Elsevier

Neuroscience Research

Volume 54, Issue 4, April 2006, Pages 276-280
Neuroscience Research

The right hemisphere of sleeping infant perceives sentential prosody

https://doi.org/10.1016/j.neures.2005.12.006Get rights and content

Abstract

Behavioral studies proposed that prosodic information in speech sounds plays important roles for human infants to acquire their native languages. Here, we examined the neural basis of prosodic processing in 3-month-old infants. In order to obtain hemodynamic responses with high signal-to-noise ratio, we used near-infrared optical topography in the infants while they were in quiet sleep. First, we observed bilateral activation under each of the normal and flattened speech conditions. The flattened speech sound was created by eliminating changes in the pitch contours of the original utterance. In a direct comparison between the two conditions, the right temporoparietal region showed more prominent activation to normal speech sounds than to flattened speech sounds. This result demonstrates that the localized region of the right hemisphere in 3-month-old infant is involved in the processing of pitch contours. Our findings suggest that prosodic processing in the right hemisphere may facilitate the acquisition of lexical or syntactic knowledge in the early stages of language development.

Introduction

Language acquisition is one of the unique features of human nature. Human infants begin to process language inputs prior to the onset of speech production (Jusczyk, 1997, Werker and Tees, 1999, Kuhl, 2004). Among various types of information related to language inputs, sentential prosody is considered to be essential for neonates and infants to acquire their native languages (Fernald and Kuhl, 1987, Mehler et al., 1988, Mandel et al., 1994). The attributes of speech prosody are mainly served by three acoustic parameters of pitch (fundamental frequency), duration and amplitude. The information from these acoustic parameters provides cues to find phrase boundaries and helps listeners decode syntactic structures of sentences (Cutler et al., 1997). Taking into consideration the close correspondence between prosodic and syntactic properties, Gleitman and Wanner formulated the prosodic bootstrapping hypothesis, wherein infants could use prosodic information to acquire valuable knowledge about the syntactic organization of their native language (Gleitman and Wanner, 1982). This hypothesis has been supported and developed in recent behavioral studies on prosodic processing in infants (Morgan and Demuth, 1996, Jusczyk, 1997).

A critical question here is which cortical region is related to prosodic processing in infants. Lateralization and localization in the infant brain for processing sentential prosody has never been demonstrated; this is partly because measurement tools that have been applied to infants (e.g., electroencephalogram (EEG) and magnetoencephalogram (MEG)) (Cheour et al., 2000, Kujala et al., 2004) are less apt at revealing localization and detecting cortical responses to stimuli lasting several seconds. With regard to lateralization in adult, there appear to be a number of positions in previous clinical and neuroimaging studies (Baum and Pell, 1999). One major hypothesis is that the right hemisphere is related to emotional or paralinguistic prosody. Recent studies have confirmed the involvement of the right hemisphere in at least some aspects of pitch processing (Zatorre et al., 1992, Johnsrude et al., 2000, Meyer et al., 2004). The prosodic processing in the right hemisphere is supposed to interact with syntactic processing at the phrasal or sentential level (Baum and Dwivedi, 2003, Herrmann et al., 2003). In contrast, the involvement of the left hemisphere in the processing of linguistic prosody including lexical tones is still under debate (Wong, 2002). The left-lateralized activation was reported when adult subjects were required both prosodic and linguistic processing, suggesting that activation in the left hemisphere is task dependent (Gandour et al., 2004). Based on previous findings on prosodic processing, we expect that several-month-old infants have some neural mechanisms for processing sentential prosody. If the right hemisphere of infants is related to prosodic processing, we can consider that the neural mechanisms affect cortical regions involved in other aspects of language processing as shown in adults.

In the present study, we used a near-infrared optical topography (OT) (Maki et al., 1995), which is an effective method to examine the cortical hemodynamic responses in infants to stimuli lasting several seconds (Taga et al., 2003). Here, we investigated the cortical activation of 3-month-old infants; behavioral studies have reported that at least 2- or 4-month-old infants are sensitive to sentential prosody (Fernald and Kuhl, 1987, Mandel et al., 1994). The infants were studied while they were in quiet sleep. In recent studies, neural responses of sleeping infants have been reported by using auditory mismatch negativity (MMN) (Cheour et al., 2000). Adult subjects were also examined by using functional magnetic resonance imaging (fMRI), and the activation pattern for speech sounds in the bilateral temporal regions was similar in wakefulness and sleep (Portas et al., 2000). Thus, we considered that the OT recordings during quiet sleep can detect cortical responses to auditory stimuli, and further that the OT recordings under the sleeping state provide long time and motion-free data with high signal-to-noise ratio. In the present study, we focused on the variation in the levels of oxyhemoglobin ([oxy-Hb]) in the OT data, and identified the cortical regions that were responsive to each of the normal and flattened speech conditions (Fig. 1A; see Section 2) by performing t-tests for each measurement channel. We further performed direct comparisons between the two conditions to identify the cortical regions that are related to the processing of pitch contours in sentences.

Section snippets

Subjects

Twenty-one full-term healthy Japanese infants participated in the present study (girls: 12, boys: 9; mean age: 107.6 days; range: 92–118 days). An additional 10 infants were studied, but excluded from the analysis due to their awakening during the experiment (n = 5), head movements producing large motion artifacts in the signals (n = 3) and experimental error (n = 2). Informed consent was obtained from the parents of the infants prior to the initiation of the experiments. The study was approved by

Results

In order to quantify event-related hemodynamic responses to speech sounds, we first determined an averaged time course among all the measurement channels under the two conditions and calculated the time to peak and latency in the time course. The maximum increase was attained at 5.9 s with the signal change of 0.0293 mM·mm (Fig. 1C). This response returned to the baseline at approximately 13 s. We compared this averaged time course with a canonical hemodynamic response function of adults (Friston

Discussion

In the present study, we elucidated that the right temporoparietal region in 3-month-old infants was sensitive to normal speech, which includes pitch information. The right-lateralized activation demonstrates that sleeping 3-month-old infants do not merely receive speech sounds at the primary sensory level, but also proceed to analyze acoustic parameters in utterances. We used a single set of sentences in both the conditions; therefore, phonological information, lexico-semantics and syntactic

Acknowledgments

We would like to thank M. Fujiwara and T. Ishizuka for developing probes of OT for measurement in infants, and N. Okabe and R. Momoi for their administrative assistance.

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