Intact Spectral but Abnormal Temporal Processing o

Authors: Wouter B Groen Linda van Orsouw Niels ter Huurne Sophie Swinkels RutgerJan van der Gaag Jan K Buitelaar Marcel P Zwiers

Publish Date: 2009/01/16

Volume: 39, Issue: 5, Pages: 742-750

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Abstract

The perceptual pattern in autism has been related to either a specific localized processing deficit or a pathwayindependent complexityspecific anomaly We examined auditory perception in autism using an auditory disembedding task that required spectral and temporal integration 23 children with highfunctioningautism and 23 matched controls participated Participants were presented with twosyllable words embedded in various auditory backgrounds pink noise moving ripple amplitudemodulated pink noise amplitudemodulated moving ripple to assess speechinnoisereception thresholds The gain in signal perception of pink noise with temporal dips relative to pink noise without temporal dips was smaller in children with autism p = 0008 Thus the autism group was less able to integrate auditory information present in temporal dips in background sound supporting the complexityspecific perceptual accountSeveral studies have found abnormal lowlevel perceptual capabilities in autism in the visual Bertone et al 2005 Behrmann et al 2006 and auditory domains Samson et al 2006 Atypical processing of lowlevel ie early perceptual information processing is therefore considered to be a characteristic feature of autism Happe 1999 It is however not clear which processes give rise to the atypical perceptual processing Two opposing hypotheses on perception in the visual domain have been formulated Bertone et al 2005 the pathwayspecific hypothesis and the complexityspecific hypothesis The distinction between these two theories has important conceptual consequences for the inferred organisation of the autistic brain since essentially the pathwayspecific hypothesis states that perceptual deficits in autism can be traced back to deficits in specific cortical modules whereas the complexityspecific hypothesis states that general integrational functional processes that are not bound to specific cortical modules are atypical in autismThe finding that people with autism were less sensitive to global motion than to static visual stimuli inspired the pathwayspecific hypothesis which states that the autistic brain has a deficient dorsal visual motion information processing stream but an intact ventral visual static information processing stream Blake et al 2003 Spencer et al 2000 Milne et al 2002 However a recent study found ventral stream deficits in autism as well Bertone et al 2005 Bertone et al found that people with autism showed an enhanced sensitivity to the orientation of static luminancedefined stimuli that require V1 processing only while the static texturedefined stimuli that require additional V2/V3 processing were diminished They therefore concluded that rather than the neural pathway the amount of neural integrative processing required for the task relative to the hierarchical posterior–anterior organisation of the visual cortex predicted perceptual performance in autismSeveral authors have suggested that the complexityspecific hypothesis also applies to the auditory domain Bertone et al 2005 Samson et al 2006 Mottron et al 2006 Mottron and colleagues’ Enhanced Perceptual Functioning model EPF Mottron et al 2006 states that there is an inverse relation between increasing levels of neural complexity and the level of performance in lowlevel perceptual tasks in autism independent of the sensory domain thus providing an explanation for both enhanced and diminished perceptual functioning in autism More specifically Samson et al hypothesised that based on the hierarchical neural organisation of the auditory cortex spectrotemporal complexity of auditory stimuli may explain the autistic pattern of performance in the auditory domain such that perception of simple lowlevel auditory stimuli will be enhanced in autism while perception of complex lowlevel auditory stimuli will be spared or impaired Samson et al 2006Given the hypothesis of the EPF model we sought to create an auditory task that required neural integration of stimuli in the hierarchical and systemwide tonotopic organisation of the auditory system The hierarchical organisation is reflected by the fact that spectral and temporal cues are processed separately in early subcortical parts of the auditory pathway and that these are progressively integrated from the midbrain inferior colliculus to primary A1 and secondary nonA1 auditory cortex A2 where the spectral and temporal response characteristics are most complex and broadly tuned The tonotopic spectral organisation refers to neighbouring neural assemblies responding to similar frequencies such that orderly maps are formed with lowest frequency on one end and highest frequency on the other It is implied naturally from this organisation that shortrange lateral connections mediate integration or segregation of spectral information from simple sounds such as pure tones The processing of more complex sounds such as noise or speech involves larger neural assemblies Scott and Johnsrude 2003 and moreover segregating different simultaneously presented sounds sources requires reallocation of additional supporting neural processing resources PichoraFuller et al 1995 Also the auditory system has a hemispheric lateralisation The left auditory cortex is more involved in the perception of temporal information whereas the right auditory cortex is committed to spectral processing Robin et al 1990 Zatorre 1997According to the hierarchical neural organisation of the auditory pathway pitch identification of pure tones is the simplest task that requires least neurointegrative processing and is mediated more by A1 than by A2 The EPF model predicts that A1mediated perceptual processing will be superior in autism Indeed superior loworder auditory perception has been reported in experimental paradigms involving pitch perception Bonnel et al 2003 and chord segmentation Heaton 2003 However few studies assessing complex lowlevel perceptual tasks in the auditory domain that require extensive neural integration have yet been conducted TederSalejarvi et al 2005 Alcantara et al 2004 One study by Alcantara et al 2004 pioneered research on complex lowlevel auditory information processing studying speechinnoise perception in autism Using several types of noise that contained either spectral dips temporal dips or a mixture of both they found significant differences between the control and subject groups in the ability to disembed speech from noise which were mainly attributable to the temporal dips in the noise These results are suggestive of diminished complex loworder auditory perception in autism but two disadvantages make inferences on the predictions of the EPF model rather difficult First the noise stimuli were designed to mimic naturalistic speech the temporal dips in the noise therefore varied from seconds to milliseconds and were consequently not well controlled Second the wholesentence material impeded differentiation between languagemediated topdown influences higher linguistic ability in the control group may lead to better sentence recognition and bottomup perceptual effects as predicted by the EPF modelTo assess complex lowlevel auditory perceptual functioning in autism we extended Alcantara and colleagues’ speechinnoise perception task by a controlling for languagemediated topdown influences and b by using welldefined background stimuli In random dot kinematograms isolated processing of single dots is not sufficient to perceive global motion since local information fragments must be integrated across time and space before a global motion direction can be discriminated Similarly we presented participants with single words and concurrent masking background stimuli in which the background stimuli were fragmented both temporally and spectrally to vary the neural demand needed to integrate information present in spectral and temporal dips Based on the predictions of the EPF model we hypothesised that with increasing neurointegrative demand task performance in autism would decrease such that enhanced speech perception in a simple lowlevel auditory task is met by normal or decreased complex lowlevel perceptual performance in the auditory domain More specifically we hypothesised that the participants with autism would show a preserved or reduced rather than an enhanced to integrate information present in temporal and spectral dips in the background sounds

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