Tonotopic representation of missing fundamental complex sounds in the human auditory cortex

The N1m component of the auditory evoked magnetic field in response to tones and complex sounds was examined in order to clarify whether the tonotopic representation in the human secondary auditory cortex is based on perceived pitch or the physical frequency spectrum of the sound. The investigated stimulus parameters were the fundamental frequencies (F0 = 250, 500 and 1000 Hz), the spectral composition of the higher harmonics of the missing fundamental sounds (2nd to 5th, 6th to 9th and 10th to 13th harmonic) and the frequencies of pure tones corresponding to F0 and to the lowest component of each complex sound. Tonotopic gradients showed that high frequencies were more medially located than low frequencies for the pure tones and for the centre frequency of the complex tones. Furthermore, in the superior-inferior direction, the tonotopic gradients were different between pure tones and complex sounds. The results were interpreted as reflecting different processing in the auditory cortex for pure tones and complex sounds. This hypothesis was supported by the result of evoked responses to complex sounds having longer latencies. A more pronounced tonotopic representation in the right hemisphere gave evidence for right hemispheric dominance in spectral processing.     

Auditory processing abnormalities in schizotypal personality disorder: an fMRI experiment using tones of deviant pitch and duration

BACKGROUND: One of the cardinal features of schizotypal personality disorder (SPD) is language abnormalities. The focus of this study was to determine whether or not there are also processing abnormalities of pure tones differing in pitch and duration in SPD. METHODS: Thirteen neuroleptic-na?ve male subjects met full criteria for SPD and were group-matched on age and parental socio-economic status to 13 comparison subjects. Verbal learning was measured with the California Verbal Learning Test. Heschl's gyrus volumes were measured using structural MRI. Whole-brain fMRI activation patterns in an auditory task of listening to tones including pitch and duration deviants were compared between SPD and control subjects. In a second and separate ROI analysis we found that peak activation in superior temporal gyrus (STG), Brodmann Areas 41 and 42, was correlated with verbal learning and clinical measures derived from the SCID-II interview. RESULTS: In the region of the STG, SPD subjects demonstrated more activation to pitch deviants bilaterally (p<0.001); and to duration deviants in the left hemisphere (p=0.005) (two-sample t). SPD subjects also showed more bilateral parietal cortex activation to duration deviants. In no region did comparison subjects activate more than SPD subjects in either experiment. Exploratory correlations for SPD subjects suggest a relationship between peak activation on the right for deviant tones in the pitch experiment with odd speech and impaired verbal learning. There was no difference between groups on Heschl's gyrus volume. CONCLUSIONS: These data suggest that SPD subjects have inefficient or hyper-responsive processing of pure tones both in terms of pitch and duration deviance that is not attributable to smaller Heschl's gyrus volumes. Finally, these auditory processing abnormalities may have significance for the odd speech heard in some SPD subjects and downstream language and verbal learning deficits.     

Enhanced pure-tone pitch discrimination among persons with autism but not Asperger syndrome

Persons with Autism spectrum disorders (ASD) display atypical perceptual processing in visual and auditory tasks. In vision, Bertone, Mottron, Jelenic, and Faubert (2005) found that enhanced and diminished visual processing is linked to the level of neural complexity required to process stimuli, as proposed in the neural complexity hypothesis. Based on these findings, Samson, Mottron, Jemel, Belin, and Ciocca (2006) proposed to extend the neural complexity hypothesis to the auditory modality. They hypothesized that persons with ASD should display enhanced performance for simple tones that are processed in primary auditory cortical regions, but diminished performance for complex tones that require additional processing in associative auditory regions, in comparison to typically developing individuals. To assess this hypothesis, we designed four auditory discrimination experiments targeting pitch, non-vocal and vocal timbre, and loudness. Stimuli consisted of spectro-temporally simple and complex tones. The participants were adolescents and young adults with autism, Asperger syndrome, and typical developmental histories, all with IQs in the normal range. Consistent with the neural complexity hypothesis and enhanced perceptual functioning model of ASD (Mottron, Dawson, Soulières, Hubert, & Burack, 2006), the participants with autism, but not with Asperger syndrome, displayed enhanced pitch discrimination for simple tones. However, no discrimination-thresholds differences were found between the participants with ASD and the typically developing persons across spectrally and temporally complex conditions. These findings indicate that enhanced pure-tone pitch discrimination may be a cognitive correlate of speech-delay among persons with ASD. However, auditory discrimination among this group does not appear to be directly contingent on the spectro-temporal complexity of the stimuli.     

Atypical processing of auditory temporal complexity in autistics

Autistics exhibit a contrasting combination of auditory behavior, with enhanced pitch processing abilities often coexisting with reduced orienting towards complex speech sounds. Based on an analogous dissociation observed in vision, we expected that autistics’ auditory behavior with respect to complex sound processing may result from atypical activity in non-primary auditory cortex. We employed fMRI to explore the neural basis of complex non-social sound processing in 15 autistic and 13 non-autistics, using a factorial design in which auditory stimuli varied in spectral and temporal complexity. Spectral complexity was modulated by varying the harmonic content, whereas temporal complexity was modulated by varying frequency modulation depth. The detection task was performed similarly by autistics and non-autistics. In both groups, increasing spectral or temporal complexity was associated with activity increases in primary (Heschl's gyrus) and non-primary (anterolateral and posterior superior temporal gyrus) auditory cortex Activity was right-lateralized for spectral and left-lateralized for temporal complexity. Increasing temporal complexity was associated with greater activity in anterolateral superior temporal gyrus in non-autistics and greater effects in Heschl's gyrus in autistics. While we observed similar hierarchical functional organization for auditory processing in both groups, autistics exhibited diminished activity in non-primary auditory cortex and increased activity in primary auditory cortex in response to the presentation of temporally, but not of spectrally complex sounds. Greater temporal complexity effects in regions sensitive to acoustic features and reduced temporal complexity effects in regions sensitive to more abstract sound features could represent a greater focus towards perceptual aspects of speech sounds in autism.     

Delayed automatic detection of change in speech sounds in adults with autism: a magnetoencephalographic study.

OBJECTIVE: Autism is a form of pervasive developmental disorder in which dysfunction in interpersonal relationships and communication is fundamental. This study evaluated neurophysiological abnormalities at the basic level of language processing, i.e. automatic change detection of speech and non-speech sounds, using magnetoencephalographic recording of mismatch response elicited by change in vowels and tones. METHODS: The auditory magnetic mismatch field (MMF) was evaluated in 9 adults with autism and 19 control subjects using whole-head magnetoencephalography. The MMF in response to the duration change of a pure tone or vowel /a/ and that in response to across-phoneme change between vowels /a/ and /o/, were recorded. RESULTS: The groups were not significantly different in MMF power under any conditions. However, the autism group showed a left-biased latency prolongation of the MMF particularly under the across-phoneme change condition, and this latency delay was significantly associated with greater symptom severity. CONCLUSIONS: These results suggest that adults with autism are associated with delayed processing for automatic change detection of speech sounds. These electrophysiological abnormalities at the earliest level of information processing may contribute to the basis for language deficits observed in autism. SIGNIFICANCE: These results provide the first evidence for delayed latency of phonetic MMF in adults with autism.     

Responsiveness to repeated speech stimuli persists in left but not right auditory cortex

Activation of the auditory cortex habituates with repeated stimulation. While behaviorally adaptive in most circumstances, decreasing auditory responsiveness could interfere with speech perception. We therefore tested whether auditory habituation differs for speech and non-speech stimuli and for left and right auditory cortex. We examined seven right-handed subjects in whom we had determined left-hemispheric language dominance by event-related blood flow assessment. We recorded magnetoencephalographic-evoked responses to trains of four sine tones or vowels and measured the decrement from the first to the last stimulus of the response component about 100 ms after stimulus onset (N1). For the sine tones there was a decrement in both hemispheres. Conversely, for vowels there was significant attenuation of the auditory decrement in the left compared with the right hemisphere (p=0.017). This left-hemisphere persistence in auditory responsiveness to vowels demonstrates that the human brain processes speech stimuli differently than non-speech stimuli and that the left-hemisphere plays a dominant role in this speech-specific auditory processing.     

Perception of dichotic chords by normal and commisurotomized human subjects

A perceptual suppression of an ipsilateral by a concurrent contralateral auditory signal occurs in commissurotomized subjects and probably in normal subjects. This suppression of the ipsilateral signal depends on the nature of the auditory stimuli. For dichotic speech sounds the suppression of the ipsilateral signal is overwhelming; for dichotically presented pure tones it is not present. For dichotically presented pure tones, unlike speech signals, a subcortical central pitch processor determines the contribution to the perceptual experience of the right and left ear signals in both normal as well as commissurotomized subjects.     

On the nature of the cortical function underlying right hemisphere auditory perception

The nature of the function underlying the right hemisphere superiority in processing some types of auditory stimuli was examined by investigating the relationship between the degree of functional asymmetry observed during dichotic testing and the harmonic information conveyed in the test stimuli. Ninety-six right handed subjects received one of four dichotic pitch recognition tests. The tests differed from one another in the number of constituent overtones present in the tonal stimuli. As stimuli increased in complexity from pure tones to square waves, the overall accuracy of pitch discriminations increased and a right hemisphere advantage emerged for both accuracy and latency of response. These results indicate that right hemisphere auditory function is specialized for the analysis of steady state harmonic information rather than for music perception per se.     

Right hemisphere specialization for intensity discrimination of musical and speech sounds

Sound intensity is the primary and most elementary feature of auditory signals. Its discrimination plays a fundamental role in different behaviours related to auditory perception such as sound source localization, motion detection, and recognition of speech sounds. This study was aimed at investigating hemispheric asymmetries for processing intensity of complex tones and consonant-vowel syllables. Forty-four right-handed non-musicians were presented with two dichotic matching-to-sample tests with focused attention: one with complex tones of different intensities (musical test) and the other with consonant-vowel syllables of different intensities (speech test). Intensity differences (60, 70, and 80 dBA) were obtained by altering the gain of a synthesized harmonic tone (260 Hz fundamental frequency) and of a consonant-vowel syllable (/ba/) recorded from a natural voice. Dependent variables were accuracy and reaction time. Results showed a significant clear-cut left ear advantage in both tests for both dependent variables. A monaural control experiment ruled out possible attentional biases. This study provides behavioural evidence of a right hemisphere specialization for the perception of the intensity of musical and speech sounds in healthy subjects.     

Maturation of the auditory t-complex brain response across adolescence

Adolescence is a time of great change in the brain in terms of structure and function. It is possible to track the development of neural function across adolescence using auditory event-related potentials (ERPs). This study tested if the brain's functional processing of sound changed across adolescence. We measured passive auditory t-complex peaks to pure tones and consonant-vowel (CV) syllables in 90 children and adolescents aged 10–18 years, as well as 10 adults. Across adolescence, Na amplitude increased to tones and speech at the right, but not left, temporal site. Ta amplitude decreased at the right temporal site for tones, and at both sites for speech. The Tb remained constant at both sites. The Na and Ta appeared to mature later in the right than left hemisphere. The t-complex peaks Na and Tb exhibited left lateralization and Ta showed right lateralization. Thus, the functional processing of sound continued to develop across adolescence and into adulthood.     

Generalized auditory agnosia with spared music recognition in a left-hander. Analysis of a case with a right temporal stroke

After a right temporoparietal stroke, a left-handed man lost the ability to understand speech and environmental sounds but developed greater appreciation for music. The patient had preserved reading and writing but poor verbal comprehension. Slower speech, single syllable words, and minimal written cues greatly facilitated his verbal comprehension. On identifying environmental sounds, he made predominant acoustic errors. Although he failed to name melodies, he could match, describe, and sing them. The patient had normal hearing except for presbyacusis, right-ear dominance for phonemes, and normal discrimination of basic psychoacoustic features and rhythm. Further testing disclosed difficulty distinguishing tone sequences and discriminating two clicks and short-versus-long tones, particularly in the left ear. Together, these findings suggest impairment in a direct route for temporal analysis and auditory word forms in his right hemisphere to Wernicke's area in his left hemisphere. The findings further suggest a separate and possibly rhythm-based mechanism for music recognition.     

The discrimination of and orienting to speech and non-speech sounds in children with autism

The present study aimed to find out how different stages of cortical auditory processing (sound encoding, discrimination, and orienting) are affected in children with autism. To this end, auditory event-related potentials (ERP) were studied in 15 children with autism and their controls. Their responses were recorded for pitch, duration, and vowel changes in speech stimuli, and for corresponding changes in the non-speech counterparts of the stimuli, while the children watched silent videos and ignored the stimuli. The responses to sound repetition were diminished in amplitude in the children with autism, reflecting impaired sound encoding. The mismatch negativity (MMN), an ERP indexing sound discrimination, was enhanced in the children with autism as far as pitch changes were concerned. This is consistent with earlier studies reporting auditory hypersensitivity and good pitch-processing abilities, as well as with theories proposing enhanced perception of local stimulus features in individuals with autism. The discrimination of duration changes was impaired in these children, however. Finally, involuntary orienting to sound changes, as reflected by the P3a ERP, was more impaired for speech than non-speech sounds in the children with autism, suggesting deficits particularly in social orienting. This has been proposed to be one of the earliest symptoms to emerge, with pervasive effects on later development.     

Mapping the Developmental Trajectory and Correlates of Enhanced Pitch Perception on Speech Processing in Adults with ASD

Whilst enhanced perception has been widely reported in individuals with Autism Spectrum Disorders (ASDs), relatively little is known about the developmental trajectory and impact of atypical auditory processing on speech perception in intellectually high-functioning adults with ASD. This paper presents data on perception of complex tones and speech pitch in adult participants with high-functioning ASD and typical development, and compares these with pre-existing data using the same paradigm with groups of children and adolescents with and without ASD. As perceptual processing abnormalities are likely to influence behavioural performance, regression analyses were carried out on the adult data set. The findings revealed markedly different pitch discrimination trajectories and language correlates across diagnostic groups. While pitch discrimination increased with age and correlated with receptive vocabulary in groups without ASD, it was enhanced in childhood and stable across development in ASD. Pitch discrimination scores did not correlate with receptive vocabulary scores in the ASD group and for adults with ASD superior pitch perception was associated with sensory atypicalities and diagnostic measures of symptom severity. We conclude that the development of pitch discrimination, and its associated mechanisms markedly distinguish those with and without ASD.     

Speech perception, rapid temporal processing, and the left hemisphere: a case study of unilateral pure word deafness

The mechanisms and functional anatomy underlying the early stages of speech perception are still not well understood. One way to investigate the cognitive and neural underpinnings of speech perception is by investigating patients with speech perception deficits but with preserved ability in other domains of language. One such case is reported here: patient NL shows highly impaired speech perception despite normal hearing ability and preserved semantic knowledge, speaking, and reading ability, and is thus classified as a case of pure word deafness (PWD). NL has a left temporoparietal lesion without right hemisphere damage and DTI imaging suggests that he has preserved cross-hemispheric connectivity, arguing against an account of PWD as a disconnection of left lateralized language areas from auditory input. Two experiments investigated whether NL's speech perception deficit could instead result from an underlying problem with rapid temporal processing. Experiment 1 showed that NL has particular difficulty discriminating sounds that differ in terms of rapid temporal changes, be they speech or non-speech sounds. Experiment 2 employed an intensive training program designed to improve rapid temporal processing in language impaired children (Fast ForWord; Scientific Learning Corporation, Oakland, CA) and found that NL was able to improve his ability to discriminate rapid temporal differences in non-speech sounds, but not in speech sounds. Overall, these data suggest that patients with unilateral PWD may, in fact, have a deficit in (left lateralized) temporal processing ability, however they also show that a rapid temporal processing deficit is, by itself, unable to account for this patient's speech perception deficit.     

Cortical sound processing in children with autism disorder: an MEG investigation

Previous work investigating frequency encoding mechanisms in human auditory cortex has provided evidence that latency of the auditory evoked M100 is strongly proportional to frequency, with low frequency (100-200 Hz) tones associated with approximately 30 ms longer latencies than mid-range frequency (1-2 kHz) tones. Motivated by pervasive speech and auditory perception deficits observed in autism spectrum disorder, we evaluated M100 frequency dependence in children with autism disorder and typically developing controls. Results indicate that for control children, the dynamic range of frequency modulation was similar to previous reports for healthy adults. Children with autism had a much reduced range of modulation in right hemisphere sites. Findings indicate that frequency encoding mechanisms may follow a differential maturational path in autism spectrum disorder.     

Auditory processing in autism spectrum disorder: a review

For individuals with autism spectrum disorder or 'ASD' the ability to accurately process and interpret auditory information is often difficult. Here we review behavioural, neurophysiological and imaging literature pertaining to this field with the aim of providing a comprehensive account of auditory processing in ASD, and thus an effective tool to aid further research. Literature was sourced from peer-reviewed journals published over the last two decades which best represent research conducted in these areas. Findings show substantial evidence for atypical processing of auditory information in ASD at behavioural and neural levels. Abnormalities are diverse, ranging from atypical perception of various low-level perceptual features (i.e. pitch, loudness) to processing of more complex auditory information such as prosody. Trends across studies suggest auditory processing impairments in ASD are most likely to present during processing of complex auditory information and are more severe for speech than for non-speech stimuli. The interpretation of these findings with respect to various cognitive accounts of ASD is discussed and suggestions offered for further research.     

Representation of temporal sound features in the human auditory cortex

Temporal information in acoustic signals is important for the perception of environmental sounds, including speech. This review focuses on several aspects of temporal processing within human auditory cortex and its relevance for the processing of speech sounds. Periodic non-speech sounds, such as trains of acoustic clicks and bursts of amplitude-modulated noise or tones, can elicit different percepts depending on the pulse repetition rate or modulation frequency. Such sounds provide convenient methodological tools to study representation of timing information in the auditory system. At low repetition rates of up to 8-10 Hz, each individual stimulus (a single click or a sinusoidal amplitude modulation cycle) within the sequence is perceived as a separate event. As repetition rates increase up to and above approximately 40 Hz, these events blend together, giving rise first to the percept of flutter and then to pitch. The extent to which neural responses of human auditory cortex encode temporal features of acoustic stimuli is discussed within the context of these perceptual classes of periodic stimuli and their relationship to speech sounds. Evidence for neural coding of temporal information at the level of the core auditory cortex in humans suggests possible physiological counterparts to perceptual categorical boundaries for periodic acoustic stimuli. Temporal coding is less evident in auditory cortical fields beyond the core. Finally, data suggest hemispheric asymmetry in temporal cortical processing.     

Auditory processing studied prospectively in two hemidecorticectomy patients

Auditory processing of speech and nonspeech sounds was studied prospectively in two hemidecorticectomy patients (ages 10-11 years) with Rasmussen's syndrome. We tested auditory word recognition under four listening conditions: in quiet, in noise, after acoustic filtering, and dichotically. Recognition of environmental sounds and discrimination of tones and digitized syllables were also tested. Presurgical testing confirmed normal processing of speech and nonspeech, for both patients, under all listening conditon. One year after surgery, both patients demonstrated intact recognition of words and environmental sounds in quiet but impaired word recognition in noise. The left hemidecorticectomy patient also demonstrated impaired recognition of low-pass filtered words. These findings suggest that either hemisphere can process speech or nonspeech sounds in quiet, whereas both hemispheres are needed to process speech in background noise. Hemispheric contributions to processing speech in noise appear to differ, with the left hemisphere compensating for loss of phonologic information and the right hemisphere compensating for increased attention demands.     

Can Spectro-Temporal Complexity Explain the Autistic Pattern of Performance on Auditory Tasks?

To test the hypothesis that level of neural complexity explain the relative level of performance and brain activity in autistic individuals, available behavioural, ERP and imaging findings related to the perception of increasingly complex auditory material under various processing tasks in autism were reviewed. Tasks involving simple material (pure tones) and/or low-level operations (detection, labelling, chord disembedding, detection of pitch changes) show a superior level of performance and shorter ERP latencies. In contrast, tasks involving spectrally- and temporally-dynamic material and/or complex operations (evaluation, attention) are poorly performed by autistics, or generate inferior ERP activity or brain activation. Neural complexity required to perform auditory tasks may therefore explain pattern of performance and activation of autistic individuals during auditory tasks.     

Latency of the auditory evoked neuromagnetic field components: stimulus dependence and insights toward perception.

This review will focus on investigations of the auditory evoked neuromagnetic field component, the M100, detectable in the magnetoencephalogram recorded during presentation of auditory stimuli, approximately 100 milliseconds after stimulus onset. In particular, the dependence of M100 latency on attributes of the stimulus, such as intensity, pitch and timbre will be discussed, along with evidence relating M100 latency observations to perceptual features of the stimuli. Comparison with investigation of the analogous electrical potential component, the N1, will be made. Parametric development of stimuli from pure tones through complex tones to speech elements will be made, allowing the influence of spectral pitch, virtual pitch and perceptual categorization to be delineated and suggesting implications for the role of such latency observations in the study of speech processing. The final section will deal with potential clinical applications offered by M100 latency measurements, as objective indices of normal and abnormal cortical processing.