Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling

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Abstract

Objectives: Previous studies have shown that observed patterns of auditory evoked potential (AEP) maturation depend on the scalp location of the recording electrodes. Dipole source modeling incorporates the AEP information recorded at all electrode locations. This should provide a more robust description of auditory system maturation based on age-related changes in AEPs. Thus, the purpose of this study was to evaluate central auditory system maturation based dipole modeling of multi-electrode long-latency AEPs recordings.

Methods: AEPs were recorded at 30 scalp-electrode locations from 118 subjects between 5 and 20 years of age. Regional dipole source analysis, using symmetrically located sources, was used to generate a spatio-temporal source model of age-related changes in AEP latency and magnitude.

Results: The regional dipole source model separated the AEPs into distinct groups depending on the orientation of the component dipoles. The sagittally oriented dipole sources contained two AEP peaks, comparable in latency to Pa and Pb of the middle latency response (MLR). Although some magnitude changes were noted, latencies of Pa and Pb showed no evidence of age-related change. The tangentially oriented sources contained activity comparable to P1, N1b, and P2. There were various age-related changes in the latency and magnitude of the AEPs represented in the tangential sources. The radially oriented sources contained activity comparable to the T-complex, including Ta, and Tb, that showed only small latency changes with age. In addition, a long-latency component labeled TP200 was observed.

Conclusions: It is possible to distinguish 3 maturation groups: one group reaching maturity at age 6 and comprising the MLR components Pa and Pb, P2, and the T-complex. A second group that was relatively fast to mature (50%/year) was represented by N2. A third group was characterized by a slower pattern of maturation with a rate of 11–17%/year and included the AEP peaks P1, N1b, and TP200. The observed latency differences combined with the differences in maturation rate indicate that P2 is not identical to TP200. The results also demonstrated the independence of the T-complex components, represented in the radial dipoles, from the P1, N1b, and P2 components, contained in the tangentially oriented dipole sources.

Introduction

Studies of age-related changes in auditory evoked potentials (AEPs) have demonstrated at least 3 features of human central auditory system maturation. First, maturation rates are not the same throughout the auditory system (Ponton et al., 1996a, Ponton et al., 1996b). Second, comparisons of maturation rates for latencies of the different AEP peaks indicate that this activity must arise from parallel subsystems in the thalamo-cortical pathway, since the early maturing peak P2 has a longer latency than the more slowly maturing shorter latency N1b (e.g. Ponton et al., 1996a, Ponton et al., 2000a). Third, generators or pathways contributing to a single evoked response peak may be distinguished by very different maturation rates. For example, the middle latency response (MLR) peak Pa, appears to represent the sum of activity from two generators and two different pathways with very different maturation rates (McGee and Kraus, 1996).

Almost exclusively, AEP maturation has been assessed by measuring the age-related changes in latencies and magnitudes of peaks at selected scalp electrode locations. However, when AEPs are sampled by an array of electrodes distributed across the scalp, it is apparent that the pattern of AEP maturation depends on the location of the recording electrode (e.g. Bruneau et al., 1997, Ponton et al., 2000a). As shown for electrodes Pz, Cz, and Fz in Fig. 1, age-related changes in AEP morphology vary significantly even for nearby locations on the scalp. The variation in AEP maturation as a function of scalp electrode location reflects the weighted contribution of activity from different sources, each with potentially different maturation rates. Electrode-by-electrode AEP analyses may be appropriate when waveform morphology is relatively constant, but this approach has significant limitations when the AEPs undergo dramatic morphological and scalp distribution changes as a function of the variable of interest; in this case, age. An ideal approach would provide a maximal separation of maturational changes per auditory pathway or cortical projection area.

A dipole model of AEP maturation based on activity recorded from a distribution of electrodes covering large areas of the scalp may provide a more robust representation of auditory system maturation. Spatio-temporal source modeling (STSM), a form of dipole source analysis, takes into account the scalp distribution and timing of the AEPs at all electrodes across the entire recording epoch (Scherg and Von Cramon, 1985, Scherg and Von Cramon, 1986, Achim et al., 1991). Regional dipole source modeling, a form of STSM described by Scherg (1990), assumes 3 orthogonally oriented dipoles with a common location. For AEPs, regional sources are placed in each hemisphere in order to model the origins of auditory cortical activity in both the left and the right temporal lobes. This is illustrated in Fig. 2a. To simplify regional dipole source modeling, an additional constraint of symmetry may be applied so that the regional sources must be in the same relative location in each hemisphere (Scherg and Von Cramon, 1986). Ponton et al. (1993a) previously used this approach to compare the obligatory P1–N1b–P2 complex in normal-hearing adults and in adults and children fitted with a cochlear implant. If the location of the regional source is also constrained, along with the orientation of each of the 3 orthogonal component dipoles, then the analysis essentially operates like a spatial filter. This dipole spatial filter analysis provides a method of separating AEP components based on the orientation of their underlying generators. Using this approach, the only factor that remains variable is the time-varying dipole moment (i.e. strength). Age-related changes in dipole strength may represent maturational alterations in the degree of synchronization, as well as the orientation and number of contributing neural generators.

The use of a regional dipole model as a spatial filter provides the potential opportunity to assess separately the maturation of those AEP components that have sufficiently large orientation differences in their underlying neural generators. For example, the MLR peaks Pa and Pb are well-represented by recordings from electrode pairs located along the sagittal midline of the head; for example, one at C7 and another at Cz or Fz (e.g. Cacace et al., 1990, Nelson et al., 1997). Thus, dipole sources oriented parallel to the sagittal plane, i.e. along the anterior–posterior axis (see Fig. 2c), should contain the AEP peaks, Pa and Pb. Due to the location and orientation of generators (i.e. the cortical pyramidal cells) perpendicular and close to the superior surface of temporal lobe, activity from primary auditory cortex should be maximally represented in the tangential (vertical) sources. As shown in Fig. 2b, c, secondary auditory areas (mainly Brodman's area 22 in Fig. 2c, red shading in Fig. 2b) surround the primary cortical areas (Brodman's areas 41 and 42 in Fig. 2c, green and yellow shading in Fig. 2b) on the superior surface of the temporal lobe. Thus, the tangential source incorporates activity mainly from primary areas as well as from secondary (belt) areas. Previous studies have shown that the tangential sources contain the AEP peaks P1, N1b, P2, and N2 (e.g. Scherg and Von Cramon, 1985, Scherg and Von Cramon, 1986, Knight et al., 1988, Ponton et al., 1993a, Albrecht et al., 2000). Secondary auditory cortex also extends onto the lateral surface of superior temporal cortex (Kaas and Hackett, 1998). This lateral surface is approximately perpendicular to the superior surface of the temporal lobe. Consequently, radially oriented dipole sources are effectively blind to activity generated by secondary areas located on the superior surface of the temporal lobe. Thus, the radial (lateral) dipole sources isolate activity originating from secondary (parabelt areas) auditory cortical areas on the lateral surface of the temporal lobe. AEP components reflected in the radial sources include the T-complex components Ta and Tb (e.g. Scherg and Von Cramon, 1985, Scherg and Von Cramon, 1986, Knight et al., 1988, Ponton et al., 1993a, Albrecht et al., 2000). This limited division of activity from primary and secondary auditory cortical areas into the tangential and radial sources, respectively, provides an opportunity to at least partly assess the maturation of AEP activity originating from each of these areas separately.

The purpose of this study is to describe central auditory system maturation using age-related changes in AEPs subjected to regional dipole spatial filtering. Based on the age-related changes in AEP activity represented in each of the orthogonal dipole sources, this analysis may distinguish maturational differences in primary (core) and secondary (belt and parabelt) cortical areas and the pathways that dominantly project to these regions. The analyses described in this study are based on AEP data previously reported by Ponton et al. (2000a). The subject population and data collection procedures have been described in Ponton et al. (2000a), but will be reviewed in detail.

Section snippets

Subjects

All individuals tested were neurologically normal (no reported head injuries resulting in a loss of consciousness) with pure-tone thresholds ≤25 dB HL (ANSI 1989) for the audiometric frequencies between 0.5 and 8 kHz. Data from 118 subjects representing 137 test sessions are included in the analyses; 7 subjects were tested twice and 6 subjects were tested 3 times. At least 1 year elapsed between sessions for those subjects who were tested on more than one occasion. As shown in Table 1, all

Dipole source waveforms

Fig. 3 presents the time-varying dipole moment waveforms calculated for each of the 3 orthogonal components of the regional dipole sources located in the hemispheres ipsilateral and contralateral to the stimulated ear. Source waveforms for the sagittally oriented dipoles shown in Fig. 3a contain two peaks with latencies consistent with the Pa and Pb components of the MLR. While the latencies of these peaks show no consistent variation as a function of age, magnitude changes result in some

Discussion

Results of the regional spatial filter analysis demonstrated that the 3 orthogonal dipole components isolate 3 distinct sets of AEP components. The MLR peaks Pa and Pb are best represented by the sagittal dipole sources, the ‘classic’ P1–N1b–P2–N2 sequence is isolated to the tangential sources perpendicular to the superior surface of the temporal lobe, and the T-complex peaks Ta and Tb, together with the TP200, are represented in the radial dipole sources. The grouping of AEP components

Acknowledgements

We wish to acknowledge the contributions of Ann Masuda, who collected some of the data in the early phases of this project.

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