Neonatal frequency discrimination in 250–4000-Hz range: Electrophysiological evidence
Introduction
The ability to tell apart sounds of different frequency is one of the important basic properties of the central auditory system. Both music and speech perception rely upon frequency discrimination. From the clinical perspective, the identification of abnormalities in frequency discrimination abilities may improve, for instance, the diagnostics of dyslexia (Baldeweg et al., 1999). Yet, the developmental course of the frequency-discrimination ability is poorly understood.
Behavioural studies in adult humans have shown that the ratio between the minimum distinguishable frequency interval (difference limen, DL) and the frequency is smallest in the 500–2000 Hz frequency range, becoming larger at higher and lower frequencies (Wier et al., 1977, Sek and Moore, 1995). As determined by otoacoustic emission studies (Abdala and Sininger, 1996), cochlear frequency resolution is fully mature by term birth; behavioural studies report sound-frequency discrimination in infants as young as 3 months (Werner and Gray, 1998). Early attempts (Leventhal and Lipsitt, 1964, Trehub, 1973) to find evidence for tonal frequency discrimination in newborns by using behavioural methods have failed. However, the sucking rate measurement and other methods indicate that newborns can discriminate the differences in the fundamental frequency of the human voice (DeCasper and Fifer, 1980, Mehler et al., 1988; for review, see Gerken and Aslin, 2005). At 3 months, DLs are smaller for low than for high-frequency tones (Olsho et al., 1987a), but the frequency discrimination at high frequencies develops faster, reaching the adult level by 6 months, whereas low-frequency DLs remain immature until the late childhood (Maxon and Hochberg, 1982).
However, the behavioural data obtained in infants younger than 5 months may provide incomplete and unreliable information about their frequency discrimination (Stapells and Kurtzberg, 1991). First, behavioural responses, such as head turning, often leave space for subjective interpretation (even though this could be overcome by introducing an additional observer, unaware of the paradigm, reporting any change in the infant’s behavior; Olsho et al., 1987b). Second, a failure in behavioural discrimination may be due either to genuine perceptual immaturity or to not fully developed attentional and memory mechanisms. This stresses the importance of the electrophysiological measures of frequency discrimination, which are independent of attention and enable direct measurement of auditory discriminative abilities (Kurtzberg and Vaughan, 1985, Stapells and Kurtzberg, 1991).
In adults, frequency discrimination can be assessed objectively by recording the mismatch negativity (MMN; Näätänen et al., 1978, Hari et al., 1984, Sams et al., 1985). The MMN correlates with the behavioural performance (Tervaniemi et al., 1993, Tiitinen et al., 1994, Amenedo and Escera, 2000, Novitski et al., 2004). It does not require the subject’s attention or task performance and can therefore be used in subject groups that are not able to cooperate with the experimenter. The MMN-like response to frequency change was found in newborns (Alho et al., 1990) and its magnetoencephalographic (MEG) analog (Hari et al., 1984) was recently discovered even in fetuses (Draganova et al., 2005, Huotilainen et al., 2005).
Unlike in adults, in young infants the mismatch response was found to be in different studies of either negative (Alho et al., 1990, Cheour et al., 1998, Ceponiene et al., 2002) or positive polarity (Dehaene-Lambertz and Dehaene, 1994, Leppänen et al., 1997, Morr et al., 2002, Sambeth et al., 2006). In addition, in one study (Ceponiene et al., 2002) the negativity was present only in part of the subject group. The differences between individual newborns can be explained by different degrees of maturation: Leppänen et al. (2004) showed that less mature infants showed a tendency towards negativity and more mature ones towards positivity. The infant’s arousal state can also have an impact: 2-month-old infants showed negative responses when awake and positive responses when asleep (Friederici et al., 2002). Moreover, the inter-stimulus interval may also have some effect on polarity as the negative response was elicited with an 800-ms stimulus onset asynchrony (SOA) but not with a 450 or 1500-ms SOA (Cheour et al., 2002). Finally, the higher cutoff of high-pass filtering selectively reduced positive responses due to the longer duration of the positive response (Trainor et al., 2003, Weber et al., 2004). Despite the discrepancies in the polarity of the response, it is clear that the auditory discriminative abilities of newborns can be measured with ERP recordings. This is true not only for the physical features of a stimulus but also for the abstract rules governing an auditory stimulus stream (Ruusuvirta et al., 2003, Ruusuvirta et al., 2004, Winkler et al., 2003, Carral et al., 2005).
In the majority of the afore-mentioned studies, the frequency difference between the standard and the deviant was large: the minimum was 10%, while the most often used difference was 20%. Also, in tonal studies, the frequency range of 1000–2000 Hz has usually been applied whereas the discriminative response in other frequency ranges has not been investigated. In adults, a 5% frequency difference elicits a significant MMN in the frequency range from 250 to 4000 Hz (Novitski et al., 2004). The present study used the MMN paradigm to estimate automatic frequency discrimination in the 250–4000-Hz range.
Section snippets
Subjects and the experimental environment
Initially, 19 full-term newborn infants (mean age 2 days, mean gestational age at birth 41.2 ± 0.4 weeks, activity-pulse-grimace-appearance-respiration (APGAR) scores between 8 and 10) participated in the study. Their sleep stage during the recordings was determined in each experimental block by a qualified specialist on the basis of the EEG and behavioural patterns. Thereafter, the percentage of each of the three sleeping stages in the experiment was calculated as
Waveform description
The individual deviant-standard difference waves for 11 subjects in the 1000-Hz-standard condition are shown in Fig. 1. There was substantial individual variation in the shape of the waveform which had both negative and positive deflections. The grand-averaged ERPs of standards and deviants, the grand-average difference waves, and the voltage maps of the grand-average ERPs and difference waves at 288 ms in the 1000-Hz-standard condition are presented in Fig. 2. The most prominent deflection at
Discussion
The present results demonstrate that the electrophysiological response of healthy newborns to sound frequency changes is manifested as a positive deflection in the event-related potential in the 200–300-ms window after stimulus onset. Based on its automatic elicitation during sleep, the mismatch response (MMR) can be regarded as the newborn equivalent of the mismatch negativity (MMN).
This response was obtained for the 20% change in frequency around 250, 1000, and 4000 Hz. There was no conclusive
Acknowledgements
We thank Tarja Ilkka, RN for recording the data. We also thank Dr. Istvan Winkler, Dr. Elina Pihko, and Dr. Anke Sambeth for their helpful comments during the discussion of preliminary results of the present project and Dr. Ilkka Linnankoski for language editing. This research was supported by the Academy of Finland (projects 200522, 77322, and 73038).
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