© Springer International Publishing Switzerland 2015
Maria de los Angeles Robinson-Agramonte (ed.)Translational Approaches to Autism Spectrum Disorder10.1007/978-3-319-16321-5_55. Autism Spectrum Disorder. A Clinical Neurophysiology Approach II
(1)
International Center for Neurological Restoration (CIREN), Clinical Neurophysiology Service, Havana, Cuba
Abstract
One of the most controversial issues in the study of autism spectrum disorder (ASD) is the involvement and dysfunction of sensory systems that underlie atypical behaviors, which could be evaluated through neuroimaging and electrophysiological techniques. Auditory disturbances are the most frequently reported sensory deficits that could explain language and communication deficits shown in ASD patients. Event-related potentials such as auditory brainstem response, mismatch negativity, P50, and P300 have shown differences between patients and normal subjects, supporting the existence of an abnormal auditory processing. Somesthetic perception is also distorted in this heterogeneous group of patients, probably associated with deficits in communication, motor ability, and social skills. It has been confirmed by abnormalities in short- and long-latency somatosensory evoked potentials. Visual processing impairment has also been described in children and young adults with autism. Dipole source analysis revealed that the visual cortex, fusiform gyrus, and medial prefrontal lobe are less active in autism compared with control subjects during the execution of emotion processing tasks. ASD patients also have problems to integrate information from multiple sensory sources necessary to a successful social behavior, and consequently, they show deficits with social and cognitive processes. Electrophysiological and imaging techniques may constitute useful tools in the diagnosis, classification, and therapeutic strategies of ASD patients, considering the diversity of this spectrum.
Keywords
Auditory brainstem responseAutism spectrum disorderMiddle latency responseSensory integrationSomatosensory evoked responseSomesthetic perceptionVisual perceptionAbbreviations
ABR
Auditory brainstem response
AD/HD
Attention deficit/hyperactivity disorder
ASD
Autism spectrum disorder
MLR
Middle latency response
MRI
Magnetic resonance imaging
PDD
Pervasive development disorder
S-SEPs
Short-latency somatosensory evoked potentials.
TEOAEs
Transient evoked otoacoustic emissions
5.1 Introduction
Autism spectrum disorder (ASD) refers to a group of disorders including autistic disorder, Asperger’s disorder, and pervasive developmental disorder (American Psychiatric Association 2013).
One of the most controversial issues in the study of ASD is the involvement and dysfunction of sensory systems that underlie atypical behaviors.
In an extensive review of the literature published in 2008 (1300 reports), Hughes summarizes this contradiction finding equally a low and high frequency of sensory symptoms in patients with autism, and hyper- or hypofunctioning of the sensory systems (Hughes 2009).
Techniques like electroencephalography (EEG), magnetoencephalography (MEG), and functional Magnetic Resonance Imaging (fMRI) have demonstrated their utility to evaluate unimodal sensory processing and multisensory integration (Marco et al. 2011). Neurophysiological responses to auditory, tactile, and visual stimuli in autistic patients have been studied to explain the neural bases of the atypical behaviors previously mentioned (Marco et al. 2011). Other sensory processing deficits, including olfactory and gustatory, have been also described in children with ASD (Tomchek and Dunn 2007; Bennetto et al. 2007).
This chapter aims to summarize the electrophysiological and imaging evidences published in the past years that support the existence of sensory deficits in ASD patients.
5.2 Auditory Perception
Disturbances in auditory processing are the most frequently reported sensory deficits in patients with ASD. In fact, children with autism show a major impairment during the processing of auditory and verbal information compared with visual information (Duncan et al. 2009).
The main trends point out the disturbances of auditory perception of linguistic and social auditory stimulus, and enhanced perception of pitch and music. These discordant findings in auditory abnormality reported in ASD might be the consequence of differences between global and local processing of auditory information occurring in these patients (Kellerman et al. 2005).
Diverse studies in ASD have been designed to test the integrity of the auditory pathway using electrophysiological techniques, such as auditory brainstem response (ABR), but the results are not coincident. In consequence, some authors state that these studies do not support the involvement of brainstem in autism, despite the presence of peripheral hearing impairment in a nonnegligible number of autistic subjects (Klin 1993). For example, Novick et al. show that abnormalities in the brainstem are scarce in patients with ASD using evoked potentials to clicks, pitch changes, and tones. These authors suggest that the registration and storage of stimulus information in the higher levels of processing are more engaged, and they could explain the severe language disorders in ASD (Novick et al. 1980).
Most reports support the hypothesis of impairment in the brainstem auditory pathway to explain the disturbances in auditory processing demonstrated in ASD subjects (Kwon et al. 2007; Magliaro et al. 2010; Maziade et al. 2000; Tas et al. 2007).
The objective evaluation of hearing in a group of children with ASD was carried out by Taset et al. (2007) using transient evoked otoacoustic emissions (TEOAEs) and ABR. Both these techniques were obtained in the majority of ASD children bilaterally (83.3 %), while the remaining cases showed an increase in duration of III–V interpeak latency compared with a control group (Tas et al. 2007). Similar results were reported by Kwon et al. (2007) studying 121 autistic children compared with a control group. They reported a prolonged latency of wave V, and an increase in duration of III–V interpeak interval in the ASD group, suggesting a dysfunction or immaturity of the central auditory pathway, particularly at the level of mesencephalon (Kwon et al. 2007).
Autistic patients and unaffected first degree relatives showed the prolongation of I–III interpeak interval of ABR in relation to control subjects. So, this finding could be proposed as an endophenotype of the disease (Maziade et al. 2000).
The auditory abnormalities mentioned could contribute to sensory deprivation and consequently to communication deficits. Furthermore, aberrations in the perception and processing of the audiological stimuli, like maturational defects and atypical lateralization, has been proposed (Hitoglou et al. 2010).
Other techniques have been used to assess hearing in autistic subjects: pure tone and speech audiometry, acoustic immitance measures, ABR, auditory middle latency response (MLR), and cognitive potential (P300). All auditory evoked potentials showed differences with respect to a group of normal subjects. Particularly, statistically significant differences between groups were observed in the latency of waves III and V, and in the duration of interpeak intervals I–III and I–V of ABR, confirming the impairment of the brainstem auditory pathway. The absence of P300 component suggests the dysfunction of cortical areas in the same patients (Magliaro et al. 2010).
Abnormal auditory symptoms include peripheral and sensorineural hearing deficit, both hypo- and hypersensitivity to auditory stimulation with bizarre reactions to sounds, and limitations to filter relevant auditory information in the presence of environmental background noise (Källstrand et al. 2010). Khalfa et al. explained that difficulty in filtering information presupposes the participation of active cochlear mechanisms regulated by the efferent olivocochlear system and evaluated with TEOAEs. The abnormalities in lateralization at the auditory periphery observed in ASD patients are probably related to dysfunction at higher levels of the auditory processing mediated by the medial olivocochlear system (Khalfa et al. 2001).
Limitations to filter auditory information in a noisy background also include speech. Evidence of this was provided by Russo et al., evaluating speech-evoked responses in quiet and noise background in ASD patients and typically developing children. Differences between quiet and noise responses were minimal in ASD children, probably related to a severe depression of the responses in a noise background (Russo et al. 2009).
On the contrary, other authors reported that nonmentally retarded children with autism had a sensory gating to auditory stimulus similar to a control group using the P50 gating paradigm (Kemner et al. 2002). All these apparent differences in published papers are probably related to the nature of the auditory stimuli used.
Another aspect that has to be taken into account is the automatic and active processing of auditory stimuli evaluated with the mismatch negativity. The amplitude of this event-related potential is smaller in autistic than in normal children in unattended conditions. On the other hand, when the stimuli are attended the differences between groups disappear. All these results confirmed the existence of an abnormal automatic auditory processing in autism (Dunn et al. 2008).
Larger P300 component to target auditory stimuli has been also found in autistic children during active conditions with respect to healthy, dyslexic, and attention deficit/hyperactivity disorder (AD/HD) groups, while other authors found larger P300a in younger children with respect to older (Hughes 2009).
An interesting finding reported by Lai et al. in low-functional autistic patients showed that functional systems which process speech and song are more related to the last one. Some structures, like the left inferior frontal gyrus, are more activated during song stimulation and less with speech stimulation in autistic patients compared with control normal subjects. Measures like functional connectivity between this gyrus and superior temporal gyrus was increased for songs compared to speech in patients. At the same time, there were increased frontal-posterior connections. These and other findings of this study support the assumption that functional systems related to speech and song are more active for song in this subgroup of autistic patients (Lai et al. 2012).
Deficits in communication in ASD patients include a variety of disturbances in language, ranging from semantic-pragmatic deficits to the absence of speech. But these problems are probably dependent, at least in part, on auditory aberrant perception (Kujala et al. 2013).
Deficient prosody, for example, is a distinguishing characteristic of the language impairment in ASD patients related to acoustic cues such as pitch contour. The sensory encoding of pitch was evaluated by evoked brainstem responses to pitch syllables in a group of ASD patients with normal intelligence and hearing, some of them showed deficient pitch tracking compared with normal children. Obviously, there is a subcortical origin of prosody encoding deficits demonstrated by electrophysiological techniques. This should be taken into account in the diagnosis and treatment of this subgroup of ASD patients (Russo et al. 2008).
Of course, ASD include a wide spectrum of entities with a diversity of responses. Matas et al. studied the audiological and electrophysiological profile of patients with autism and Asperger syndrome, and compared their results with a group of normal subjects. They did not find abnormalities in the audiological evaluation in all subjects, but 50 % of patients with autism and 30 % with Asperger syndrome showed ABR alterations, with statistically significant differences between groups. Auditory MLR presented abnormalities in all groups without differences between them, while P300 component showed differences between Asperger patients and control subjects. These results suggest that auditory information processing at different levels of the pathway has specific profiles in the diverse forms of the disease (Matas et al. 2009).
Other authors have found normal hearing levels in high-functioning autistic children with a pervasive development disorder (PDD) and speech delay (Psillas et al. 2006).
Bruneau et al. demonstrated in a group of mentally retarded children with ASD the existence of electroclinical correlations between the amplitude of the right temporal N1 cortical response and the verbal and nonverbal communication abilities, suggesting a reorganization of the hemisphere functions, with a greater activation of the right hemisphere for functions that correspond to the left one. This especially was true for the lateral aspect of the superior temporal gyrus which belongs to secondary auditory areas (Bruneau et al. 2003).
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