Elsevier

Clinical Neurophysiology

Volume 111, Issue 3, 1 March 2000, Pages 388-397
Clinical Neurophysiology

Tracking the development of the N1 from age 3 to adulthood: an examination of speech and non-speech stimuli

https://doi.org/10.1016/S1388-2457(99)00259-XGet rights and content

Abstract

Objectives: To examine developmental changes in the N1a, N1b and N1c evoked by a tone and a speech consonant (/da/).

Methods: Subjects (n=70 for tones; n=69 for /da/) were grouped into 2 year intervals (age 3–16) and adults. They listened to a tone (2 kHz; 36 ms; 77 dB SL; ISI=600 ms; n=346) or a speech consonant /da/ (female voice recording; 7 ms VOT; 212 ms; 72 dB SL; ISI=600 ms; n=349) while watching a Disney® screensaver. EEG was recorded from 26 electrodes referenced to Cz. An averaged reference was computed off-line. Amplitude and latency data were analyzed with repeated-measures ANOVAs for age×electrode, and age×N1 component, respectively.

Results: Left hemisphere N1a was mature before age 3 whereas the right hemisphere N1a matured around 7–8 years. The vertex N1b showed a parietal distribution which shifted anteriorly with age. The N1c showed age- and stimulus-related changes. The N1c measured over the left hemisphere matured earlier than the N1c over the right hemisphere. The N1c to /da/ matured earlier than that to tones.

Conclusions: Auditory processing undergoes steady and subtle developmental changes. These changes follow different maturational patterns depending on the type of stimuli. The evidence suggests earlier development of the left hemisphere and earlier development of the generators underlying speech processing.

Introduction

An important factor in the development of language and speech function is the normal maturation of auditory processing. Although many behavioral studies have examined how language and speech develop, it is more difficult to investigate auditory processing using behavioral measures. A method that has been employed successfully to study auditory processing in adults is the auditory evoked potential, N1.

The auditory N1 is well understood in adults, and it is known that the N1 consists of multiple components observed at the vertex and over temporal sites (Näätänen and Picton, 1987). The vertex N1 (or N1b), evoked at about 100 ms to tones, is a fronto-central negativity generated by bilateral vertically oriented dipoles on the supratemporal planes of the auditory cortices (Vaughan and Ritter, 1970). The T-complex N1 (Wolpaw and Penry, 1975) is largest at temporal electrodes and consists of a negative component, the N1a, at approximately 75 ms, and a second negative component, the N1c, at approximately 130 ms (McCallum and Curry, 1980; Giard et al., 1994). This complex originates in the auditory association cortices in the superior temporal gyri and can be modeled by bilateral radially-oriented dipoles (Scherg and von Cramon, 1986).

There is much less literature regarding the N1 in children. The evidence to date suggests that the N1 changes with age, but whether all of the components change and whether these changes occur synchronously remains unknown. An early study (deCrévoisier et al., 1975) used a coronal chain of 11 electrodes to measure the N1 to tones in children aged 2–15 years. They found that in children younger than 8 years, the maximal N1 was observed at the temporal electrodes at a latency of approximately 178 ms, while in children older than 10 years, the maximal N1 was observed closer to the vertex at a latency of 97 ms. In light of our current knowledge of N1 components, this study suggests that the predominant contributions of the N1b and N1c may change as a function of age. As well, Goodin et al. (1978) measured the N1 to tones in subjects aged 6–76 years at midline, C3, C4, P3 and P4. They did not find significant amplitude changes but report that there was a striking change in the distribution of the N1 for the children from a predominantly parietal distribution to the adult centro-frontal distribution. Another study (Bruneau et al., 1997) measured the N1 to tones with electrodes at midline, T3 and T4. They found that in the 4–8 year old group, the temporal N1 was of greater amplitude than the vertex N1 whereas this pattern was reversed in the adult group. These results corroborate those of deCrévoisier et al. (1975).

Two other studies have examined topographical changes in the N1 with development. Tonnquist-Uhlén et al. (1995) used 17 electrodes to map the foci of the N1 evoked by tones in children aged 8–16. They found no changes in amplitude although they report a distinct fronto-central focus in the distribution of the N1 in children which shifted towards the right side with increasing age. Oades et al. (1997) tested subjects aged 8–22, also using tonal stimuli and measuring at 15 electrodes. In contrast to Tonnquist-Uhlén et al. (1995), they reported that the N1 was biased to the right in the 10–14 year old group, but this shifted to a left bias after the mid-teens. The topology changes reported by these two groups may differ for a number of reasons. The most probable explanation is that the ERPs of children show high variability; thus, the use of small sample sizes within broad age ranges cannot map out developmental changes, particularly if these changes are small and progressive over a number of years. Thus far, the evidence is suggestive, although not convincing, that the N1 shows developmental changes.

A second question of interest is whether the N1 develops differently for speech and non-speech stimuli. In adults, the mechanism underlying the N1 seems to be the same for acoustic and phonetic stimuli, since no differences were observed between tones and speech consonants with surface electrodes (Lawson and Gaillard, 1981; Woods and Elmasian, 1986) or MEG (Hari et al., 1987). Given the importance of auditory processing to language learning and comprehension, it would be of interest to determine if language processors show differential development to speech and non-speech stimuli.

Clearly, there is a need to map out changes in each of the three components of the N1, using larger sample sizes within smaller age ranges and a larger number of electrodes, while examining speech and non-speech stimuli. This paper reports two series. One presents tonal and the other presents speech stimuli. The three components of the N1 were recorded to both stimulus types using a full head of electrodes in children aged 3–16 years, divided into 2 year blocks. This paper will follow the terminology of Giard et al. (1994), where N1a and N1c refer to the two negative components of the T-complex and N1b refers to the vertex N1.

Section snippets

Subjects

All subjects were volunteers recruited by advertisements placed in a local daily newspaper and children of hospital staff and friends. All subjects were in good health at testing, had normal hearing and reported normal histories, neurologically and psychologically. Informed consent was given by both the child and the legally responsible adult; this study was approved by the Human Ethics Review Board at the Hospital for Sick Children.

Tone study

Grand averaged waveforms, for all electrodes, for the oldest (adult), middle (11–12 years) and youngest (3–4 years) groups are shown in Fig. 1. As expected for the adult group, a clear N1b to the tone is observable at Fz and Cz at approximately 120 ms; the N1a and N1c are observable at the temporal electrodes at a latency of 80 ms and 170 ms, respectively. This figure suggests progressive changes in the amplitudes of the N1a, N1b and N1c from the adult to the middle to the youngest age group.

Discussion

In adults, for both the tone and speech consonant study, the vertex N1b and the T-complex, N1a and N1c, are consistent with the literature. For the developmental data, there are significant, progressive changes in the morphology and distribution of the N1 across the age groups. These patterns of change both confirm previous results (deCrévoisier et al., 1975; Goodin et al., 1978; Bruneau et al., 1997) and provide interesting and definitive extensions to the literature. As well, examination of

Acknowledgements

This work was supported by a Hospital for Sick Children Research Fellowship (RESTRACOM) to the first author. The authors would like to thank Gillian Edmonds for her assistance.

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