Event-related oscillations in the theta (4-7 Hz) frequency range define the theta frequency component of the event-related brain potentials (ERPs) or the EEG theta response. Prominent theta responses have been observed in various experimental conditions in both humans and animals and have been assigned an important role in integrative stimulus processing  (Miller, 1991; Schürmann & Basar, 1994). The scalp recorded theta responses have been suggested to reflect the functioning of a diffuse and distributed theta system in the brain (Basar-Eroglu, Basar, Demiralp, & Schürmann, 1992) involving primarily the hippocampus and associative frontal cortex (Miller, 1991; Basar-Eroglu et al., 1992; Demiralp & Basar, 1992; Klimesch, Schimke, & Schwaiger, 1994) and generating both the spontaneous and elicited theta oscillations (Basar, 1992).

    The spontaneous EEG theta activity has been found to decrease in absolute and relative band power with progressing age in children (Matoušek & Petersén, 1973; John, Ahn, Prichep, Trepetin, Brown, & Kaye, 1980; Matthis, Scheffner, Benninger, Lipinski, & Stolzis, 1980; Gasser, Verleger, Bächer, & Sroka, 1988; etc.). However, the information about theta response development is insufficient although the event-related theta activity may also vary with age in children. Firstly, the evoked potential magnitude is known to be significantly correlated with the power of the background EEG but in many instances EEG and ERP amplitudes have shown relatively independent behaviour (see e.g., Shagass, 1976). It is an open question whether a decrease in theta activity during stimulus processing accompanies the developmental reduction of the spontaneous EEG theta power. Secondly, increased theta activity in human adults has been consistently associated with higher cognitive processes like memory, concept learning, attention, etc. (Mizuki, Takii, Nishijima, & Inanaga, 1983; Lang, Lang, Diekmann, & Kornhuber, 1989; Basar-Eroglu et al., 1992; Inouye, Shinosaki, Iyama, Matsumoto, & Toi, 1994; Klimesch et al., 1994; Klimesch, Doppelmayr, Russeger, & Pachinger, 1996). Given these correlations, it is striking that although the spontaneous EEG theta power decreases with age in children and is relatively small in adults, the efficiency of cognitive functioning improves in the course of development (Piaget 1969). This implies that changes in theta system involvement during event processing as reflected by the theta response should occur with  brain development. Finally, theta responses of young (three-year-old) children were demonstrated to be larger, delayed, and more variable than those of adults (Basar, 1982; Basar-Eroglu, Kolev, Ritter, Aksu, & Basar, 1994; Kolev, Basar-Eroglu, Aksu, & Basar, 1994). Taken together, these findings suggest that the EEG theta response undergoes specific developmental variations but it is not known how and which response characteristics change as children mature. Therefore, the present study aimed to assess age-dependent alterations of EEG theta responses in 6-10-year-old children. Healthy young adults were also studied to evaluate the mature theta response.

    As mentioned above, the EEG frequency responses are proposed to originate from the reorganization of the spontaneous EEG. Therefore, theta response characteristics reflecting the stimulus-related changes in the ongoing EEG should be regarded as relevant for analysis. Such characteristics are the response phase-coupling to stimulus and amplitude enhancement or suppression in the post-stimulus epoch (Sayers, Beagley, & Riha, 1979; Kalcher & Pfurtscheller, 1995). In the averaged ERPs, however, amplitude and phase-locking effects are confounded and cannot be analyzed separately (see e.g., Ruchkin, 1988). To quantify theta response phase-locking independently of amplitude effects, an original method for single-sweep analysis was applied (Kolev & Daskalova, 1990; Yordanova & Kolev, 1996a; 1998; Kolev & Yordanova, 1997). Thus, the major questions addressed in this research were how single theta response amplitude, phase-locking, and enhancement relative to prestimulus activity vary with age in children and whether their developmental changes depend on the background EEG theta activity?

    Previous studies on adults have shown that event-related theta activity differs between processing conditions (Demiralp & Basar, 1992; Basar-Eroglu et al., 1992; Klimesch et al., 1994; Mecklinger, Kramer, & Strayer, 1992; Yordanova & Kolev, 1998). To examine whether the age-related variations in the theta response are restricted to a specific processing condition, passive and task auditory stimuli were used. Since the latency of the maximal theta response in the averaged ERPs has been shown to be longer in younger children (Basar-Eroglu et al., 1994; Yordanova & Kolev, 1996b), measurement and evaluation were made for early and late post-stimulus epochs to enable assessment of single theta response dynamics over time after stimulus appearance. The relationship between single theta response parameters and the ongoing (prestimulus) theta band power was also evaluated. Results of the alpha frequency range in the same groups of children are presented in a related paper (Yordanova & Kolev, 1996a).
 

    The auditory stimuli were generated by a PC, filtered, amplified, and reproduced by a loudspeaker in a free-sound field. All stimuli were presented with intensity of 60 dB SPL and  duration of 50 ms (r/f 10 ms). The stimuli were delivered with random inter-stimulus intervals (3.5-6.5 s) in two different task situations:

1) Tone bursts of 800 Hz frequency (N = 50) were presented in a passive listening condition, with subjects instructed to relax silently. Before the recording session, they were told that the stimuli would be delivered for testing the technical equipment and would be of no relevance for them.

2) Auditory target and nontarget stimuli were presented in an oddball task. During the task condition, 100 high and low frequency tones (1200 Hz and 800 Hz) were delivered randomly, with probability P = 0.75 for the high tones, and P = 0.25 for the low tones. Subjects were required to press a button with their dominant hand as quickly and accurately as possible in response to the low tones.

Data collection and processing
 
Electrodes
 
The EEG was recorded with Ag-AgCl disc electrodes placed on midline frontal, central and parietal sites (Fz, Cz, Pz), with linked mastoids as a reference. The ground electrode was positioned on the forehead. The electrooculogram (EOG) was recorded bipolarly with electrodes placed below and at the outer canthus of the left eye. Electrode impedance did not exceed 10 kOhms.
 
EEG recording and data storage
 
EEG was amplified with cut-off frequencies of 0.5 and 70 Hz by means of a Nihon Kohden Electroencephalograph (model EEG-4314F). Stop-band filtering (band limits 48-52 Hz) was used for eliminating line frequency interference. The amplified EEG analog signals were digitized with a sampling frequency of 250 Hz (12 bit analog-to-digital converter) and stored for off-line processing with epoch length of 1024 ms pre- and 1024 ms post-stimulus. Reaction times (RTs) were recorded automatically.
 
Artifact rejection
 
The stored raw single sweeps were inspected visually off-line to eliminate EEG segments contaminated with blink, muscular, or any other type of artifact activity, with any EEG or EOG trial exceeding ±50 µV for adults and ±90 µV for children excluded from further analysis. Thus, the number of artifact-free sweeps analyzed for each subject in each condition was between 40 and 50 for the passive and nontarget ERPs, and about 20-23 for the target ERPs.
 
 
Data analysis
 
Prestimulus EEG power spectral density
 
For each artefact-free single sweep, the power spectral density functions were calculated for the prestimulus epochs (-1000, 0 ms) using the Fast Fourier Transform (FFT), and then averaged separately for each stimulus type. For statistical evaluation, the mean absolute band power (X) in the range of 4-7 Hz, was log-transformed according to the formula Y = log₁₀(X) to normalize the power distributions (Gasser, Bächer, & Möcks, 1982; Gasser et al., 1988).
 
Digital filtering
 
Averaged and single-sweep ERPs were digitally band-pass filtered in the theta frequency range (4-7 Hz). To provide a zero phase shift, a modified linear band-pass filter was used, whose weights were based on binomial coefficients (Wastell, 1979). The filter band width was adjusted to be 5% from the total analyzed frequency band, which was experimentally proven to minimize filtering artifacts. Although in this study the main emphasis is placed on single-sweep parameters, averaged unfiltered and filtered (4-7 Hz) ERPs were also obtained to enable comparison with results from the single-sweep analysis and with literature data.
 
Single sweep analysis
 
Three parameters of the single-sweep theta responses were analyzed for two time windows, early (0-300 ms) and late (300-600 ms):  (1) maximal amplitude, (2) phase-locking, and (3) amplitude enhancement relative to prestimulus theta activity.

1) The maximal peak-to-peak amplitude of the single theta responses was measured in each of the two time windows. The mean value was calculated for each subject, stimulus type, and electrode location.

2) For a quantitative evaluation of the phase-locking, a modification of the single sweep wave identification (SSWI) method was applied (Kolev & Daskalova, 1990; Kolev & Yordanova, 1997). The steps of the analysis procedure are described below and are illustrated schematically in Figure 1.

Figure 1. Single Sweep Wave Identification (SSWI) method. The left panel presents (a) five single sweeps filtered in the theta range (4-7 Hz), and (b) their averaged waveform. The wave extrema in the single sweeps are detected according to the local maxima and minima, shown as vertical bars in (a). The same vertical bars (c) are located at the corresponding latency positions without the signals, and (d) the corresponding SSWI-histogram is build according to the rule:  in consecutive 20 ms time-lags +1 is added to the histogram bar if the detected extremum in the single sweep is maximum, or respectively -1, if the detected extremum is minimum. T1 - time window 0-300 ms, T2 - time  window 300-600 ms.

3) Single-sweep enhancement relative to prestimulus activity was analyzed by calculating the enhancement factor EF (Basar, 1982):  For each single sweep N, the ratio of the maximal response amplitude R_N to the root mean square value rms_N of the ongoing EEG amplitude prior the stimulus (in the time window -500,0 ms) was calculated  according to the formula:

Figure 2. Grand average passive, nontarget, and target ERPs at three electrode locations (Fz, Cz, and Pz) from different age groups:  6 year-olds, 7 year-olds, 8 year-olds, 9 year-olds, 10 year-olds, AD - adults. Each age group consists of 10 subjects. Stimulus presentation is at 0 ms.

Figure 3. Grand average passive, nontarget, and target ERPs at three electrode locations (Fz, Cz, and Pz) filtered in the theta (4-7 Hz) range. The age groups are designated as in Figure 2.

Figure 4. (a) Averaged ERPs filtered in the theta (4-7 Hz) range, (b) superimposed single sweeps filtered in the same (4-7 Hz) range, and (c) the corresponding SSWI histograms for six representative subjects at 6, 7, 8, 9, and 10 years of age, and an adult. Children had larger single theta responses than adults, especially in the late time window (300-600 ms). As reflected in the SSWI histograms, children also displayed a weaker phase-locking in both the early and late time windows than adults. All recordings are from the passive listening condition at Cz. Along the Y-axes — amplitude (µV) for (a) and (b), and number of synchronized single waves for (c).

* P < 0.05,  ** P < 0.01,  *** P < 0.001

Figure 5. Effects of Time window on theta responses to passive, target, and nontarget stimuli in six age groups:  (a) maximal peak-to-peak amplitude of the single theta responses, (b) number of the phase-locked single theta waves, and (c) enhancement factor. The age groups are designated as in Figure 2.

* P < 0.05,  ** P < 0.01,  *** P < 0.001

Figure 6. Effects of TIME WINDOW on theta responses to nontarget stimuli from each ELECTRODE and AGE group:  (a) number of phase-locked single theta waves, (b) enhancement factor. The age groups are designated in the same manner as in Figure 2.

 
Discussion
 
The present study assessed the event-related theta activity in children and adults at the level of single-sweep analysis. It was hypothesized that the EEG theta responses would differ between children and adults as well as among children groups, which can be evinced by differences in single-sweep parameters. This hypothesis was confirmed and significant age-related variations were found for single theta response amplitude, phase-locking, and enhancement relative to prestimulus activity. Furthermore, these variations were specific for each parameter.  A major finding was that whereas single-sweep amplitudes decreased, the phase-locking increased with age. As described in the results, the averaged filtered ERPs did not manifest significant differences between children and adults. It was because the smaller single-sweep amplitudes of adults were accompanied by a pronounced phase-locking, and the opposite was true for children. Thus, since additional information was obtained that was obscured in the averaged waveforms, the developmental changes in the EEG theta response could be revealed and evaluated precisely at the level of single-sweep analysis.
 
 
Single-sweep theta responses in adults
 
In adults, the theta component of averaged auditory ERPs has been described previously (Demiralp & Basar, 1992; Basar-Eroglu et al., 1992). In the present study, by using single-sweep analysis the following new characteristics of the event-related theta activity were found:  (1) Auditory theta responses display strong phase-locking and amplitude enhancement in the post-stimulus epoch, which verifies the stimulus-related reorganization of the ongoing theta activity in adults;  (2) The early theta responses (0-300 ms) are higher in magnitude and enhancement, and stronger in phase-locking than the late ones (300-600 ms), with the differences between early and late components being most pronounced at the mid-central location. These observations were true for passive, target, and nontarget ERPs, which shows that the early and late theta responses may reflect mechanisms activated during both passive and task stimulus processing. Previous reports on adults have found that enhanced (synchronized) event-related theta activity accompanies short-term memory activation (Mecklinger et al., 1992; Klimesch et al., 1994) and increased focused attention (Basar-Eroglu et al., 1992). These memory- and attention-related effects were observed for the post-stimulus epochs later than 250-300 ms. In addition, the late (300-600 ms) fronto-parietal theta responses to target oddball tones have been reported to be more enhanced and more strongly phase-locked than the late responses to passive stimuli, whereas the early theta components did not differ between target and passive stimulus processing (Yordanova & Kolev, 1998). Stimulus type effect was not tested in the present study because only the developmental changes in theta activity were focused on. However, the reports mentioned above suggest that the early and late responses of adults as observed here may relate to different processing mechanisms.
 
 
Differences in theta responses of children and adults
 
The organization of the auditory theta response was specific for children. This was evidenced by the significant differences between the single-sweep parameters of 6-10-year-old children and adults:  (1) Single theta responses of children were larger but not enhanced against prestimulus theta activity, and also less synchronized than those of adults;  (2) In adults, the early theta oscillations expressed higher responsiveness than the late ones, whereas in children the late responses were either more enhanced than the early ones or no reliable differences were observed between the early and late theta activity. It is noteworthy that the age-related variations were similar for the three stimulus types. These findings generally indicate that during auditory stimulus processing the theta response system in adults operates in a manner different from that in 6-10-year-old children. Since the passive and task-related stimuli produced similar age-related differences, it may be further suggested that the specific organization of the theta response in children reflects developmental variations of basic stimulus-processing mechanisms common for the different processing conditions. Such a proposal is supported by the observation that single theta response parameters do not correlate with response speed.
 
 
Theta response system development
 
Single theta responses in children not only differed from those in adults, but also changed with advancing age from 6 to 10 years:  A decrease in single-response amplitudes occurred at 10 years for the task stimuli and at 7 and 9 years for the passive stimuli, with the values of the mature theta response not achieved even by eldest (ten-year-old) children. The developmental alterations in amplitude are not likely to result from differences in cranial parameters such as thickness of the scalp or head circumference (Polich, Ladish, & Burns, 1990; Gasser et al., 1988) - a conclusion supported also by the different time courses of single theta amplitudes for the passive and task stimuli. As revealed by the multiple regression analysis results, these age-related amplitude effects resulted exclusively from the developmental decrease in the power of the ongoing EEG theta activity. Furthermore, the early theta responses displayed a maximum at Cz as did the prestimulus theta power. The observation of the strong relationship between the pre- and post-stimulus theta amplitudes may be regarded as supporting the concept of the diffuse and distributed theta system in the brain generating both the spontaneous and stimulus-related 4-7 Hz activity (Basar, 1992). Hence, the developmental reduction of EEG theta activity may indicate a decrease in the number and/or intensity of the neuronal elements that determine operative theta states of the brain.
 
    The present results demonstrate, however, that single theta responses of children are large but do not change relative to the prestimulus theta activity after stimulation. Also, the ability to enhance the magnitude of the evoked theta component does not improve from 6 to 10 years was not confirmed.
 
    In parallel to the decrease in amplitude, an increase in the  phase-locking of early theta responses took place at about 9 years of age. However, for all three types of ERPs adults had remarkably stronger phase-locking than any of the children groups. Hence, it may be concluded that the capability to produce stable (congruent) theta responses to auditory stimulation improves with development but appears related to brain mechanisms that reach maturation at developmental stages later than 10 years.
 
    The phase-locking in children did not depend on the power of the prestimulus EEG theta activity. Instead, subject age was the determinant of the developmental increase in phase-synchronization. This result demonstrates that theta response phase-locking reflects processes specifically activated after stimulus presentation. It is to be noted that the developmental increase in phase-locking was found only for the early theta responses and at the central site where the early theta responses of adults were mostly expressed (Figure 6a). Although the phase-locking of late responses was also significantly stronger in adults than in children, no increase of late theta response phase-locking was observed for children groups. These differential time courses support the assumption that the early and late responses may have different functional roles.
 
    In addition, major developmental differences were revealed for the time structure of all single-sweep parameters:  Adults manifested pronounced differences between the early and late theta responses, but in children younger than 9-10 years the magnitude and phase-locking of the early theta responses were similar to those of the late ones. Furthermore, younger (6-7-year-old) children had a greater enhancement for the late compared to the early theta responses (Figure 5c) and all children groups tended to enhance the frontal late theta responses more than the early ones (Figure 5b). Given the previous results of adults outlined above, it cannot be ruled out that the relation between early and late theta responses varies as a function of the specific task conditions. Whether the reverse pattern in children reflects a response delay, a different way of involvement of processes functionally specific to the early and late responses in adults, or a qualitatively different mode of organization of the event-related theta activity, is an open question. The precise functional significance of the event-related theta activity in both adults and children requires further investigation, especially with respect to the meaning of single-sweep parameters. Nevertheless, the present findings suggest that single theta response parameters and their timing may provide a sensitive indicator of stimulus- and task-related information processing in children.
 
    Altogether, the single-sweep analysis results demonstrate that the theta response system is not completely developed at the age of 10 years. At which age the adult values of single theta response parameters are reached is not clear from the results but the processes related to theta response system functioning obviously reach maturation at later stages of development. It is to be emphasized that at the age of 10 years the frontal lobes, unlike other brain structures, are reported not to have reached functional maturity with respect to their anatomical structure and input-output connections (Rothenberger, 1990). Miller (1991) has raised the hypothesis that the EEG theta rhythm reflects the fronto-hippocampal interplay during context processing. The present findings of the incomplete development of theta responses at 10 years of age as well as of the delayed enhancement of frontal theta responses in children support the notion about the association between the theta response and frontal lobe processes. In this regard, since frontal lobe functioning has been assigned a major role for the occurrence and course of psychiatric disorders in children (Rothenberger, 1990), event-related theta activity may appear informative as a supplementary tool for such clinical studies (e.g., Rothenberger, 1995; Yordanova, Dumais-Huber, Rothenberger, & Woerner, 1997). It is also to be noted that the developmental changes of single-sweep parameters, although occurring at different ages, were rather step-wise than gradual, which points to their possible relation with stages of cognitive development (Piaget, 1969) but the precise correlations of single theta response parameters with cognitive stage is still to be investigated.
 
 
Theoretical implications
 
The developmental time courses were different for theta response amplitude, phase-locking, and enhancement. These differential developmental courses might reflect sequential effects in the maturation of a common underlying mechanism. Alternatively, they may point to that specific mechanisms might be involved in the maturation of the processes related to each of the three single-sweep parameters.
 
    The strong phase-locking of theta responses in adults shows that repeatable and stable waveforms are produced after stimulation. In the framework of the concept of the theta system in the brain (Basar, 1992), the strong phase-locking is likely to result from stable (facilitated or traced) connections between neuronal elements. Hence, it can be assumed that the theta networks involved in responding during the early stage (0-300 ms) of stimulus information processing are stabilized or traced with development in children so that repeatable patterns can be produced at the central but not at the frontal and parietal locations. The increase in repeatability of the early theta responses is accompanied by a decrease in magnitude, which might reflect a developmental specialization of the theta networks based on involving less but functionally defined elements (Courchesne 1990). The large enhancement factors in adults suggest that the neuronal elements responding in the theta channel can be coactivated (synchronized) simultaneously by the external stimulus (Klimesch et al., 1994) but no developmental changes were observed for the enhancement of the theta responses. With regard to the three single-sweep parameters analyzed here, it might be assumed that the theta response system changes with development in a way that enables less but functionally specified elements to be coactivated simultaneously under defined conditions. Reduction of active elements, selection of networks, and capability of synchronizing them upon stimulation seem to follow differential time courses.
 

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