increased with increasing SOA in children, whereas the amplitudes of the Na in children and the Tb in adults were not affected, probably because the responses were too small and too variable in amplitude. Our results regarding the effects of SOA on the Tb peak in children are in accordance with those previously reported by Ceponiene et al. (1998) indicating increased amplitude and no modification of latency when SOA increased in the same range as that used in our study. Increase in amplitude with increasing SOA has been extensively reported for the fronto-central N1 response in adults and older children (e.g. Alcaini et al., 1994; Budd et al., 1998; Ceponiene et al., 2002; Coch et al., 2005; Roder et al., 1999; Shelley et al., 1999; Sussman et al., 2008), while discrepant results have been reported for modification of latency. Only two of these studies reported decreased latency with increasing SOA (Roder et al., 1999; Shelley et al., 1999). All of these authors interpreted the increase in amplitude with lengthening SOA as resulting from the refractory period of the neural assemblies involved in generation of the response. This explanation fits well with a decrease in peak latency with increasing SOA, as we found for Na and Ta peaks. However, increased amplitude might be associated with no effect on latency, as we found for Tb and as reported by Ceponiene et al. (2002), Coch et al. (2005) and Sussman et al. (2008) for the frontocentral N1 peak. The present findings therefore indicated a long refractory period for the generators underlying the different peaks of the T-complex since the effects of SOA were still present for the longest SOA used in our study (i.e., 3 s). 4.2. Maturation of the T-complex Temporal-recorded auditory responses were of greater amplitude and successive peaks are better defined in children than in adults, in agreement with previous findings on the T-complex (Bruneau et al., 1997; Tonnquist-Uhlen et al., 2003). In particular, the Tb peak recorded in all participants displayed longer latency and greater amplitude in children than in adults. These age-related latency differences might be related to maturation processes occurring throughout childhood in both auditory pathways and auditory cortical areas, such as maturation of the superficial cortical
layers (III and II) and their intracortical connections (Moore and Linthicum, 2007), as well as marked changes in axonal myelination and synaptic efficiency (Eggermont, 1992; Moore and Guan, 2001). The age-related amplitude differences might also be dependent on the evolution of location and/or orientation of neural generators contributing to scalp-recorded potentials which may be linked to changes in the relative geometry of the brain and skull during development (Dekaban, 1970). Moreover, the signal-to-noise ratio might be better in children than in adults partly due to the thinner temporal bone, resulting in greater responses from the temporal associative cortex in children. 4.3. Asymmetry of T-complex amplitudes Amplitude measurements indicated left hemisphere dominance of the Na peak. Predominance of Na(N1a) in the left hemisphere irrespective of the ear stimulated was reported in earlier studies in adults (Knight et al., 1988; Woods, 1995), whereas no findings have been reported in children. The subsequent Ta and Tb peaks of children displayed rightward lateralization but for left ear stimulation only. Responses were fairly symmetrical for right ear stimulation. Using left ear stimulation only, Tonnquist-Uhlen et al. (2003) found the same pattern of amplitude asymmetry for these two peaks. Our results on asymmetry of Tb peak amplitude are in accordance with results from a previous research examining asymmetry of AEP to monaural tones with source analysis of the radial activity recorded in the 140 ms latency range, corresponding to the Tb peak in adults (Picton et al., 1999; Hine and Debener, 2007). Several explanations can be proposed to justify such results. The temporal cortical regions involved in the generation of these deflections display anatomical asymmetry. The leftward asymmetry of the planum temporale surface and rightward asymmetry of the superior temporal sulcus (STS) and of the sulcal depth previously reported in adults (Geschwind and Levitsky, 1968; Ochiai et al., 2004; Van Essen, 2005), already present in infants (Dubois et al., 2010; Glasel et al., 2011; Hill et al., 2010), were recently reported in 8- to 9-year-old children (Bonte et al., 2013). These authors also described asymmetry in the slope of the Sylvian Fissure, with a steeper slope in the right than in the left hemisphere. Such anatomical asymmetry could conceivably produce hemispheric differences in the orientation and/or location of the generators underlying the different peaks, predominant in the left hemisphere for Na, and in the right hemisphere for Ta and Tb. Interhemispheric differences in the cortical folding of the auditory cortex have also to be considered. In a recent MEG study (Shaw et al., 2013), it was demonstrated that rightward lateralization of MEG auditory responses might be due to a greater degree of cortical folding in the left auditory cortex. Sources in an extended area of activation might then generate magnetic fields with varying polarity that superpose or cancel each other, depending on the local geometry of the cortex. A similar explanation might also be proposed for rightward lateralization of auditory evoked potentials, such as Ta and Tb peaks and for their sensitivity to ear stimulated, recorded on the right and not on the left temporal site. Moreover our results indicate dissociated patterns of asymmetry for peak amplitude and latency; this fits well with this explanation since folding can be hypothesized to influence amplitude but not latency. Interestingly, in children, only responses on the right temporal site seemed to be sensitive to the ear stimulated. This result is consistent with specialization of the lateral right auditory cortex for spatial sound processing as previously demonstrated by Zatorre and Penhune (2001). Indeed sound localization mostly relies on the differences in acoustic input reaching the cortex, and therefore on the differential processing of input from the left and right ears. This sensitivity of the right hemisphere to the stimulated ear indicates that T-complex amplitude recorded at the right temporal site also reflects asymmetry of ear-to-hemisphere connectivity. Indeed, each ear sends a larger number of fibers to the contralateral cortex than to the ipsilateral cortex
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(Rosenzweig, 1951). This asymmetrical connectivity was not observed in the T-complex recorded at the left temporal site since its amplitude was not dependent on the ear stimulated. We might therefore hypothesize that this left T-complex is more dependent on cortical processing occurring at the left temporal site than on auditory input associated with asymmetry of ear-to-hemisphere connectivity. 4.4. Asymmetry of T-complex latencies In children, Na and Ta peak latencies displayed a typical contralateral effect at both temporal sites (shorter latency on contra than on ipsilateral temporal site). Although nothing has been reported on asymmetry of Na peak latency, a similar contralateral Ta peak latency effect has been reported in children by Tonnquist-Uhlen et al. (2003) for left ear stimulation only. In addition to the greater number of fibers, contralateral afferents cross the midline at the brainstem with a more direct pathway, and fewer synapses to the cortex (Adams, 1979; Brunso-Bechtold et al., 1981; Coleman and Clerici, 1987). This could explain the shorter latency of contra- compared to ipsilateral responses. This does not explain the results obtained for Tb peak latency which displayed a right ear–left hemisphere (RE–LH) timing advantage: the Tb peak occurred earlier at the left temporal site for contra- than for ipsilateral stimulation and earlier than the Tb peak recorded at the right temporal site regardless of ear stimulated. Early intracranial recordings and lesion studies have suggested that Tb reflects activity from the lateral surfaces of the superior temporal gyrus (Celesia, 1968; Celesia and Puletti, 1969). Studies using dipole modeling in adults have attributed the Tb response to bilateral radial dipoles located in the secondary auditory cortex in the lateral aspects of the temporal lobes (Scherg and Von Cramon, 1985, 1986; Albrecht et al., 2000; Ponton et al., 2002). The faster RE–LH processing might be related to the properties of the left auditory cortex allowing faster auditory processing and greater sensitivity to rapid acoustic changes as is required for speech processing. Possible microstructural asymmetry of auditory cortical areas has been proposed to explain such lateralized processing (Zatorre and Belin, 2001; Zatorre and Gandour, 2008). Faster temporal processing in the left hemisphere is suggested to be related to the greater volume of white matter tissue in the left than in the right hemisphere, due to greater myelin sheath thickness in the left hemisphere as shown by post mortem analysis of the posterior temporal lobe (Anderson et al., 1999). Moreover, several studies have indicated that the auditory processing reflected in the Tb peak may be critical for language. Delayed, deviant or absent Tb peaks have been reported in clinical populations with language impairments such as children with SLI (Tonnquist-Uhlen, 1996; Shafer et al., 2011), children with autism (Bruneau et al., 1999, 2003), and children with Down syndrome (Groen et al., 2008). The shorter RE–LH Tb latency might thus be due to faster neuronal communication between auditory areas involved in Tb generation and in language processing in the left hemisphere. The present study shows for the first time that both the Na and the Ta peak occur earlier at the temporal site contralateral to the stimulated ear in children whereas the Tb peak latency presented a particular pattern, with the shortest latency in the left hemisphere after right ear stimulation suggesting faster neuronal communication within the left auditory cortex. 4.5. Asymmetry in Tb peak latency and right ear advantage The present results on Tb peak latency could reflect fundamental auditory processes, such as those related to superiority of the dominant hemisphere in dichotic listening (Hellige, 1993; Davisdson and Hugdahi, 1998 for reviews). Dichotic listening is a standard task which is mainly used to study auditory lateralization. Using verbal material in right-handed subjects, stimuli presented to the right ear are more efficiently processed than those presented to the left ear. This right ear advantage (REA) has been widely attributed to the left hemisphere
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supremacy in language perception and the contralateral pathway dominance in auditory signal transmission. Whereas the input of the right ear is immediately transferred to the left-hemisphere language receptive areas, the input of the left ear entering the right hemisphere requires callosal transfer to the left hemisphere in order to be processed, and thus needs extra transfer time. According to this structural model, termed “callosal relay” model (Zaidel, 1983), the magnitude of the ear advantage would be directly related to the functional properties of the corpus callosum (Westerhausen and Hugdahl, 2008). Only one study was performed in adults in order to relate asymmetry of auditory evoked potentials and REA in dichotic listening (Eichele et al., 2005). It focused on the N100 peak asymmetry measured at left and right temporal sites in response to two different syllables presented dichotically. A relationship was found between the individual differences in asymmetry of the N100 peak and the ear advantage evaluated with dichotic listening. Since the significant measurements were those from temporal sites, the authors suggested a possible influence of the T-complex in the effect observed. Our findings suggest that in children interhemispheric differences in Tb peak latency at temporal sites could reflect the right ear advantage. Moreover, our results provide an approximation of the duration of callosal transfer in children since right-ear input seemed to reach the left auditory cortex 10 ms earlier than auditory information from the left ear. Therefore, the present results not only provide extensive information on the asymmetry of latency and amplitude of the different peaks of the T-complex in children, but also, more importantly, indicate that the Tb peak in children would be a good candidate marker of ear preference in dichotic listening in children. Besides being a marker of lateralized temporal lobe language function, the Tb peak would be a marker of functional inter-hemispheric interaction and connectivity in children. 5. Disclosure statement All authors declare they have no financial interest, and no current or potential conflicts of interest. Acknowledgments We thank all of the participants for their cooperation, Rémy Magné for preparation of the figures and Doreen Raine for correction of the English language. References Adams, J.C., 1979. Ascending projections to the inferior colliculus. J. Comp. Neurol. 183, 519–538. Aguera, P.E., Jerbi, K., Caclin, A., Bertrand, O., 2011. ELAN: a software package for analysis and visualization of MEG, EEG, and LFP signals. Comput. Intell. Neurosci. 2011, 158970. Albrecht, R., Suchodoletz, W., Uwer, R., 2000. The development of auditory evoked dipole source activity from childhood to adulthood. Clin. Neurophysiol. 111, 2268–2276. Alcaini, M.,Giard, M.H.,Thevenet, M.,Pernier, J., 1994. Two separate frontal components in the N1 wave of the human auditory evoked response. Psychophysiology 31, 611–615. Anderer, P., Semlitsch, B., Saletu, B., 1989. Ein Korrekturverfahren zur Reduktion okulärer Artefakte in der EEG- und ERP- Topographie. In: Saletu, B. (Ed.), Fortschritte in der Biologischen Psychiatrie. Thieme, Stuttgart, New York. Anderson, B.,Southern, B.D.,Powers, R.E., 1999. Anatomic asymmetries of the posterior superior temporal lobes: a postmortem study. Neuropsychiatry Neuropsychol. Behav. Neurol. 12, 247–254. Bonte, M., Frost, M.A.,Rutten, S., Ley, A.,Formisano, E., Goebel, R., 2013. Development from childhood to adulthood increases morphological and functional inter-individual variability in the right superior temporal cortex. Neuroimage 83, 739–750. Bruneau, N.,Gomot, M., 1998. Auditory evoked potentials (N1 wave) as indices of cortical development throughout childhood. In: Garreau, B. (Ed.), Neuroimaging in Child Neuropsychiatric Disorders. springer, pp. 113–124. Bruneau, N., Roux, S., Guerin, P., Barthelemy, C., Lelord, G., 1997. Temporal prominence of auditory evoked potentials (N1 wave) in 4–8-year-old children. Psychophysiology 34, 32–38. Bruneau, N.,Roux, S.,Adrien, J.L.,Barthelemy, C., 1999. Auditory associative cortex dysfunction in children with autism: evidence from late auditory evoked potentials (N1 wave-T complex). Clin. Neurophysiol. 110, 1927–1934.
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