Maturation of obligatory auditory responses and their neural sources: Evidence from EEG and MEG
Highlights
► EEG and MEG measured in children (9 to 10 years) and adults. ► Similar auditory cortex sources of evoked fields in children and adults. ► Frequency-specific N1 is mature at 9 to 10 years of age.
Introduction
In the last two decades, the number of studies investigating auditory processes in school-aged children with methods such as electroencephalography (EEG) and magnetoencephalography (MEG) has been growing steadily (e.g., Cardy et al., 2004, Korpilahti and Lang, 1994, Kotecha et al., 2009, Paetau et al., 1995, Sussman et al., 2008). Based on these and other studies, it has become common knowledge that event-related potentials (ERPs) as measured with EEG and event-related fields (ERFs) as measured with MEG change over the whole life span (for an overview of auditory ERP development from childhood to late adulthood, see Mueller et al., 2008). These changes can be due to maturation of the white and the gray matter volume affecting processing speed and processing efficiency (Albrecht et al., 2000, Caviness et al., 1996, Tonnquist-Uhlén et al., 1996), and to the progressive folding of the cortex (Moore and Guan, 2001). This probably leads to shorter latencies, larger amplitudes, and different topographical distributions in the children's ERPs/ERFs (Pang and Taylor, 2000, Ponton and Eggermont, 2007). Many of the studies so far focused on the maturation of single ERP/ERF components (e.g., elicited by simple tones). Studies providing a comparison of ERPs/ERFs as well as their underlying cortical mechanisms in adults and children are sparse (for reviews, see Ponton and Eggermont, 2007, Wunderlich and Cone-Wesson, 2006). The current study aims to shed more light on this issue.
In the following, findings on maturation of ERPs and ERFs will be outlined. We will use the nomenclature derived from EEG research in adults to describe wave peaks indicating polarity and position in time – as in P1 and N1 for first positive/negative deflection – and add an uncapitalized “m” (as in magnetic) to indicate MEG components.
In adults, sinusoidal tones evoke a P1 followed by a prominent N1, sometimes succeeded by a P2 and an N2 (Picton et al., 1974, Mueller et al., 2008, Wunderlich et al., 2006). This polyphasic response, however, is in contrast to the biphasic response consisting of a P1 and an N2 typically found in school-aged children (≈ 6–12 years; Albrecht et al., 2000, Bishop et al., 2007, Ĉeponienė et al., 2005, Fox et al., 2010, Korpilahti and Lang, 1994, Sussman et al., 2008, Wetzel et al., 2011). Such ERP patterns are typically observed when tones are presented in quick succession (Ĉeponienė et al., 1998, Sussman et al., 2008). Based on MEG findings, it has been suggested that the P1m is the most prominent and replicable indicator of auditory processing in children (Cardy et al., 2004, Kotecha et al., 2009) in contrast to the N1m in adults. These early components are functionally linked to sensory auditory processing, perception and sensory gating.
Although the N1 is rarely observed in children, the maturation of the auditory N1 has been in the focus of research (Bruneau et al., 1997, Fox et al., 2010, Karhu et al., 1997, Pang and Taylor, 2000, Ponton et al., 2002, Poulsen et al., 2009, Rojas et al., 1998, Tonnquist-Uhlén et al., 1996), probably due to its prominence in adults. The N1 has been observed in children at six years of age, but only when tones were presented at slow rates, i.e., a stimulus onset asynchrony (SOA) of more than 3 s (Bruneau et al., 1997, Ĉeponienė et al., 1998, Takeshita et al., 2002). When the SOA is between 1 to 3 s, some studies report an N1 at around eight years of age (Ĉeponienė et al., 1998, Gilley et al., 2005, Kotecha et al., 2009), while others observe it at 11 to 13 (Albrecht et al., 2000, Ĉeponienė et al., 2005). With even faster presentation (SOAs of less than a second), the N1 is not observed before adolescence (13–14 years and later; Gilley et al., 2005, Pang and Taylor, 2000, Sussman et al., 2008). Consequently, Ponton et al. (2002) speculated that it is not the absence of the N1 but more a superimposition of the strong P1 that leads to the N1 being obscured. However, others suggest that the N1 is less developed and therefore recommend focusing on the P1 to investigate auditory development and developmental abnormalities (Cardy et al., 2004, Kotecha et al., 2009). In studies were the N1 was elicited, it was found to be smaller and delayed in children (Gilley et al., 2005, Mueller et al., 2008, Takeshita et al., 2002, Wunderlich and Cone-Wesson, 2006).
Interestingly, the maturation of the auditory P1(m), although much more prominent in children, is far less investigated (Cardy et al., 2004, Ĉeponienė et al., 1998, Kotecha et al., 2009). It is assumed that the P1 develops in early childhood (Ponton and Eggermont, 2007, Moore and Linthicum, 2007) and reaches its maximum amplitude in toddlers, while it declines thereafter (Ponton et al., 2002, Wunderlich et al., 2006). It has been argued that this amplitude decrease may in part be a result of the emerging N1 component (Ponton and Eggermont, 2001).
Evidence on the N2(m) wave in school-aged children is similarly sparse. This component is already observed in early childhood (Moore and Linthicum, 2007, Wunderlich et al., 2006) and persists into adolescent years (Sussman et al., 2008). Earlier studies interpreted the N2 in terms of a delayed N1 (Korpilahti and Lang, 1994, Kurtzberg et al., 1995). However, there is strong evidence that this negativity, peaking at around 250 ms, in fact corresponds to the adult N2 (Albrecht et al., 2000, Johnstone et al., 1996).
The neural generators of auditory event-related responses in children have been shown to be highly similar to the generators observed in adults. For adults, the P1(m) as well as the N1(m) have been localized in auditory cortex regions (for a review, see Eggermont and Ponton, 2002), with some studies being able to dissociate the two cortically, with the P1 being localized in the primary cortex and the N1 in the secondary cortex, both moving laterally with decreasing frequency (e.g., Liégeois-Chauvel et al., 2001). A similar pattern has been reported for the P1(m) and the N2(m) in children, showing strongest activations of auditory cortex areas in the superior temporal gyrus (STG). Most of these studies used a dipole model to localize the neural generators by seeding a dipole in regions of the auditory cortex and constraining the location (Bishop et al., 2011, Kotecha et al., 2009, Pang et al., 2003, Ponton et al., 2002, Poulsen et al., 2009, Takeshita et al., 2002). Furthermore, previous MEG studies in children mainly used a sphere/inner skull as a source space for the localization, while the precise brain anatomy of the participants was disregarded (Pang et al., 2003, Takeshita et al., 2002).
The current study was designed to shed more light on the maturation of early auditory brain responses and their underlying neural generators. On this account, neural responses elicited by simple tones were measured in school-aged children (9–10 years) and adults using anatomically constrained MEG. Additionally, EEG was recorded in a separate session in order to relate the MEG findings to ERP responses. The main focus was on the P1(m)–N2(m) complex in children, which has previously been shown to be the most prominent ERP/ERF pattern. We explicitly aimed to investigate whether the N1(m) can be observed in school-aged children at a fast presentation rate, commonly applied in adults. On this account, a two-condition design was utilized, whereby a sine tone was presented either repetitively or in a random sequence with other tones. Our design was based on the finding that a large N1 component is observed in adults when tones are presented randomly as compared to repetitive stimulation (Horváth et al., 2008, Jacobsen and Schröger, 2001, Maess et al., 2007). However, the current paradigm should not affect the P1 and N2 as this effect was only observed for the N1, and has been related to refractory states of the underlying neuronal population.
Section snippets
Participants
Two groups of different ages – 20 adults (10 females, mean age 28, range: 24 to 34) and 15 children (9 females, mean age 9; 9 [Year; Month], range: 9; 1 to 10; 9) – participated in the MEG part of the current experiment. All participants were right-handed. Ten participants from each age group repeated the experiment in an EEG setup. All adult participants and, in the case of the children, their parents, gave written consent prior to testing. All reported normal hearing and a history free of
MEG data
In adults, the rmANOVA for the time window of the P1m (50–80 ms) revealed no main effect of Condition or Hemisphere (F(1,19) = 1.539, p = 0.230; F(1,19) = 0.402, p = 0.534 respectively), nor a Condition × Hemisphere interaction (F(1,19) = 0.905, p = 0.353). The rmANOVA for the N1m time window (90–130 ms) revealed a main effect of Condition (F(1,19) = 13.492, p = 0.002, η2G = 0.188), confirming higher N1m amplitudes for tones in the random compared to tones in the repetitive condition. Furthermore, the main effect of
Discussion
The focus of the current study was to investigate the maturation of early auditory processing. For this purpose, we used a sophisticated paradigm in school-aged children and adults while measuring EEG and MEG. In the following, the findings in children are discussed first, followed by the findings in adults. Finally, effects in children and adults will be related to each other.
Conclusion
In the present study, we investigated the maturation of early auditory responses using EEG and MEG. The two methods showed rather similar results for the initial responses namely the P1(m) and N2(m) in children and the P1(m) and N1(m) in adults. Source localization of the MEG data revealed comparable sources of obligatory responses in both age groups, mainly in primary auditory cortices, indicating mature neural sources of the investigated components. Most importantly, the present EEG data
Acknowledgments
The authors wish to thank Ulrike Barth, Kristiane Werrmann and Yvonne Wolff for help with data collection. We wish to thank Jens Brauer for help with preprocessing of the children's MRI scans. Furthermore, we want to thank Rosie Wallis for proofreading the manuscript. PR and BH were supported by the Deutsche Forschungsgemeinschaft, graduate program “Function of Attention in Cognition” at the University of Leipzig. We thank two anonymous reviewers for their very helpful comments.
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