Enhanced pitch sensitivity in individuals with autism: a signal detection analysis

Past research has shown a superiority of participants with high-functioning autism over comparison groups in memorizing picture-pitch associations and in detecting pitch changes in melodies. A subset of individuals with autism, known as "musical savants," is also known to possess absolute pitch. This superiority might be due to an abnormally high sensitivity to fine-grained pitch differences in sounds. To test this hypothesis, psychoacoustic tasks were devised so as to use a signal detection methodology. Participants were all musically untrained and were divided into a group of 12 high-functioning individuals with autism and a group of 12 normally developing individuals. Their task was to judge the pitch of pure tones in a "same-different" discrimination task and in a "high-low" categorization task. In both tasks, the obtained psychometric functions revealed higher pitch sensitivity for subjects with autism, with a more pronounced advantage over control participants in the categorization task. These findings confirm that pitch processing is enhanced in "high-functioning" autism. Superior performance in pitch discrimination and categorization extends previous findings of enhanced visual performance to the auditory domain. Thus, and as predicted by the enhanced perceptual functioning model for peaks of ability in autism (Mottron & Burack, 2001), autistic individuals outperform typically developing population in a variety of low-level perceptual tasks.     

A review of behavioural and electrophysiological studies on auditory processing and speech perception in autism spectrum disorders

This literature review aims to interpret behavioural and electrophysiological studies addressing auditory processing in children and adults with autism spectrum disorder (ASD). Data have been organised according to the applied methodology (behavioural versus electrophysiological studies) and according to stimulus complexity (pure versus complex tones versus speech sounds). In line with the weak central coherence (WCC) theory of autism we aimed to investigate whether individuals with ASD show a more locally and less globally oriented processing style in the auditory modality. To avoid the possible confound of stimulus complexity, this influence was taken into account as an additional hypothesis. The review reveals that the identification and discrimination of isolated acoustic features (in particular pitch processing) is generally intact or enhanced in individuals with ASD, for pure as well as for complex tones and speech sounds. It thus appears that the local processing advantage is not influenced by stimulus complexity. Individuals with ASD are also less susceptible to global interference of speech-like material. A deficit in global auditory processing, however, is less universally confirmed. We propose that the observed pattern of auditory enhancements and deficits in ASD may be related to an atypical pattern of right hemisphere dominance. As the right and left hemisphere are relatively more specialized in spectral versus temporal auditory processing, respectively, right hemisphere dominance in ASD could provoke enhanced pitch and vowel processing, whereas left hemisphere deficiencies might explain speech perception problems and temporal processing deficits.     

Enhanced Perceptual Functioning in Autism: An Update, and Eight Principles of Autistic Perception

We propose an "Enhanced Perceptual Functioning" model encompassing the main differences between autistic and non-autistic social and non-social perceptual processing: locally oriented visual and auditory perception, enhanced low-level discrimination, use of a more posterior network in "complex" visual tasks, enhanced perception of first order static stimuli, diminished perception of complex movement, autonomy of low-level information processing toward higher-order operations, and differential relation between perception and general intelligence. Increased perceptual expertise may be implicated in the choice of special ability in savant autistics, and in the variability of apparent presentations within PDD (autism with and without typical speech, Asperger syndrome) in non-savant autistics. The overfunctioning of brain regions typically involved in primary perceptual functions may explain the autistic perceptual endophenotype.     

Parameters of semantic multisensory integration depend on timing and modality order among people on the autism spectrum: evidence from event-related potentials

Individuals with autism spectrum disorders (ASD) report difficulty integrating simultaneously presented visual and auditory stimuli (Iarocci & McDonald, 2006), albeit showing enhanced perceptual processing of unisensory stimuli, as well as an enhanced role of perception in higher-order cognitive tasks (Enhanced Perceptual Functioning (EPF) model; Mottron, Dawson, Soulières, Hubert, & Burack, 2006). Individuals with an ASD also integrate auditory-visual inputs over longer periods of time than matched typically developing (TD) peers (Kwakye, Foss-Feig, Cascio, Stone & Wallace, 2011). To tease apart the dichotomy of both extended multisensory processing and enhanced perceptual processing, we used behavioral and electrophysiological measurements of audio-visual integration among persons with ASD. 13 TD and 14 autistics matched on IQ completed a forced choice multisensory semantic congruence task requiring speeded responses regarding the congruence or incongruence of animal sounds and pictures. Stimuli were presented simultaneously or sequentially at various stimulus onset asynchronies in both auditory first and visual first presentations. No group differences were noted in reaction time (RT) or accuracy. The latency at which congruent and incongruent waveforms diverged was the component of interest. In simultaneous presentations, congruent and incongruent waveforms diverged earlier (circa 150 ms) among persons with ASD than among TD individuals (around 350 ms). In sequential presentations, asymmetries in the timing of neuronal processing were noted in ASD which depended on stimulus order, but these were consistent with the nature of specific perceptual strengths in this group. These findings extend the Enhanced Perceptual Functioning Model to the multisensory domain, and provide a more nuanced context for interpreting ERP findings of impaired semantic processing in ASD.     

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.     

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.     

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.     

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.     

Effects of voice harmonic complexity on ERP responses to pitch-shifted auditory feedback

Objective

The present study investigated the neural mechanisms of voice pitch control for different levels of harmonic complexity in the auditory feedback.

Methods

Event-related potentials (ERPs) were recorded in response to +200 cents pitch perturbations in the auditory feedback of self-produced natural human vocalizations, complex and pure tone stimuli during active vocalization and passive listening conditions.

Results

During active vocal production, ERP amplitudes were largest in response to pitch shifts in the natural voice, moderately large for non-voice complex stimuli and smallest for the pure tones. However, during passive listening, neural responses were equally large for pitch shifts in voice and non-voice complex stimuli but still larger than that for pure tones.

Conclusions

These findings suggest that pitch change detection is facilitated for spectrally rich sounds such as natural human voice and non-voice complex stimuli compared with pure tones. Vocalization-induced increase in neural responses for voice feedback suggests that sensory processing of naturally-produced complex sounds such as human voice is enhanced by means of motor-driven mechanisms (e.g. efference copies) during vocal production.

Significance

This enhancement may enable the audio-vocal system to more effectively detect and correct for vocal errors in the feedback of natural human vocalizations to maintain an intended vocal output for speaking.     

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.     

Discrimination in Autism Within Different Sensory Modalities

Recent studies have suggested that unusual visual processing in autism might stem from enhanced visual discrimination. Although there are also many anecdotal reports of auditory and tactile processing disturbances in autism these have received comparatively little attention. It is possible that the enhanced discrimination ability in vision in autism might extend to other modalities and further that they may underlie many reports of unusual touch and audition. The present study investigated the performance of children with and without autism on auditory and tactile discrimination tasks and revealed superior auditory but comparable tactile discrimination in autism relative to controls. These results extend previous findings of perceptual discrimination in autism and may be relevant for a neuro-developmental hypothesis of the disorder.     

Brief Report: Atypical Neuromagnetic Responses to Illusory Auditory Pitch in Children with Autism Spectrum Disorders

Atypical auditory perception is a widely recognised but poorly understood feature of autism. In the current study, we used magnetoencephalography to measure the brain responses of 10 autistic children as they listened passively to dichotic pitch stimuli, in which an illusory tone is generated by sub-millisecond inter-aural timing differences in white noise. Relative to control stimuli that contain no inter-aural timing differences, dichotic pitch stimuli typically elicit an object related negativity (ORN) response, associated with the perceptual segregation of the tone and the carrier noise into distinct auditory objects. Autistic children failed to demonstrate an ORN, suggesting a failure of segregation; however, comparison with the ORNs of age-matched typically developing controls narrowly failed to attain significance. More striking, the autistic children demonstrated a significant differential response to the pitch stimulus, peaking at around 50 ms. This was not present in the control group, nor has it been found in other groups tested using similar stimuli. This response may be a neural signature of atypical processing of pitch in at least some autistic individuals.     

Local visual perception bias in children with high-functioning autism spectrum disorders; do we have the whole picture?

Objective: While local bias in visual processing in children with autism spectrum disorders (ASD) has been reported to result in difficulties in recognizing faces and facially expressed emotions, but superior ability in disembedding figures, associations between these abilities within a group of children with and without ASD have not been explored. Methods: Possible associations in performance on the Visual Perception Skills Figure–Ground test, a face recognition test and an emotion recognition test were investigated within 25 8–12-years-old children with high-functioning autism/Asperger syndrome, and in comparison to 33 typically developing children. Results: Analyses indicated a weak positive correlation between accuracy in Figure–Ground recognition and emotion recognition. No other correlation estimates were significant. Conclusion: These findings challenge both the enhanced perceptual function hypothesis and the weak central coherence hypothesis, and accentuate the importance of further scrutinizing the existance and nature of local visual bias in ASD.     

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.     

Delayed mismatch field for speech and non-speech sounds in children with autism

This study investigated the magnetic mismatch field elicited by changes in streams of vowels or spectrally matched tones in children with autism spectrum disorder (ASD) relative to children with typical development to explore whether impaired sound discrimination may contribute to language impairments in autism spectrum disorder. Using magnetoencephalography, we recorded evoked neural activity to 300-Hz and 700-Hz tones (and /u/ and /a/ vowels) presented in an oddball paradigm with deviant stimuli (15%) occurring within a train of standards (85%). The magnetic mismatch field was robustly observed in both groups, but children with autism spectrum disorder demonstrated a significantly delayed magnetic mismatch field compared with typically developing peers. Difficulty parsing transient differences in sounds may lead to impaired acoustic or phonological representations and subsequent language impairment in autism spectrum disorder.     

Atypical attention to voice in toddlers and pre-schoolers with autism spectrum disorder is related to unimpaired cognitive abilities. An ERP study

BackgroundSound perception in autism spectrum disorder (ASD) is usually at typical levels, even when auditory stimuli carry a social value, as it is the case for speech. Nevertheless, orienting to sounds in a speech context might be atypical in some individuals with ASD, which in ERP studies is reflected by a diminished P3a component. As P3 values and cognitive abilities seem to be inversely related under some circumstances, the current study investigates whether diminished attentional orienting to sounds in speech is equally observable in children with ASD with and without developmental delay (DD).MethodChildren with typical development (TD, n = 17) or ASD, with or without comorbid DD (ASD/DD, n = 22, and ASD/noDD, n = 12), aged 1.5 through 4 years took part in a passive auditory oddball task while EEG data were recorded. The paradigm consisted in the presentation of two deviant stimuli (one vowel sound and one complex tone) either in a speech or in a non-speech context.ResultsWe found overall more negative MMN voltages in both ASD groups compared to TD. For P3a mean voltages, we found an attenuated response in children ASD/noDD when deviant tones were presented in speech, but not in other conditions. Children with ASD/DD did not differ from TD in P3a mean voltages.ConclusionAtypical speech sound processing might be more accentuated in children with ASD/noDD than in their peers with comorbid DD. This finding is interpreted within the theoretical framework of neural adaptation.     

Differentiation of negative event-related potentials in an auditory discrimination task.

Several different negative potentials elicited in auditory perceptual tasks make spatially and temporally overlapping contributions to the scalp-recorded event-related potential. Frequent non-target tones in a 2-stimulus oddball pitch discrimination task, when compared with the same stimuli in ignore or simple reaction time conditions, elicit a negative deflection with two peaks (NA1 and NA2) differing in their latency and topography from the exogenous N92-P156 deflections. Oddball tones, when compared with the frequent ones, elicit mismatch negativity (MMN) in both ignore and discrimination conditions; MMN displays a frontocentral-posterolateral polarity inversion. In the discrimination condition, MMN is followed by N2 and P3b; the former has a more central amplitude maximum than MMN, and no posterolateral polarity inversion. When the pitch discrimination task was made more difficult, there was no effect on NA1 or NA2, but the latency of MMN, N2, P3b, and reaction time all increased in parallel. It is hypothesized that MMN reflects the outcome of an automatic mismatch detection process, and that the subsequent processing of targets is related to the event of mismatch detection.     

Atypical Categorical Perception in Autism: Autonomy of Discrimination?

A diminished top-down influence has been proposed in autism, to account for enhanced performance in low-level perceptual tasks. Applied to perceptual categorization, this hypothesis predicts a diminished influence of category on discrimination. In order to test this hypothesis, we compared categorical perception in 16 individuals with and 16 individuals without high-functioning autism. While participants with and without autism displayed a typical classification curve, there was no facilitation of discrimination near the category boundary in the autism group. The absence of influence of categorical knowledge on discrimination suggests an increased autonomy of low-level perceptual processes in autism, in the form of a reduced top-down influence from categories toward discrimination.     

Motion perception in autism: a "complex" issue

We present the first assessment of motion sensitivity for persons with autism and normal intelligence using motion patterns that require neural processing mechanisms of varying complexity. Compared to matched controls, our results demonstrate that the motion sensitivity of observers with autism is similar to that of nonautistic observers for different types of first-order (luminance-defined) motion stimuli, but significantly decreased for the same types of second-order (texture-defined) stimuli. The latter class of motion stimuli has been demonstrated to require additional neural computation to be processed adequately. This finding may reflect less efficient integrative functioning of the neural mechanisms that mediate visuoperceptual processing in autism. The contribution of this finding with regards to abnormal perceptual integration in autism, its effect on cognitive operations, and possible behavioral implications are discussed.     

Auditory micropattern discrimination in brain damaged subjects

Patients with cerebral lesions were given two tests of pitch discrimination. The first was a pure tone discrimination test; in the second, complex tones were employed in which the pitch difference between the test tones was a consequence of the temporal microstructure of the stimuli. In contrast to non-fluent aphasics whose performance was normal for both tests, six of the seven patients having a fluent aphasia performed normally on the first test but revealed a significant deficit in the second. Patients with right temporal lesions also had the same pattern of deficit. The results suggest that the temporal lobes play a special role in the processing of auditory information in which the temporal structure of the stimuli is a critical feature.