Eino Partanen

Learning-induced neural plasticity of speech processing before birth

Significance Learning, the foundation of adaptive and intelligent behavior, is based on changes in neural assemblies and reflected by the modulation of electric brain responses. In infancy, long-term memory traces are formed by auditory learning, improving discrimination skills, in particular those relevant for speech perception and understanding. Here we show direct neural evidence that neural memory traces are formed by auditory learning prior to birth. Our findings indicate that prenatal experiences have a remarkable influence on the brain’s auditory discrimination accuracy, which may support, for example, language acquisition during infancy. Consequently, our results also imply that it might be possible to support early auditory development and potentially compensate for difficulties of genetic nature, such as language impairment or dyslexia. Learning, the foundation of adaptive and intelligent behavior, is based on plastic changes in neural assemblies, reflected by the modulation of electric brain responses. In infancy, auditory learning implicates the formation and strengthening of neural long-term memory traces, improving discrimination skills, in particular those forming the prerequisites for speech perception and understanding. Although previous behavioral observations show that newborns react differentially to unfamiliar sounds vs. familiar sound material that they were exposed to as fetuses, the neural basis of fetal learning has not thus far been investigated. Here we demonstrate direct neural correlates of human fetal learning of speech-like auditory stimuli. We presented variants of words to fetuses; unlike infants with no exposure to these stimuli, the exposed fetuses showed enhanced brain activity (mismatch responses) in response to pitch changes for the trained variants after birth. Furthermore, a significant correlation existed between the amount of prenatal exposure and brain activity, with greater activity being associated with a higher amount of prenatal speech exposure. Moreover, the learning effect was generalized to other types of similar speech sounds not included in the training material. Consequently, our results indicate neural commitment specifically tuned to the speech features heard before birth and their memory representations.

Auditory event-related potentials and cognitive function of preterm children at five years of age

OBJECTIVE In our previous study, auditory event-related potentials (AERPs) in preterm 1-year-old children had a positive deflection at 150-350 ms that correlated positively with their 2-year neurodevelopmental outcome. In a study of the same subjects at age 5, our aim was to assess AERPs and their relationship to neuropsychological test results. METHODS Preterm small (SGA, n=13), appropriate for gestational age (AGA, n=15), and control (n=13) children were assessed with an Easy paradigm presenting a large frequency change accompanied with occasional novel sounds, and a Challenging paradigm presenting small frequency and duration changes with a rapid rate. The preterm children underwent neurocognitive tests. RESULTS Easy paradigm. The P1 response to frequency deviant was smaller and MMN larger in the preterm than in the control children. Challenging paradigm. The P1 response to standard, frequency, and duration deviants was smaller in the preterm than in the control children. The N2 response to frequency deviant was larger in the preterm than in the control children. AGA and SGA children had similar AERPs. The P1, N2, and MMN amplitudes correlated with verbal IQ and NEPSY language subtests. CONCLUSIONS Small P1 response(s) appears to be typical for preterm children. SIGNIFICANCE Small P1 response in preterm children may suggest altered primary auditory processing.

Linguistic multifeature MMN paradigm for extensive recording of auditory discrimination profiles.

We studied whether a multifeature mismatch negativity (MMN) paradigm using naturally produced speech stimuli is feasible for studies of auditory discrimination accuracy of adult participants. A naturally produced trisyllabic pseudoword was used in the paradigm, and MMNs were recorded to changes that were acoustic (changes in fundamental frequency or intensity) or potentially phonological (changes in vowel identity or vowel duration). All the different changes were presented in three different word segments (initial, middle, or final syllable). All changes elicited an MMN response, but the vowel duration change elicited a different response pattern than the other deviant types. Changes in vowel duration and identity also had an effect on MMN lateralization. Our results show that assessing speech sound discrimination of several features in word context is possible in a short recording time (30 min) with the multifeature paradigm.

The neural basis of sublexical speech and corresponding nonspeech processing: a combined EEG-MEG study.

We addressed the neural organization of speech versus nonspeech sound processing by investigating preattentive cortical auditory processing of changes in five features of a consonant-vowel syllable (consonant, vowel, sound duration, frequency, and intensity) and their acoustically matched nonspeech counterparts in a simultaneous EEG-MEG recording of mismatch negativity (MMN/MMNm). Overall, speech-sound processing was enhanced compared to nonspeech sound processing. This effect was strongest for changes which affect word meaning (consonant, vowel, and vowel duration) in the left and for the vowel identity change in the right hemisphere also. Furthermore, in the right hemisphere, speech-sound frequency and intensity changes were processed faster than their nonspeech counterparts, and there was a trend for speech-enhancement in frequency processing. In summary, the results support the proposed existence of long-term memory traces for speech sounds in the auditory cortices, and indicate at least partly distinct neural substrates for speech and nonspeech sound processing.

Musicianship facilitates the processing of Western music chords—An ERP and behavioral study

The present study addressed the effects of musicianship on neural and behavioral discrimination of Western music chords. In abstract oddball paradigms, minor chords and inverted major chords were presented in the context of major chords to musician and non-musician participants in a passive listening task (with EEG recordings) and in an active discrimination task. Both sinusoidal sounds and harmonically rich piano sounds were used. Musicians outperformed non-musicians in the discrimination task. Change-related mismatch negativity (MMN) was evoked to minor and inverted major chords in musicians only, and N1 amplitude was larger in musicians than non-musicians. While MMN was absent in non-musicians, both groups showed decreased N1 in response to minor compared to major chords. The results indicate that processing of complex musical stimuli is enhanced in musicians both behaviorally and neurally, but that major-minor chord categorization is present to some extent also in the absence of music training.

Auditory event-related potentials at preschool age in children born very preterm

OBJECTIVE To assess auditory event-related potentials at preschool age in children born very preterm (VP, 27.4 ± 1.9 gestational weeks, n=70) with a high risk of cognitive dysfunction. METHODS We used an oddball paradigm consisting of a standard tone randomly replaced by one of three infrequent deviants (differing in frequency, sound direction or duration). RESULTS The P1 and N2 latencies were inversely correlated to age (50-63 months) both in VP (r=-0.451, p<0.001, and r=-0.305, p=0.01, respectively) and term born controls (TC; n=15). VP children had smaller P1 than near-term (n=12) or TC (1.70 ± 0.17 μV vs 2.68 ± 0.41 and 2.92 ± 0.43, respectively; p<0.05). Mismatch negativity response did not differ between groups. CONCLUSIONS Our data suggest a fast maturation of P1 and N2 responses with fast decrease in P1 and N2 latencies around the age of 5 years. Mismatch negativity response does not seem to be a robust measure for defining abnormalities in VP children. SIGNIFICANCE In ERP studies in preschool children, even small, non-significant group differences in age at recording should be corrected for. Very preterm born children at preschool age have aERP patterns as earlier described in full-term born children with cognitive deficits.

Auditory event-related potentials are related to cognition at preschool age after very preterm birth

Background:Auditory event-related potentials (AERP) are neurophysiological correlates of sound perception and cognitive processes. Our aim was to study in very preterm born children at preschool age if AERP correlate with cognitive outcome.Methods:Seventy children (mean ± SD gestational age 27.4 ± 1.9 wk, birth weight 996 ± 288 g) were investigated at age 4.3–5.3 y with psychological testing (WPPSI-R, four subtests of NEPSY). Electroencephalogram was recorded while they listened to a repeated standard tone, randomly replaced by one of three deviants. Latencies and amplitudes for AERP components and mean amplitudes in successive 50-ms AERP time windows were measured.Results:Better cognitive test results and higher gestational age correlated with shorter P1 latencies and more positive mean amplitudes 150–500 ms after stimulus change onset. Neonatal brain damage was associated with a negative displacement of AERP curves. Neonatal morbidity had an impact on earlier time windows while gestational age and brain damage on both early and later time windows.Conclusion:AERP measures were associated with cognitive outcome. Neonatal morbidity mainly affects early cortical auditory encoding, while immaturity and brain damage additionally influence higher cortical functions of auditory perception and distraction. Perinatal auditory environment might play a role in development of auditory processing.

Formation of neocortical memory circuits for unattended written word forms: neuromagnetic evidence

To master linguistic communication, humans must acquire large vocabularies quickly and effortlessly. Efficient word learning might be facilitated by the ability to rapidly acquire novel word forms even outside the focus of attention, occurring within minutes of repetitive exposure and suggesting fast and automatic lexicon acquisition. However, this phenomenon has been studied in the auditory modality only, and it is unknown whether similar mechanisms also exist in the visual domain. We tested this by presenting participants with novel written word forms while the focus of their attention was on a non-linguistic dual colour-detection task. Matched familiar word forms served as a control. Using magnetoencephalography (MEG), we scrutinised changes in neuromagnetic responses to familiar and to novel word forms over approximately 15 minutes of exposure. We found, for the first time, a visual analogue of automatic rapid build-up of neural memory circuits for unattended novel lexical items, seen as a rapid enhancement of early (~100 ms post-onset) activation in the left anterior-superior temporal lobe. Our results suggest that the brain quickly forms cortical representations for new written forms, and indicate that the automatic neural mechanisms subserving rapid online acquisition of novel linguistic information might be shared by both auditory and visual modalities.

Impaired neural mechanism for online novel word acquisition in dyslexic children

Developmental dyslexia is characterised as an inability to read fluently. Apart from literacy problems, dyslexics have other language difficulties including inefficient speech encoding and deficient novel word learning. Yet, the neural mechanisms underlying these impairments are largely unknown. We tracked online formation of neural memory traces for a novel spoken word-form in dyslexic and normal-reading children by recording the brain’s electrophysiological response dynamics in a passive perceptual exposure session. Crucially, no meaning was assigned to the new word-form nor was there any task related to the stimulus, enabling us to explore the memory-trace formation of a purely phonological form in the absence of any short-term or working memory demands. Similar to previously established neural index of rapid word learning in adults, the control children demonstrated an early brain response enhancement within minutes of exposure to the novel word-form that originated in frontal cortices. Dyslexic children, however, lacked this neural enhancement over the entire course of exposure. Furthermore, the magnitude of the rapid neural enhancement for the novel word-form was positively associated with reading and writing fluency. This suggests that the rapid neural learning mechanism for online acquisition of novel speech material is associated with reading skills. Furthermore, the deficient online learning of novel words in dyslexia, consistent with poor rapid adaptation to familiar stimuli, may underlie the difficulty of learning to read.

Neural discrimination of speech sound changes in a variable context occurs irrespective of attention and explicit awareness

To process complex stimuli like language, our auditory system must tolerate large acoustic variance, like speaker variability, and still be sensitive enough to discriminate between phonemes and to detect complex sound relationships in, e.g., prosodic cues. Our study determined discrimination of speech sounds in input mimicking natural speech variability, and detection of deviations in regular pitch relationships (rule violations) between speech sounds. We investigated the automaticity and the influence of attention and explicit awareness on these changes by recording the neurophysiological mismatch negativity (MMN) and P3a as well as task performance from 21 adults. The results showed neural discrimination of phonemes and rule violations as indicated by MMN and P3a, regardless of whether the sounds were attended or not, even when participants could not explicitly describe the rule. While small sample size precluded statistical analysis of some outcomes, we still found preliminary associations between the MMN amplitudes, task performance, and emerging explicit awareness of the rule. Our results highlight the automaticity of processing complex aspects of speech as a basis for the emerging conscious perception and explicit awareness of speech properties. While MMN operates at the implicit processing level, P3a appears to work at the borderline of implicit and explicit.