Attentional shifts between audition and vision in Autism Spectrum Disorders

Abstract

Previous evidence on neurotypical adults shows that the presentation of a stimulus allocates the attention to its modality, resulting in faster responses to a subsequent target presented in the same (vs. different) modality. People with Autism Spectrum Disorders (ASDs) often fail to detect a (visual or auditory) target in a stream of stimuli after shifting attention between modalities, possibly because they do not fully switch their attention from one modality to the other. In this study, the performance of a group of high-functioning patients with ASDs and a group of neurotypical controls was compared. Participants were asked to detect a target, auditory or visual, which was preceded, at different temporal intervals (i.e., 150, 600, 1000 ms), by an uninformative cue, either in the same or a different modality. In controls, when the target was visual, the cue modality did not affect performance. Unlike, when the target was auditory, a visual cue produced longer reaction times as compared to when it was auditory. In the ASD group, irrespectively of the modality of the cue, a slowing-down of responses to the target was observed at increasing temporal intervals. The discrepancy of performance is consistent with the ‘over-focused’ theory of sensory processing.

Introduction

The label ‘Autism Spectrum Disorders’ (ASDs) indicates a heterogeneous group of pathologies characterized by behavioural dysfunctions in specific developmental areas, such as social interaction, communication, a restricted range of interests and stereotyped behaviours (DSM-IV; Diagnostic and statistical manual of mental disorders; 4th ed., American Psychiatric Association, 1994). Observational and empirical evidence shows that ASDs are also frequently associated with abnormal response patterns to sensory stimulations (e.g., Kern, 2002, Marco et al., 2011, O’Neill and Jones, 1997, Rogers and Ozonoff, 2005, Wiggins et al., 2009). The sensory processing abnormalities in ASDs, occurring in absence of any disorders in the peripheral nervous system, have been described in all sensory modalities. These can result into various behavioural outcomes such as hyper-responsivity to some stimuli, with subsequent aversive or avoiding reactions (e.g., shutting her/his ears with the hands, ‘sensory defensiveness’; Green et al., 2012, Reynolds and Lane, 2008, Schoen et al., 2009, Van Hulle et al., 2012) or, by contrast, the hypo-responsivity to others (e.g., absence of orienting responses to her/his own name; e.g., Ceponiene et al., 2003, Whitehouse and Bishop, 2008). The prevalence of sensory processing abnormalities in ASDs has been estimated to range between 30 and 100%, although at various degrees of severity (Dawson & Watling, 2000).

The possibility that these dysfunctions extend to the situations where stimulation occurs simultaneously in more than one sensory modality has become the object of increasing research (e.g., Ciesielski et al., 1995, Corbett and Constantine, 2006, Foss-Feig et al., 2010, Reed and McCarthy, 2012). Some of these studies have focused on the investigation of the performance of children and adolescents with ASDs in audiovisual attentional tasks (cf. Courchesne et al., 1994; see Ciesielski et al., 1995 for evidence on adults). The interest in this cognitive function arose from the observation that ASDs are accompanied by both functional and structural cerebellar abnormalities (Kern, 2002), which is a structure involved in a number of different functions, including motor control, attentional orienting, cognitive and sensory processing (see Timmann et al., 2010, for a review). Indeed, in people with ASDs, the decreased number of cerebellar Purkinje cells (Courchesne, 1991) is associated with the hypoplasia of the posterior cerebellar vermis, especially of lobules (Courchesne, 1995, Courchesne et al., 2005, Courchesne et al., 1988), which play a role in modulating sensory inputs from different senses (Parsons & Fox, 1997). Moreover, the cerebellum is connected with brain areas involved in shifting attention, such as brainstem (Kern, 2002), thalamus and parietal lobe (e.g., Posner and Petersen, 1990, Posner et al., 1984).

On the basis of this evidence, Courchesne et al. (1994) tested whether the capability to move the attentional focus from one source of information (e.g., auditory modality) to another (e.g., visual modality) is impaired in ASDs. This process involves the cerebellum, since it requires to rapidly and accurately disengage attention from one source and then move and reengage it on another (e.g., Posner et al., 1984, Posner and Petersen, 1990). In Courchesne et al.’s study, the participants (i.e., patients with ASDs, patients with acquired cerebellar lesions, and chronologic- and mental-age-matched controls) were presented with series of randomly intermingled auditory and visual stimuli and asked to detect rare deviant targets in one of the two sensory modalities. The detection of the target in the attended sensory modality acted as the cue for the participants to shift their attention and detect the target presented in the other sensory modality. The results showed that the performance of the groups of patients with ASDs and neurotypical controls significantly varied as a function of elapsed time since the last correctly detected target. Namely, just as like cerebellar patients, children with ASDs often missed the target when it was presented within 2.5 s after the previous target detection. However, when more time had elapsed (2.5–3.0 s), the performance of the children with ASDs and neurotypical controls did not differ. Overall, these data suggest that the participants with ASDs are less efficient than controls at rapidly and efficaciously shifting attention between sensory modalities (cf. Renner, Grofer Klinger, & Klinger, 2006; see also Lincoln, Lai, & Jones, 2002 for evidence in Williams Syndrome).

It should be noted that some confounds could have possibly biased those results. Firstly, the task used in Courchesne et al.’s study, although aiming to test perceptual processes, also involved higher-order functions, such as the capability of shifting between different tasks and perceptual contests (see also Minshew et al., 1997, Reed and McCarthy, 2012, Yerys et al., 2009). Secondly, in that study the visual stimuli were presented from a central screen, whereas the auditory stimuli were presented from headphones. The necessity of allocating and shifting the attentional resources between two discrepant spatial locations could have made the task particularly demanding to be performed (Driver & Spence, 1998). Moreover, presenting the stimuli from discrepant spatial locations does not allow to disentangle whether the highlighted impaired performance could be due to difficulties in shifting attention across modalities or rather between different spatial positions.

An alternative paradigm that can possibly overcome these pitfalls has been developed by Turatto, Benso, Galfano, and Umiltà (2002). In a series of experiments, Turatto and colleagues explored the attentional shift between visual and auditory modalities in neurotypical adults. The participants were presented with pairs of spatially coincident visual and/or auditory stimuli and, in different tasks, were asked to detect the onset or discriminate the modality of the second stimulus of the pair. They found that the modality of the first stimulus of the pair (S₁) significantly affected the processing of the following stimulus (S₂). More specifically, participants’ performance significantly improved (i.e., the reaction times were shorter) when the two stimuli were presented within the same modality. By contrast, in case of crossmodal pairs, a delay in processing S₂ was observed. Turatto and collaborators explained these results by claiming that S₁ acts as a signal to allocate attention to its sensory modality, thus facilitating the detection/discrimination of ipsimodal S₂; when a shift between modalities is required, more time is necessary to perform the task.

In the present study, the audiovisual attentional shift in children with ASDs and neurotypical controls is tested via a task that is purely perceptual and does not involve either spatial (cf. Casey, Gordon, Mannheim, & Rumsey, 1993) nor emotional (cf. Magnée, de Gelder, van Engeland, & Kemner, 2011) or linguistic (Ceponiene et al., 2003, Whitehouse and Bishop, 2008) factors. In order to make the task more feasible and thus increase the compliance of our participants, the sensory modality of the target (S₂) was kept constant in each task (cf. Turatto et al., 2002; Experiment 4). The group of neurotypical controls is expected to have a performance comparable with that of adults (cf. Turatto et al., 2002; Experiment 4). Namely, the detection of the target would be facilitated in the congruent condition, where the cue is presented in the same modality as S₂, as compared to when S₂ is preceded by a crossmodal S₁ (i.e., incongruent condition). By contrast, if the impairment in shifting attention between sensory modalities of patients with ASDs would be confirmed, then it is expected that this group of participants would show a higher impairment in the incongruent (vs. congruent) condition.