Atypical sensory-based behaviors are a ubiquitous feature of autism spectrum disorders (ASDs). In this article, we review the neural underpinnings of sensory processing in autism by reviewing the literature on neurophysiological responses to auditory, tactile, and visual stimuli in autistic individuals. We review studies of unimodal sensory processing and multisensory integration that use a variety of neuroimaging techniques, including electroencephalography (EEG), magnetoencephalography (MEG), and functional MRI. We then explore the impact of covert and overt attention on sensory processing. With additional characterization, neurophysiologic profiles of sensory processing in ASD may serve as valuable biomarkers for diagnosis and monitoring of therapeutic interventions for autism and reveal potential strategies and target brain regions for therapeutic interventions.
Autism spectrum disorders (ASDs) are defined clinically by impairment in communication, social interaction, and behavioral flexibility (1). In this review, ASD is used to include individuals with the full range of symptoms from the most severe form of the condition, autistic disorder or autism, to the milder forms, Asperger syndrome (AS) and pervasive developmental disorder not otherwise specified (PDD, NOS). Even within a diagnosis of autism, there can be a wide range of intellectual ability. ASD is clearly not a one size fits all diagnosis. There are many known etiologies that contribute to an ASD phenotype, including genetic variations (e.g. fragile X and tuberous sclerosis), environmental exposures (e.g. in utero valproic acid exposure), and prematurity. There also exists considerable phenotypic variation involving the pace of language development, the presence of epilepsy, and the range of cognitive ability. What does appear to be common to individuals across the spectrum are atypical behavioral responses to sensory information. More than 96% of children with ASD report hyper- and hyposensitivities in multiple domains. Similar to the wide range of spectrum severity found for communication and social deficits, sensory behavioral differences also range from mild to severe, and these behavioral differences can endure through adulthood (2–6).
Sensory processing concerns have been a key feature of ASD clinical descriptions from the original independent seminal reports by Asperger (7) and Kanner (7a) to first person accounts (7b). The distress caused by particular sensory stimuli can cause self-injurious and aggressive behavior in those who are unable to communicate their duress. Although sensory hyper- and hyporesponsiveness are not unique to ASD, they appear to be more prevalent in this population than in other developmental disabilities (4,8,9). There is limited consensus regarding the pattern of these sensory deficits in ASD. However, historically, proximal senses such as touch, smell, and taste were thought to be particularly at risk and to indicate developmental immaturity (10,11). Interestingly, these tend to be the least well studied of the sensory modalities, whereas there is mounting evidence for disruption of the auditory and visual processing pathways and a surging interest in multisensory integration (MSI). We will review the current literature on the neurophysiology in individuals on the autism spectrum with a focus on the processing of simple sensory input in the auditory, visual, and tactile modalities. We begin by considering the processing of unimodal stimuli, then we will address MSI, and finally, we will examine the role of attention on the sensory processing stream.
Auditory Sensory Processing
As language deficits are a core feature of ASD, the study of auditory processing is essential to considering the roots of ASD and to conceptualizing rational interventions. One way of measuring the flow of auditory information processing is through the traditional auditory brainstem response in which the electrical activity evoked from a series of clicks or tones is recorded in milliseconds using surface electrodes. Incoming auditory stimuli from the vestibulocochlear nerve (cranial nerve VIII) travel to processing structures in the brainstem (cochlear nuclei and the superior olivary complex) and midbrain (inferior colliculus). The auditory brainstem response literature reports varied and contradictory findings. Some studies show no differences in central transmission latency nor amplitude (12,13). In contrast, other studies have shown prolonged latencies in child and adolescent ASD cohorts (14,15). Both of these studies found significantly longer III-V interpeak latency (thought to represent neural conduction time between cranial nerve VIII and the lateral leminiscus). A recent study increased the complexity of the auditory processing demand by using a “forward masking paradigm” in adults with AS and found an attenuation of wave III amplitude that separated AS individuals from control, schizophrenic, and attention deficit hyperactivity disorder individuals (16). In addition, work by Russo et al. (17,18) with ASD children demonstrates typical brainstem responses to clicks; however, they find differences in response to varied pitch and speech sounds with noise. Consequently, although brainstem abnormalities do not appear sufficient to explain the deficits for all individuals on the autism spectrum, there is literature suggesting measurable differences in early auditory pathways, especially with increasingly complex stimuli. Understanding the nature of this fundamental step in the auditory sensory stream is crucial because the ability to acquire and parse a variety of incoming sounds forms the foundation for language and communication.
Beyond the brainstem, cortical auditory sensory processing has traditionally been examined using event-related potentials (ERPs) with EEG and magnetoencephalography (MEG). Simple auditory stimuli are presented, and the brain responses are collected over multiple trials and averaged to generate information about the temporal and spatial resolution of responses. Both EEG and MEG studies show atypical latencies in the early peaks (<150 ms) that are thought to reflect activity from the primary and association auditory cortices. Unfortunately, these studies have shown differences in latency in both directions. Two studies using 1000 Hz tones showed faster cortical latencies with varying tone durations. Ferri et al. (19) used a 100-ms tone, and Martineau et al. (20) used a 4-ms tone. Others have shown delayed latencies relative to controls. Bruneau et al. showed late auditory evoked potentials with a 750-Hz tone and 200-ms duration (21); Oram Cardy et al. (22) found the same delay with a 1-kHz tone and 300-ms duration; and Roberts et al. (23), using MEG, report a delay in right hemisphere M100 response to 300-ms tones over a range of frequencies (200, 300, 500, and 1000 Hz). When assessing vowel sounds, complex nonspeech sounds, and complex tones, Whitehouse and Bishop (24) found differences in the early peak latencies of the standard repeated tones. Studies from two groups, Bruneau et al. (21) and Oram Cardy et al. (22), suggest that in this realm of low-level processing, earlier and higher right hemisphere cortical peaks might predict better language function (21,22). The discrepancy in findings may reflect the considerable variation in ages, diagnosis, and paradigms used. The addition of behavioral phenotyping and correlations is likely to help clarify this work going forward. Furthermore, the investigation of more complex auditory tasks (such as pitch discrimination and speech versus nonspeech paradigms) coupled with variation of attention will aid in understanding altered cortical processing in ASD and will be addressed further in the attention section below.
In general, the neurophysiologic study of auditory processing in autism does suggest atypical neural activity as early in the processing stream as the primary auditory cortex. However, as Whitehouse and Bishop (24) suggest, these differences may be a result of top-down inhibitory processes mediating encoding and early sound processing. As we learn more, we may be able to predict the nature of the atypical cortical activity by defining the etiology of the individual's ASD, such that children with Fragile X may show one form of cortical differences whereas children with 16p11 duplications may show another form. It is probable that the atypical processing is related to the unusual behavioral responses so commonly observed in children on the autism spectrum such as covering of the ears to seemingly benign sounds such as the vacuum cleaner and the blender. Furthermore, one might conjecture that if the auditory input is perceived as unpleasant or noxious, affected individuals will learn to avoid auditory input, and thus curtail the learning that comes from listening to the people and world around them. Comprehension of the potentially atypical auditory processing in children with autism may be key to parsing different etiologies of autism, targeting treatments to children with auditory hyper/hypo-sensitivities, and ameliorating overwhelming auditory sensory input to facilitate learning.
Tactile Sensory Processing
Although tactile sensitivity is commonly reported in ASD, it has received far less attention in the neuroscience literature than auditory sensitivity (25). Common clinical complaints are avoiding light touch to the head and body as occur with grooming and particular clothing. The psychophysical tactile studies look at thresholds and sensitivity using vibrotactile stimuli. Adults with AS showed lower tactile perceptual thresholds for 200 Hz but not 30 Hz vibrotactile stimuli, implying a specific hypersensitivity in the Pacinian corpuscles receptor pathway (3). Tactile hypersensitivity was again shown to vibrotactile stimuli as well as thermal stimuli but not to light touch in adults with autism (26). In contrast, in a small sample of children with autism, there were no tactile perceptual threshold differences for vibrotactile (40 and 250 Hz) detection (27). However, this study did suggest a correlation between a measure of behavioral tactile sensitivity phenotype and emotional/social reaction. (This trend is considerably underpowered with a sample size of only six boys.) Beyond threshold investigation, Miyazaki et al. (28) demonstrate an enhanced early (low-level) somatosensory evoked potential peak in young autistic children using median nerve stimulation that was most prevalent in the right hemisphere response. Coskun et al. (29) most recently investigated somatosensory mapping in high functioning adults with autism using MEG. High functioning adults with autism appear to have a disrupted cortical representation of their face and hand. Again, because of the heterogeneity of ASD, the electrophysiology and functional imaging work in this domain should include behavioral measures so that within group differences do not obscure real between group differences. There is a tremendous need for further exploration in this domain as atypical tactile sensitivity appears with particularly high frequency in the autism population.
Visual Sensory Processing
Individuals with ASD also exhibit atypical visual behavior that can be construed as attempting to avoid visual input (e.g. covering eyes at bright lights) or to seek additional visual stimuli (e.g. twisting fingers in front of eyes) (4). Similar to the auditory and tactile domains, there is considerable discrepancy in neurophysiological findings. There are suggestive reports in the visual domain of enhanced detail perception, particularly for simple stimuli with impairment in more complex tasks (30). Some threshold studies show no difference between ASD individuals and controls in contrast sensitivity for low versus high spatial frequencies or motion/form processing (31,32). Other visual-evoked potential studies indicate that individuals with ASD possess atypical early peaks with impairments in object boundary detection (33), decreased contrast detection ability in both still and moving stimuli at a range of signal/noise ratios (34), and undifferentiated responses for mid- and high spatial frequency gratings (35). Local motion processing studies show differences in second order (texture defined) motion processing but intact first-order (luminance defined) processing, suggesting difficulties with effective integration of incoming stimuli that is magnified with more nuanced tasks (36).
One of the most well-studied aspects of visual perception in autism is that of face processing given the pertinence of this skill for human social interaction (37). As Klin (38) suggests, the literature is heavily confounded by differences in the familiarity of the face, attention, gaze direction and fixation, and the type/complexity of the stimulus. A functional MRI study with eye tracking shows that activation of the fusiform gyrus and the amygdala is reduced in an ASD cohort, as well as their unaffected siblings, but correlates positively with fixation time on the eye region of the face (39,40). An ERP study again highlights group differences that are dependent on directed attention such that ASD individuals do not show the expected increase in the N170 (face processing) wave with directed attention (41). An EEG study assessing γ-band activity, thought to represent the binding of visual information, gives convergent evidence for a neurophysiologic difference in AS face processing (42). Furthermore, the type of visual information matters; children with autism may respond more robustly than controls to neutral and detailed, high spatial frequency information and less robustly to the rapid low-frequency processing that is so critical to our fast-paced social world (43). The emotional valence of face processing has been investigated with a recent study suggesting hyperactivity in the right amygdala with altered connectivity between the frontal and temporal lobes (44). It is a challenge to interpret whether these differences represent primary cortical abnormalities, result from decreased visual exploration in early infancy, or are secondary to a primary social cognitive deficit.
Deficits in simple stimuli and faces extend to studies of biological motion, such that children with autism show impairments in the processing of dynamic noise, motion coherence, and form-from-motion detection (45). There are suggestions that this observed deficit may result in part from atypical processing of emotional information as children with autism were found to differ from control children only in their ability to name emotional point-light displays and not point-light displays of everyday objects (46). This finding suggests a potential disconnection from the limbic or “emotion” neural networks that inform primary sensory processing. Speaking to a genetic underpinning for these differences, inefficient motion processing has been found in siblings of individuals with ASD as well (47). In accordance with theories of increased local cortical activity (48) with impaired long-range connectivity (49), individuals with autism appear to be over-recruiting their left primary cortex compared with typicals during a motion coherence functional MRI study (50). Taken as a whole, these studies further support a disruption in the processing of basic unimodal sensory information that forms the backbone of higher order cortical abilities such as socialization.
Low-Level Multisensory Integration
Similar to the aforementioned deficits in unimodal sensory processing in children with ASD, these individuals may also perform poorly during conditions that require collapsing information across multiple modalities (or MSI). Many of the atypical perceptual experiences reported in those with ASD are believed to be due to an inability to properly filter or process simultaneous channels of visual, auditory, and tactile inputs (51). There is evidence that sensory illusions that require the proper concatenation of inputs across multiple domains operate at a different level in ASD, compared with typically developing individuals. In the “flash-beep” illusion, multiple auditory tones paired with a single transient visual stimuli can induce the perception that multiple flashes are present. At a cursory level, it appears that the integration necessary to produce this illusion is preserved in ASD, as demonstrated through a lack of difference between patients and Intelligence Quotient (IQ)-matched typical individuals (52). However, when the timing between stimulus sets is perturbed during presentation, deficits in processing begin to emerge in subjects with autism. Typically, disparity between the auditory and visual stimulus onset times will impact the effect of the illusion, until they appear uncoupled at a certain threshold. Foss-Feig et al. (53) were able to demonstrate that, in subjects with autism, the time duration between stimuli that continue to produce the illusion are broader than in typically developing individuals. The observation that broader temporal gaps continue to produce a “flash-beep” illusion in individuals with ASD suggests a level of inefficiency in the MSI in this population.
Electrophysiological studies probe the neural mechanisms of ASD that can manifest as behavioral multisensory deficits. EEG studies of multisensory processing have reported abnormal timing and level of activity within electrophysiological signatures of brain processing. Courchesne et al. (54,55) report that in individuals with ASD, a reduction in response amplitude (compared with typically developing children) is evident when concurrent auditory and visual stimuli streams are presented. The sequence of activity in the brain during MSI seems to deviate in children with autism, particularly within the later stages of processing when sensory information is collapsed. When auditory and somatosensory stimuli are presented in parallel, early (<100 ms) electrical potentials in primary sensory cortices are relatively spared in ASD; however, responses that follow this initial stage of activity in the cortex (at around 175 ms) are limited and delayed in ASD (56). These investigations indicate that both the magnitude and the latency of activity in the brain may contribute to multisensory processing deficits in ASD.
Higher-Order Multisensory Integration
Although both behavioral and neurophysiological processing impairments in simple MSI have been reported in ASD, salient differences in sensory integration are also evident at a complex level, particularly during speech comprehension and production. When audio and visual speech stimuli are staggered and presented to individuals with autism, performance drops to a chance level and indicates deficits in speech comprehension (57). Multimodal illusions of linguistic processing in ASD, such as the McGurk effect, suggest that improper timing of sensory integration contributes to observable deficits in communication in ASD. In the McGurk effect, visual processing (e.g. lip reading) is combined with auditory processing (phoneme perception) to produce the comprehension of spoken language. Although both typically developing and ASD individuals perform well during this task, typical individuals show a greater dependence on visual feedback (lip reading) compared with ASD (58,59). When both groups are trained on the visual feedback component of the McGurk effect, ASD participants fail to show improvements in performance (60,61). Furthermore, a reliance on visual feedback in noisy auditory environments is unattainable for ASD participants (61). An inability to “fall back” on certain sets of sensory stimuli in the presence of challenging environmental stimuli may contribute to the communication deficits that are well characterized in this disorder.
MSI investigations exploring the specific neurophysiological mechanisms that are compromised in ASD is just beginning (62). Many of the regions known to integrate multiple sensory inputs have been implicated, including prefrontal cortex and association regions of the temporal lobe. At the cellular level, postmortem studies of ASD have illustrated that the columnar density in the neocortex is dense in autism, potentially facilitating local processing (63). It has also been hypothesized that the cerebellum, a structure that shows significant changes in neuronal density in autism (64), may play a role in impaired sensory integration in the disorder. This mediation could occur through atypical filtering of afferent inputs, although these exact mechanisms are unclear (65). Many of the neocortical fields that play a role in MSI are also part of a putative “mirror neuron” network, first identified in homologues of these regions in nonhuman primates (66). Given the observable deficits in imitation and empathy known to be a core feature of the autism spectrum, it has been proposed that communication deficits arise from an inability of multisensory “mirror neurons” to concatenate information to facilitate higher order cognitive function (67). However, others propose that as sensory integration is dependent on the rapid exchange of information between distinct cortical and subcortical regions, disruptions in connectivity likely play the causative role (68). The ASD literature suggests both direct axonal disconnection such as has been implied by the abnormalities of the corpus callosum (69) and indirect disruption of long-range firing synchrony (70,71).
Attention Impacts Every Stage of Sensory Processing
The discussion of sensory processing in ASD would be incomplete without the consideration of the role of attention on cognitive processing. In their review, Allen and Courchesne (72) suggest that that the clinical observation of heightened reactivity to seemingly meaningless stimuli (e.g. intense tantrums in response to the hum of a blender) may be related to a neurobehavioral driven distractibility. Furthermore, narrowed interest and repetitive behaviors may represent deficits in attentional shifting. However, even defining attention is a challenging matter. According to Talsma et al. (73), “attention is a relatively broad cognitive concept that includes a set of mechanisms that determine how particular sensory input, perceptual objects, trains of thought, or courses of action are selected for further processing from an array of concurrent possible stimuli, objects, thoughts and actions.” Functionally, an individual must be able to select certain sensory inputs for enhanced processing while either filtering out or suppressing others. This selective attention can be further subdivided in operations such as attentional switching and sustained attention over time (74–76). Many brain regions are involved in processing, modulating, and integrating sensory information. There has been a particular focus on the superior colliculus, the cerebellum, and the frontal lobes in understanding this rapid and multidirectional flow of information, which is mediated by attentional demands and resources (77,78). We suggest that this multidirectional flow of information is impaired for individuals with ASD and that this disruption in cortical communication underlies the individual's inability to attend to their environment in a flexible, productive, and meaningful way. In the following sections, we will focus on two aspects of attending: first, the ability to shift focus from stimuli of one type to another (attentional switching); and second, the effect of increasing the array of information presented to measure the subject's ability to select what information needs to be attended to and what needs to be ignored (selective attention).
Attentional Shift or Switch
In this section, we will focus on studies in which the subject shifts their attention to changes in the stimuli. In ASD neurophysiologic research, the most common form of attentional switch is between a repeated stimulus and an unfamiliar or novel stimulus within the same sensory modality (exogenous attention). However, shifting paradigms can also require the subject to move from one modality to another or to shift visual or auditory focus in space (endogenous attention). In the auditory domain, researchers have primarily used the oddball paradigm to investigate attentional shift. In the oddball paradigm, a stimulus that varies on a single parameter (deviant) such as duration, frequency or intensity, is randomly inserted into a train of repeated (standard) stimuli. This deviance leads to the generation of a negative deflection on an evoked potential recording at 150–200 ms, which is best recorded from the fronto-central sites (79). This paradigm can be extended from covert (preattentive) to overt attention with a task requiring a response to the deviant (target), and other variations of this paradigm include a third rare stimuli as a nontarget (novel) comparison. In the oddball paradigm, the difference between the neural response to the standard stimuli and the deviant stimuli is called the mismatch negativity (MMN) when using an EEG recording technique or the mismatch field when using MEG. MMN/mismatch field wave forms have generated widely disparate results from normal in an ERP study of high functioning children with autism (80) to completely absent in an MEG study of low-functioning individuals with autism (81). Although there are conflicting data from other studies (82–85), Gomot et al. (86,87) report faster MMN latencies for pitch variation and atypical activation of the left anterior cingulate. This location has been implicated in attentional switching and correlated with a behavioral measure of intolerance to change. This reduced mismatch latency to pitch variation in conjunction with superior pitch recognition has been interpreted to support the theory of perceptual enhancement, whereby local processing networks are over connected at the expense of long-range connections with integration and attention networks (88–90).
Conflicting findings have also been reported for auditory MMN amplitudes. Several groups have found increased MMN amplitude in samples of adults and children with AS and ASD (19,91,92), whereas Dunn et al. (12) found reduced MMN amplitudes using a passive paradigm. Attention shifting for individuals with autism has received less focus in the visual and somatosensory domains, perhaps related to the intense interest in the auditory domain as the gateway for understanding the language and communication deficits that are central to ASDs. When Kemner et al. (93) assessed the role of visual attention using an oddball paradigm with both a passive condition and an active counting task, they found that children with autism did not differ from controls in the passive condition, but they did show a larger response to the deviant stimuli during the active task condition.
The importance of directed or overt attention on the effects of cortical processing of novelty is further highlighted by the work of Whitehouse and Bishop (24). To clarify previous findings, suggesting that orienting deficits in autism might be speech-sound specific (80), Whitehouse and Bishop performed a layered study of boys with high functioning autism examining whether processing deficits were due to a perceptual impairment (in acoustic encoding or discrimination of different speech sounds) or a function of cognitive factors (such as reduced attention). They found that, during a passive condition, children with autism showed attenuated early cortical responses to speech sounds but not complex tones. However, when the children were instructed to attend to and respond to the deviant condition, these amplitude differences were no longer evident. Similarly, Dunn et al. (12) found that the decreased MMN to simple stimuli, apparent during a passive condition, normalized with directed attention. These studies suggest that a “top down” process mediated by directed attention influences basic sensory processing for individuals on the autism spectrum.
Beyond the effects of attentional shifting, there is interest in how individuals with ASD select what information to attend to, what to ignore, and how this guides their ability to make sense of the changing world around them. In EEG/MEG studies of attentional shift, one response property of interest is the P300. The P3a is a positive deflection culminating around 300 ms that is thought to reflect orienting to changes in the environment that may underlie attentional switching; the P3b is a component of the late attention peak that reflects task-related cortical activity and may underlie working memory. The P3b is thought to emanate from temporal and parietal neural sources (94). The earliest autism study reporting a P300 attention wave targeted attention by presenting a train of stroboscopic flashes with an occasional missing flashes (95). In the three individuals investigated, the study investigators found good accuracy in the behavioral task but small or absent late positive waves. This suggests, as has been seen in the auditory literature, that in simple tasks, behavioral performance can be similar between groups while the cortical activity differs. In a series of visual oddball studies, Courchesne et al. (54) first used a letter mismatch and found normal P3b amplitudes; in a later study, they used blue and red squares (color mismatch) and again found typical P3b responses with targeted attention (54,55). In a subsequent study, they added an additional level of spatial complexity to the task—there were five empty squares, one of which was designated to be attended to; when the circle appeared in the attended box (target), the participant responded with a button press; when the circle appeared in an “un”attended box, the condition was ignored. In this visual-spatial selective attention task, they found a delay in the frontal P3a (attention orienting) and a diminution in the parietal P3b (96). With this degree of spatial challenge, this cohort of high functioning ASD males had difficulty in both speed and accuracy relative to matched controls. This series suggests that increasing the attention and capacity demands of this visual task leads to both behavioral and physiologic differences in individuals with autism versus controls, whereas simple visual attention tasks may fail distinguish them. Other visual oddball studies support this finding of diminished P3 amplitudes and have correlated a shorter visual fixation period with the P3 diminution (93,97). These investigations suggest that the density and complexity of the incoming stimuli may affect the degree to which the attention neural networks are recruited for processing of incoming sensory information.
Our ability to attend appears to have a limited capacity (i.e. there is a finite quantity of information that can be considered simultaneously), and we therefore need to selectively concentrate on one aspect of the environment while ignoring other features to effectively and efficiency process sensory input (75). This capacity may be even more limited in certain subgroups of individuals with ASD. An ERP auditory task with selected spatial attention demonstrates this capacity effect: high functioning adults with autism showed both behaviorally diminished ability to selectively tune into a specified sound source as well as an ERP signature of this deficit with relatively broader N1 and shallower P3 peaks when compared with a typical control group (98). This finding was only evident with increased task complexity (i.e. more speakers and a continuous, rapid stream of complex tone distractors). In a task of divided attention between visual and auditory stimuli, the failure of the autism group to modulate the slow negative wave in response to focused/divided/ignored conditions is thought to indicate a potential deficit in selective inhibition and attention (99). This finding echoes the anecdotal reports of parents that children with autism can function typically in a well-controlled environment but decompensate in the face of challenging sensory environments such as a grocery store or an animated birthday party. Children with autism may have more difficulty with automatic processing of information and may already rely more heavily on already overloaded attention and working-memory based networks, such that when the stimuli reach and exceed capacity, the processing system fails (12,90).
Given the ubiquitous nature of sensory behavioral differences for individuals with autism, understanding the neural underpinnings of basic sensory processing in ASDs is an important task. Furthermore, as the neurophysiologic data mount, we suggest that differences in sensory processing may actually cause core features of autism such as language delay (auditory processing) and difficulty with reading emotion from faces (visual processing). Interpreting the neuroscience has been complicated by the heterogeneity of the disorder as well as the difficulty in designing tasks that can precisely probe our finely tuned and intricately connected sensory neural networks. Despite these challenges, tremendous gains have been made over the past 30 years and will guide both our understanding of the disorder as well as provide insights into how to strengthen basic processing and attention for affected individuals.
Going forward, studies of infant siblings of individuals affected with ASD can provide an understanding of whether sensory processing differences are a primary feature of the disorder or a result of learned behaviors. Behavioral intervention trials, such as computerized training modules and self-regulation programs, need to be studied both for efficacy and to determine whether there is normalization of neural activity in affected individuals. Psychopharmacology studies targeting attention and arousal paired with functional imaging assessments hold great promise in providing valuable treatment models. Finally, careful sensory behavioral phenotyping is essential for both understanding our neurophysiologic research as well as tailoring appropriate and effective treatments.
autism spectrum disorders
American Psychiatric Association 1994 Diagnostic and Statistical Manual of Mental Disorders: DSM-IV. 4th ed. American Psychiatric Association, Washington, D.C
Minshew NJ, Sweeney J, Luna B 2002 Autism as a selective disorder of complex information processing and underdevelopment of neocortical systems. Mol Psychiatry 7: S14–S15
Blakemore SJ, Tavassoli T, Calo S, Thomas RM, Catmur C, Frith U, Haggard P 2006 Tactile sensitivity in Asperger syndrome. Brain Cogn 61: 5–13
Leekam SR, Nieto C, Libby SJ, Wing L, Gould J 2007 Describing the sensory abnormalities of children and adults with autism. J Autism Dev Disord 37: 894–910
Tomchek SD, Dunn W 2007 Sensory processing in children with and without autism: a comparative study using the short sensory profile. Am J Occup Ther 61: 190–200
Crane L, Goddard L, Pring L 2009 Sensory processing in adults with autism spectrum disorders. Autism 13: 215–228
Asperger H 1944 [Autistic psychopathy in childhood]. Arch Psychiatr Nervenkr 117: 76–136
Kanner L 1943 Autistic disturbances of affective contact. Nervous Child 2: 217–250
Grandin T 1995 Thinking in Pictures; and other reports from my life with autism. Doubleday, New York
Baranek GT, David FJ, Poe MD, Stone WL, Watson LR 2006 Sensory Experiences Questionnaire: discriminating sensory features in young children with autism, developmental delays, and typical development. J Child Psychol Psychiatry 47: 591–601
Ben-Sasson A, Hen L, Fluss R, Cermak SA, Engel-Yeger B, Gal E 2009 A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. J Autism Dev Disord 39: 1–11
Ayres AJ, Tickle LS 1980 Hyper-responsivity to touch and vestibular stimuli as a predictor of positive response to sensory integration procedures by autistic children. Am J Occup Ther 34: 375–381
Baranek GT, Foster LG, Berkson G 1997 Tactile defensiveness and stereotyped behaviors. Am J Occup Ther 51: 91–95
Dunn MA, Gomes H, Gravel J 2008 Mismatch negativity in children with autism and typical development. J Autism Dev Disord 38: 52–71
Courchesne E, Courchesne RY, Hicks G, Lincoln AJ 1985 Functioning of the brain-stem auditory pathway in non-retarded autistic individuals. Electroencephalogr Clin Neurophysiol 61: 491–501
Rosenhall U, Nordin V, Brantberg K, Gillberg C 2003 Autism and auditory brain stem responses. Ear Hear 24: 206–214
Kwon S, Kim J, Choe BH, Ko C, Park S 2007 Electrophysiologic assessment of central auditory processing by auditory brainstem responses in children with autism spectrum disorders. J Korean Med Sci 22: 656–659
Källstrand J, Olsson O, Nehlstedt SF, Sköld ML, Nielzén S 2010 Abnormal auditory forward masking pattern in the brainstem response of individuals with Asperger syndrome. Neuropsychiatr Dis Treat 6: 289–296
Russo N, Nicol T, Trommer B, Zecker S, Kraus N 2009 Brainstem transcription of speech is disrupted in children with autism spectrum disorders. Dev Sci 12: 557–567
Russo NM, Skoe E, Trommer B, Nicol T, Zecker S, Bradlow A, Kraus N 2008 Deficient brainstem encoding of pitch in children with Autism Spectrum Disorders. Clin Neurophysiol 119: 1720–1731
Ferri R, Elia M, Agarwal N, Lanuzza B, Musumeci SA, Pennisi G 2003 The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low-functioning subjects. Clin Neurophysiol 114: 1671–1680
Martineau J, Garreau B, Barthelemy C, Lelord G 1984 Evoked potentials and P300 during sensory conditioning in autistic children. Ann N Y Acad Sci 425: 362–369
Bruneau N, Bonnet-Brilhault F, Gomot M, Adrien JL, Barthelemy C 2003 Cortical auditory processing and communication in children with autism: electrophysiological/behavioral relations. Int J Psychophysiol 51: 17–25
Oram Cardy JE, Flagg EJ, Roberts W, Roberts TP 2008 Auditory evoked fields predict language ability and impairment in children. Int J Psychophysiol 68: 170–175
Roberts TP, Khan SY, Rey M, Monroe JF, Cannon K, Blaskey L, Woldoff S, Qasmieh S, Gandal M, Schmidt GL, Zarnow DM, Levy SE, Edgar JC 2010 MEG detection of delayed auditory evoked responses in autism spectrum disorders: towards an imaging biomarker for autism. Autism Res 3: 8–18
Whitehouse AJ, Bishop DV 2008 Do children with autism ‘switch off' to speech sounds? An investigation using event-related potentials. Dev Sci 11: 516–524
Wiggins LD, Robins DL, Bakeman R, Adamson LB 2009 Brief report: sensory abnormalities as distinguishing symptoms of autism spectrum disorders in young children. J Autism Dev Disord 39: 1087–1091
Cascio C, McGlone F, Folger S, Tannan V, Baranek G, Pelphrey KA, Essick G 2008 Tactile perception in adults with autism: a multidimensional psychophysical study. J Autism Dev Disord 38: 127–137
Güçlü B, Tanidir C, Mukaddes NM, Unal F 2007 Tactile sensitivity of normal and autistic children. Somatosens Mot Res 24: 21–33
Miyazaki M, Fujii E, Saijo T, Mori K, Hashimoto T, Kagami S, Kuroda Y 2007 Short-latency somatosensory evoked potentials in infantile autism: evidence of hyperactivity in the right primary somatosensory area. Dev Med Child Neurol 49: 13–17
Coskun MA, Varghese L, Reddoch S, Castillo EM, Pearson DA, Loveland KA, Papanicolaou AC, Sheth BR 2009 How somatic cortical maps differ in autistic and typical brains. Neuroreport 20: 175–179
Bertone A, Mottron L, Jelenic P, Faubert J 2005 Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity. Brain 128: 2430–2441
de Jonge MV, Kemner C, de Haan EH, Coppens JE, van den Berg TJ, van Engeland H 2007 Visual information processing in high-functioning individuals with autism spectrum disorders and their parents. Neuropsychology 21: 65–73
Koh HC, Milne E, Dobkins K 2010 Spatial contrast sensitivity in adolescents with autism spectrum disorders. J Autism Dev Disord 40: 978–987
Vandenbroucke MW, Scholte HS, van Engeland H, Lamme VA, Kemner C 2008 A neural substrate for atypical low-level visual processing in autism spectrum disorder. Brain 131: 1013–1024
Sanchez-Marin FJ, Padilla-Medina JA 2008 A psychophysical test of the visual pathway of children with autism. J Autism Dev Disord 38: 1270–1277
Jemel B, Mimeault D, Saint-Amour D, Hosein A, Mottron L 2010 VEP contrast sensitivity responses reveal reduced functional segregation of mid and high filters of visual channels in autism. J Vis 10: 13
Bertone A, Mottron L, Jelenic P, Faubert J 2003 Motion perception in autism: a “complex” issue. J Cogn Neurosci 15: 218–225
Schultz RT 2005 Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci 23: 125–141
Klin A 2008 Three things to remember if you are a functional magnetic resonance imaging researcher of face processing in autism spectrum disorders. Biol Psychiatry 64: 549–551
Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, Alexander AL, Davidson RJ 2005 Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 8: 519–526
Dalton KM, Nacewicz BM, Alexander AL, Davidson RJ 2007 Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biol Psychiatry 61: 512–520
Churches O, Wheelwright S, Baron-Cohen S, Ring H 2010 The N170 is not modulated by attention in autism spectrum conditions. Neuroreport 21: 399–403
Grice SJ, Spratling MW, Karmiloff-Smith A, Halit H, Csibra G, de Haan M, Johnson MH 2001 Disordered visual processing and oscillatory brain activity in autism and Williams syndrome. Neuroreport 12: 2697–2700
Vlamings PH, Jonkman LM, van Daalen E, van der Gaag RJ, Kemner C 2010 Basic abnormalities in visual processing affect face processing at an early age in autism spectrum disorder. Biol Psychiatry 68: 1107–1113
Monk CS, Weng SJ, Wiggins JL, Kurapati N, Louro HM, Carrasco M, Maslowsky J, Risi S, Lord C 2010 Neural circuitry of emotional face processing in autism spectrum disorders. J Psychiatry Neurosci 35: 105–114
Annaz D, Remington A, Milne E, Coleman M, Campbell R, Thomas MS, Swettenham J 2010 Development of motion processing in children with autism. Dev Sci 13: 826–838
Parron C, Da Fonseca D, Santos A, Moore DG, Monfardini E, Deruelle C 2008 Recognition of biological motion in children with autistic spectrum disorders. Autism 12: 261–274
Koh HC, Milne E, Dobkins K 2010 Contrast sensitivity for motion detection and direction discrimination in adolescents with autism spectrum disorders and their siblings. Neuropsychologia 48: 4046–4056
Rubenstein JL, Merzenich MM 2003 Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255–267
Belmonte MK, Cook EH Jr, Anderson GM, Rubenstein JL, Greenough WT, Beckel-Mitchener A, Courchesne E, Boulanger LM, Powell SB, Levitt PR, Perry EK, Jiang YH, DeLorey TM, Tierney E 2004 Autism as a disorder of neural information processing: directions for research and targets for therapy. Mol Psychiatry 9: 646–663
Brieber S, Herpertz-Dahlmann B, Fink GR, Kamp-Becker I, Remschmidt H, Konrad K 2010 Coherent motion processing in autism spectrum disorder (ASD): an fMRI study. Neuropsychologia 48: 1644–1651
O'Neill M, Jones RS 1997 Sensory-perceptual abnormalities in autism: a case for more research?. J Autism Dev Disord 27: 283–293
van der Smagt MJ, van Engeland H, Kemner C 2007 Brief report: can you see what is not there? Low-level auditory-visual integration in autism spectrum disorder. J Autism Dev Disord 37: 2014–2019
Foss-Feig JH, Kwakye LD, Cascio CJ, Burnette CP, Kadivar H, Stone WL, Wallace MT 2010 An extended multisensory temporal binding window in autism spectrum disorders. Exp Brain Res 203: 381–389
Courchesne E, Lincoln AJ, Kilman BA, Galambos R 1985 Event-related brain potential correlates of the processing of novel visual and auditory information in autism. J Autism Dev Disord 15: 55–76
Courchesne E, Lincoln AJ, Yeung-Courchesne R, Elmasian R, Grillon C 1989 Pathophysiologic findings in nonretarded autism and receptive developmental language disorder. J Autism Dev Disord 19: 1–17
Russo N, Foxe JJ, Brandwein AB, Altschuler T, Gomes H, Molholm S 2010 Multisensory processing in children with autism: high-density electrical mapping of auditory-somatosensory integration. Autism Res 3: 253–267
Bebko JM, Weiss JA, Demark JL, Gomez P 2006 Discrimination of temporal synchrony in intermodal events by children with autism and children with developmental disabilities without autism. J Child Psychol Psychiatry 47: 88–98
Williams JH, Massaro DW, Peel NJ, Bosseler A, Suddendorf T 2004 Visual-auditory integration during speech imitation in autism. Res Dev Disabil 25: 559–575
de Gelder B, Vroomen J, van der Heide L 1991 Face recognition and lip-reading in autism. Eur J Cogn Psychol 3: 69–86
Smith EG, Bennetto L 2007 Audiovisual speech integration and lipreading in autism. J Child Psychol Psychiatry 48: 813–821
Iarocci G, Rombough A, Yager J, Weeks DJ, Chua R 2010 Visual influences on speech perception in children with autism. Autism 14: 305–320
Foxe JJ, Molholm S 2009 Ten years at the Multisensory Forum: musings on the evolution of a field. Brain Topogr 21: 149–154
Casanova MF, Buxhoeveden DP, Brown C 2002 Clinical and macroscopic correlates of minicolumnar pathology in autism. J Child Neurol 17: 692–695
Ritvo ER, Freeman BJ, Scheibel AB, Duong T, Robinson H, Guthrie D, Ritvo A 1986 Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC Autopsy Research Report. Am J Psychiatry 143: 862–866
Kern JK 2002 The possible role of the cerebellum in autism/PDD: disruption of a multisensory feedback loop. Med Hypotheses 59: 255–260
di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G 1992 Understanding motor events: a neurophysiological study. Exp Brain Res 91: 176–180
Oberman LM, Ramachandran VS 2008 Preliminary evidence for deficits in multisensory integration in autism spectrum disorders: the mirror neuron hypothesis. Soc Neurosci 3: 348–355
Stein BE, Stanford TR 2008 Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9: 255–266
Hardan AY, Pabalan M, Gupta N, Bansal R, Melhem NM, Fedorov S, Keshavan MS, Minshew NJ 2009 Corpus callosum volume in children with autism. Psychiatry Res 174: 57–61
Coben R, Clarke AR, Hudspeth W, Barry RJ 2008 EEG power and coherence in autistic spectrum disorder. Clin Neurophysiol 119: 1002–1009
Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ 2007 Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex 17: 951–961
Allen G, Courchesne E 2001 Attention function and dysfunction in autism. Front Biosci 6: D105–D119
Talsma D, Senkowski D, Soto-Faraco S, Woldorff MG 2010 The multifaceted interplay between attention and multisensory integration. Trends Cogn Sci 14: 400–410
Posner MI, Petersen SE 1990 The attention system of the human brain. Annu Rev Neurosci 13: 25–42
Gazzaley A, Cooney JW, McEvoy K, Knight RT, D'Esposito M 2005 Top-down enhancement and suppression of the magnitude and speed of neural activity. J Cogn Neurosci 17: 507–517
Berry AS, Zanto TP, Rutman AM, Clapp WC, Gazzaley A 2009 Practice-related improvement in working memory is modulated by changes in processing external interference. J Neurophysiol 102: 1779–1789
Stein BE, Meredith MA 1990 Multisensory integration. Neural and behavioral solutions for dealing with stimuli from different sensory modalities. Ann N Y Acad Sci 608: 51–65; discussion 65 ndash; 70.
Courchesne E, Akshoomoff NA, Townsend J, Saitoh O 1995 A model system for the study of attention and the cerebellum: infantile autism. Electroencephalogr Clin Neurophysiol Suppl 44: 315–325
Näätänen R 1982 Processing negativity: an evoked-potential reflection of selective attention. Psychol Bull 92: 605–640
Ceponiene R, Lepisto T, Shestakova A, Vanhala R, Alku P, Naatanen R, Yaguchi K 2003 Speech-sound-selective auditory impairment in children with autism: they can perceive but do not attend. Proc Natl Acad Sci U S A 100: 5567–5572
Tecchio F, Benassi F, Zappasodi F, Gialloreti LE, Palermo M, Seri S, Rossini PM 2003 Auditory sensory processing in autism: a magnetoencephalographic study. Biol Psychiatry 54: 647–654
Jansson-Verkasalo E, Ceponiene R, Kielinen M, Suominen K, Jantti V, Linna SL, Moilanen I, Naatanen R 2003 Deficient auditory processing in children with Asperger Syndrome, as indexed by event-related potentials. Neurosci Lett 338: 197–200
Oram Cardy JE, Flagg EJ, Roberts W, Roberts TP 2005 Delayed mismatch field for speech and non-speech sounds in children with autism. Neuroreport 16: 521–525
Kasai K, Hashimoto O, Kawakubo Y, Yumoto M, Kamio S, Itoh K, Koshida I, Iwanami A, Nakagome K, Fukuda M, Yamasue H, Yamada H, Abe O, Aoki S, Kato N 2005 Delayed automatic detection of change in speech sounds in adults with autism: a magnetoencephalographic study. Clin Neurophysiol 116: 1655–1664
Gomot M, Blanc R, Clery H, Roux S, Barthelemy C, Bruneau N . Candidate electrophysiological endophenotypes of hyper-reactivity to change in autism. J Autism Dev Disord, [epub ahead of print]
Gomot M, Giard MH, Adrien JL, Barthelemy C, Bruneau N 2002 Hypersensitivity to acoustic change in children with autism: electrophysiological evidence of left frontal cortex dysfunctioning. Psychophysiology 39: 577–584
Gomot M, Bernard FA, Davis MH, Belmonte MK, Ashwin C, Bullmore ET, Baron-Cohen S 2006 Change detection in children with autism: an auditory event-related fMRI study. Neuroimage 29: 475–484
Mottron L, Burack JA, Stauder JE, Robaey P 1999 Perceptual processing among high-functioning persons with autism. J Child Psychol Psychiatry 40: 203–211
Heaton P 2003 Pitch memory, labelling and disembedding in autism. J Child Psychol Psychiatry 44: 543–551
Belmonte MK, Yurgelun-Todd DA 2003 Functional anatomy of impaired selective attention and compensatory processing in autism. Brain Res Cogn Brain Res 17: 651–664
Lepistö T, Kajander M, Vanhala R, Alku P, Huotilainen M, Näätänen R, Kujala T 2008 The perception of invariant speech features in children with autism. Biol Psychol 77: 25–31
Lepistö T, Kujala T, Vanhala R, Alku P, Huotilainen M, Näätänen R 2005 The discrimination of and orienting to speech and non-speech sounds in children with autism. Brain Res 1066: 147–157
Kemner C, Verbaten MN, Cuperus JM, Camfferman G, Van Engeland H 1994 Visual and somatosensory event-related brain potentials in autistic children and three different control groups. Electroencephalogr Clin Neurophysiol 92: 225–237
Polich J 2007 Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118: 2128–2148
Novick B, Kurtzberg D, Vaughn HG Jr 1979 An electrophysiologic indication of defective information storage in childhood autism. Psychiatry Res 1: 101–108
Townsend J, Westerfield M, Leaver E, Makeig S, Jung T, Pierce K, Courchesne E 2001 Event-related brain response abnormalities in autism: evidence for impaired cerebello-frontal spatial attention networks. Brain Res Cogn Brain Res 11: 127–145
Verbaten MN, Roelofs JW, van Engeland H, Kenemans JK, Slangen JL 1991 Abnormal visual event-related potentials of autistic children. J Autism Dev Disord 21: 449–470
Teder-Sälejärvi WA, Pierce KL, Courchesne E, Hillyard SA 2005 Auditory spatial localization and attention deficits in autistic adults. Brain Res Cogn Brain Res 23: 221–234
Ciesielski KT, Knight JE, Prince RJ, Harris RJ, Handmaker SD 1995 Event-related potentials in cross-modal divided attention in autism. Neuropsychologia 33: 225–246
Supported by Grant number K23MH083890 from the National Institute of Mental Health [E.M.].
About this article
Cite this article
Marco, E., Hinkley, L., Hill, S. et al. Sensory Processing in Autism: A Review of Neurophysiologic Findings. Pediatr Res 69, 48–54 (2011). https://doi.org/10.1203/PDR.0b013e3182130c54
Behavioural Brain Research (2020)
ACM Transactions on Human-Robot Interaction (2020)
Neuroscience & Biobehavioral Reviews (2020)
Pediatric Research (2020)
Effects of EEG examination and ABA-therapy on resting-state EEG in children with low-functioning autism
AIMS Neuroscience (2020)