Elsevier

Brain Research

Volume 1302, 20 November 2009, Pages 132-147
Brain Research

Research Report
Auditory and visual stream segregation in children and adults: An assessment of the amodality assumption of the ‘sluggish attentional shifting’ theory of dyslexia

https://doi.org/10.1016/j.brainres.2009.07.037Get rights and content

Abstract

Among the hypotheses relating dyslexia to a temporal processing disorder, Hari and Renvall (Hari, R., Renvall, H., 2001. Impaired processing of rapid stimulus sequences in dyslexia. Trends. Cognit. Sci. 5, 525–532.) argued that dyslexic individuals would show difficulties at an attentional level, through sluggish attentional shifting (SAS) in all sensory modalities. However, the amodality assumption of the SAS theory was never straightforwardly assessed in the same group of dyslexic participants using similar paradigms in both the visual and auditory modalities. Here, the attentional sequential performance of control and dyslexic participants was evaluated using rapid serial presentation paradigms measuring individual stream segregation thresholds in the two modalities. The first experiment conducted on French dyslexic children with a phonological disorder revealed an SAS only in the auditory modality only which was strongly related to reading performance. The second experiment carried out on British dyslexic young adults with a phonological disorder using the same auditory segregation task but a different visual paradigm revealed an SAS in both the visual and the auditory modalities. In addition, a relationship was found in this group between SAS, poor reading and poor phonological skills. Two further control experiments showed that differences in task design or participants' language between Experiments 1 and 2 could not account for the differences in terms of visual segregation patterns. Overall, our results support the view that the auditory SAS plays a role in developmental dyslexia via its impact on phonological abilities. In addition, a visual temporal disorder in dyslexia might emerge at a later developmental stage, when the visual system normally becomes more expert at rapid temporal processing.

Introduction

Developmental dyslexia is a severe and persistent disorder of reading acquisition which occurs in individuals who have at least average intelligence, exhibit no basic sensory deficit and benefit from adequate educational opportunities. Given that it is considered the most common neurobehavioural disorder affecting children (Shaywitz and Shaywitz, 2005), many studies aimed to identify the cognitive, neurobiological and genetic origin of developmental dyslexia. At the cognitive level, the hypothesis of an auditory or visual processing disorder has been widely investigated. However the scale of auditory and visual impairments in dyslexia being very broad, it is barely impossible to circumscribe dyslexia to a restricted set of visual and/or auditory deficits.

The most documented and most widely accepted cognitive theory of developmental dyslexia is the phonological theory (Goswami, 2000, Ramus and Szenkovits, 2008, Snowling, 1980, Snowling, 1981). For several decades, evidence has been provided supporting the view that the core deficit in dyslexia stems from difficulties in the representation (see however, Ramus and Szenkovits, 2008) and use of phonological information, thus resulting in poor phoneme awareness i.e., in the inability to identify and manipulate the sound units (i.e., phonemes) of words (see Vellutino et al., 2004 for a review). This would lead to difficulties in acquiring the “grapheme-to-phoneme” relationships involved in reading by decoding. Several studies nevertheless assumed that a more basic deficit could lead to the phonological impairment in developmental dyslexia (Farmer and Klein, 1995, Tallal, 1980).

Tallal (1980) claimed that a reading disorder could result from a perceptual deficit in processing rapid temporal auditory sequences. Within this framework, abnormal phonological representations in poor readers would stem from the incapacity to encode properly the crucial acoustic and temporal features present in rapid auditory streams, which are typical in speech (Ahissar et al., 2000, Hari and Kiesilä, 1996, Helenius et al., 1999). These perceptual difficulties in processing rapid sequences of stimuli spread to the visual domain as well (Conlon et al., 2004, Eden et al., 1996, Lassus-Sangosse et al., 2008). Farmer and Klein (1995) reviewed studies of non-reading task revealing a visual or an auditory processing deficit in dyslexic individuals. They proposed a general temporal (or sequential) processing deficit as the cause of the reading impairment. Nevertheless, their theory was not well received by some of their peers, who argued that the nature of this temporal processing deficit is not clearly defined (Rayner et al., 1995). Indeed, Farmer and Klein (1995) included in their review several different types of temporal deficits, such as those described in the magnocellular theory of dyslexia in which temporal processing impairment is considered as affecting the dynamic aspect of stimuli, such as online physical changes inside one particular stimulus. In fact, the magnocellular theory of dyslexia was the first neurobiological explicative model attempting to unify the behavioural visual and auditory sequential impairments found in dyslexic individuals (Stein, 2001, Stein and Walsh, 1997). The theoretical roots of this hypothesis were first grounded in findings in the visual modality (Livingstone et al., 1991). Similar low-level disorders were further reported in the auditory domain (Galburda et al., 1994, Stein and Talcott, 1999, Stein and Walsh, 1997), thus resulting in the amodal version of the theory, according to which both visual and auditory magnocellular systems would be affected in the dyslexic population (Stein, 2003, Stein and Walsh, 1997). The theory thus accounts for both the visual and auditory low-level processing deficits in developmental dyslexia, with the latter somehow related to the phonological impairment.

However, the validity of the magnocellular deficit hypothesis has been hotly debated (see Skottun, 2000 for a review). When assessing the theory with specific magnocellular psychophysical paradigms, many studies failed to find evidence in support of the magnocellular theory (Amitay et al., 2002, Ben-Yehudah and Ahissar, 2004, Ram-Tsur et al., 2006, Ramus, 2003, Roach and Hogben, 2004). For example, when controlling stimulus presentation type (e.g. sequential vs. simultaneous), Ben-Yehudah and Ahissar (2004) found that the temporal structure of the behavioural paradigm was more crucial than the magnocellular nature of the stimuli (i.e. high temporal and low spatial frequencies) to discriminate control and dyslexic groups. Then, several studies suggested that deficits in attentional processing related to a parietal dysfunction might be responsible for the temporal perceptual deficits in either the visual (Facoetti et al., 2008, Pammer et al., 2006; Pammer et al., 2005; Vidyasagar, 2001, Vidyasagar and Pammer, 1999) or the auditory modality (Kujala et al., 2006, Loveless and Koivikko, 2000) in developmental dyslexia.

Hari and Renvall (2001) introduced a novel theoretical framework which ascribes a causal role to abnormal parietal activity to account for the amodal temporal impairment responsible for developmental dyslexia. They suggested that the temporal deficit in developmental dyslexia may be held up by a neurobiological dysfunction (parietal), which might result in sluggish attentional shifting (SAS) at the cognitive level. It is worth noting that the parietal disorder here assumed relates to higher-level perceptual attentional factors rather than low-level basic perceptual ones (i.e. revealed by motion or frequency detection tasks). According to the SAS theory, when dyslexic individuals have to process rapid stimuli sequences, their automatic attention system cannot disengage fast enough from an item to the following one, yielding degraded processing. The nature of the temporal deficit would then be defined as sequential.

Sluggish perceptual sequential integration in dyslexia was first described in the auditory modality (Cutting and Pisoni, 1978, Hari and Kiesilä, 1996, Helenius et al., 1999, Loveless and Koivikko, 2000). This disorder would be caused by a prolonged attentional dwell time (Hari et al., 1999) yielding dysfunction of cortical networks, in particular the auditory ones, housing phonological representations. Nevertheless, the parietal lobe is known to be involved in amodal attentional processing since it receives information from both the visual and the auditory sensory systems (see Pammer and Vidyasagar, 2005 for a review). Thus in the framework of the SAS theory, the phonological deficit in developmental dyslexia would be the consequence of a perceptual attentional auditory deficit but all other sensory modalities would further be affected. A number of data support the hypothesis of a relationship between auditory attention and phonological processing in developmental dyslexia (Facoetti et al., 2005, Facoetti et al., 2003b, Lallier et al., in press, Pammer and Vidyasagar, 2005). Other studies provided evidence for an attentional disorder which could affect visual or auditory processing in developmental dyslexia but only a few studies showed that both modalities are affected in the same participants.

Indeed, reviewing studies using tasks which engage attentional shifting in either the visual or the auditory domain, Hari and Renvall (2001) argued that dyslexic participants suffered from SAS in both modalities. However, they concluded to an amodal disorder on the basis of evidence from different modality-specific experimental paradigms and from different groups of dyslexic participants (Hari and Kiesilä, 1996, Hari and Renvall, 2001, Hari et al., 1999, Helenius et al., 1999). Obviously, such a claim would require demonstrating that the same dyslexic individuals are impaired in the two modalities (visual and auditory) on tasks using similar procedures. Several studies have assessed the amodal perceptual deficit hypothesis with similar paradigms between modalities, in children (Edwards et al., 2004, King et al., 2008, Laasonen et al., 2001, Van Ingelghem et al., 2001) and in young adults (Breznitz and Meyler, 2003, Laasonen et al., 2001, Meyler and Breznitz, 2005, Witton et al., 1998) with developmental dyslexia. However, some of these studies focused on mechanisms associated with the magnocellular pathway such as rapid temporal and low spatial frequency processing (Heim et al., 2001, Van Ingelghem et al., 2001, Witton et al., 1998). Those which specifically assessed sequential processing (Laasonen et al., 2000, Laasonen et al., 2001, Meyler and Breznitz, 2005) did not explicitly investigate the attentional disorder hypothesised by the SAS theory (see the review of Hari and Renvall, 2001). Overall, the results of these set of studies have led to discrepancies. Some studies concluded that the temporal disorder was specific to the auditory modality (Heim et al., 2001, Laasonen et al., 2001, Reed, 1989), some showed that it rather extended over modalities (King et al., 2008, Meyler and Breznitz, 2005; Van Ingelghem et al., 2001), while others failed to show any temporal deficit within modalities in developmental dyslexia (Laasonen et al., 2000). Despite these inconsistent results, studies in normally developing children have shown that amodal temporal processing skills relate to reading and spelling performance and account for a significant part of variance in reading (Talcott et al., 2002, Talcott et al., 2000, Walker et al., 2006). Further, it has been shown that amodal temporal skills assessed in pre-school children are good predictors of reading performance one year later in Grade 1 (Boets et al., 2008, Hood and Conlon, 2004).

Two studies directly addressed the amodality hypothesis of the SAS theory by testing dyslexic participants on similar tasks in different sensory modalities. Using the same lateralized cued detection task paradigm in vision and audition, Facoetti et al. (2005) varied the inter-stimulus interval between the cue and target stimuli to determine the speed at which dyslexic and control children could disengage their automatic attentional focus and exhibit attentional facilitation. The results showed that dyslexic participants only exhibited attentional facilitation at the longer intervals whereas attentional facilitation was only found at the shorter intervals in the control participants. In this study however, the modality effect was not significant thus suggesting that dyslexic children suffered from sluggish visual and auditory attentional captures. Lallier et al. (in press) have also provided evidence for amodal SAS through in a single case study of a young adult with phonological dyslexia using the same attentional blink paradigms in vision and audition. In the current study, we aimed at showing evidence for SAS in the visual and the auditory modalities in groups of dyslexic children and adults with a phonological disorder. We also wanted to investigate temporal attentional performance in children with less severe delays (i.e. in a large sample of unselected children within the same age range). Since better temporal skills have been found to be associated with better reading skills in normal readers (Au and Lovegrove, 2001b, Walker et al., 2006), we will determine the extent to which dyslexia may represent the lower end of a continuum of temporal processing abilities.

The present study aims at providing further evidence for the amodality hypothesis of the SAS theory using a stream segregation task in the visual and auditory modalities. The phenomenon of stream segregation can be observed in the two modalities. In the auditory modality (Bey and McAdams, 2003), stream segregation can occur when sequences of auditory stimuli alternate in frequency (e.g. high and low pitch tones). In the visual modality (Bregman and Achim, 1973), segregation occurs when sequences of visual stimuli alternate in space location (e.g. visual dots appearing above and below fixation). The resulting percept depends on both temporal and auditory frequency/visual distance intervals between two successive stimuli (Van Noorden, 1975). For adequate auditory frequency/visual distance intervals, two perceptual temporal patterns can occur: when the time interval is long enough, a unique auditory stream alternating high and low pitch tones – or a unique visual object – is perceived. On the contrary, for short enough intervals, the participant perceives two different auditory streams, one high- and the other low-pitched, or two visual objects, in parallel.

Three studies have already assessed auditory stream segregation in developmental dyslexia. Although two of these investigated auditory frequency in stream segregation (Sutter et al., 2000, Taylor et al., 2003), only the third focused on temporal features (Helenius et al., 1999). Auditory stream segregation thresholds were found to be higher in dyslexic adults than controls: in other words, at a point where dyslexic participants could segregate the two streams accurately control participants still perceived a single stream. The authors concluded that the perceptual integration time window may be extended in dyslexic individuals. This would lead to interference between the previous- and current-occurring sounds, yielding degraded temporal processing. Helenius et al. (1999) argued that this interference would prevent efficient processing of critical salient phonological features in speech, which in turn would prevent adequate phonological representation build-up. Hari and Renvall (2001) assume that the perception of one stream reflects the speed at which automatic attention can disengage from a stimulus to process a rapidly successive one. As long as one stream is perceived, automatic attentional resources are orienting the focus online to capture every single stimulus of the sequence. Thus, one would expect the segregation of one stream into two different streams to occur when automatic attentional focus is no longer able to shift fast enough from one stimulus to the other.

The examination of perceptual segregation (or fusion) skills in dyslexia was not confined to the auditory modality. In the visual domain and by reference to the visual magnocellular theory (Stein and Walsh, 1997), a number of studies assessed apparent motion in dyslexia within the processing of rapid stimulus sequences via the Ternus display (see Skottun, 2000 for a review). Ternus stimuli lead to two mutually exclusive visual perceptual patterns, as in visual stream segregation. At long intervals, the elements in the Ternus display are perceived as moving together as a whole (‘group movement’), while at shorter intervals only one element appears to be moving (‘element movement’). However, results were inconsistent: some authors found that dyslexic participants were impaired in the task (Cestnick and Coltheart, 1999, Slaghuis et al., 1996) but others did not (Davis et al., 2001). Finally, the Finnish team of Laasonen investigated visual, auditory and tactile segregation rate with temporal processing acuity tasks in dyslexic children (Laasonen et al., 2001) and young adults (Laasonen et al., 2001). When the task was administered to children, the authors failed to demonstrate any difference between groups in visual and auditory segregation thresholds. In adults, although dyslexic participants reached the threshold at longer intervals than the controls in the auditory modality, the auditory performance of the two groups largely overlapped.

The auditory stream segregation task of Helenius et al. (1999) was used to assess the SAS theory of dyslexia, because results on this task were interpreted by Hari and Renvall (2001) themselves as evidence for the SAS theory. A similar visual stream segregation task was further designed. Both tasks were administered to a group of French dyslexic children with phonological impairments in Experiment 1. Their performance was compared with that of two groups of chronological-age-matched good and poor readers in order to determine whether rapid sequential attentional skills played a role in both mild and severe reading difficulties. Stream segregation thresholds were measured in each population and the link between each modality-specific segregation threshold and reading achievement was investigated in the whole population. British young adults with developmental dyslexia were assessed in Experiment 2. They were given the same auditory segregation task but a modified version of the visual task. The relations between segregation thresholds, reading and spelling skills were explored in these older participants as well as the critical link between phonological skills and amodal attentional shifting when controlling for the effects of age and non-verbal IQ. Lastly, two additional control experiments were carried out to determine whether the observed differences in visual segregation thresholds between Experiment 1 and Experiment 2 could be due to differences in task designs or in participants' language (French vs. English).

Section snippets

Experiment 1

As shown in Table 1, the three groups did not differ significantly in chronological age (CA) (for all comparisons, ps > .05). However, the dyslexic group showed a lower reading age (RA) than the two non-dyslexic groups and RA was lower in poor than in good readers (for all comparisons, ps < .001).

Discussion

The present study aimed at testing the amodality assumption of the SAS theory in both the visual and the auditory domains, using the same participants and similar experimental paradigms in the two sensory modalities. The theory assumes that dyslexic individuals should exhibit sluggish automatic attentional shifting in both modalities. This disorder would impair the build-up of phonological representations and the acquisition of grapheme-to-phoneme mappings.

Conclusion

In the present research, the amodality assumption of the SAS theory and the relation between SAS, reading/spelling and phonological awareness were assessed in the same participants using experimental paradigms as similar as possible between sensory modalities. The results suggest that whatever their age, dyslexic individuals with a phonological disorder suffer from sluggish auditory attentional shifting. In support of the amodality assumption, a visual SAS was found in adults. However, this

Participants

Thirty-six French children took part in Experiment 1: 12 dyslexic children (6 boys; 3 in Grade 3, 4 in Grade 4, and 5 in Grade 53), 12 chronological age matched good readers (5 boys; Grade 5) and 12 chronological age-matched poor readers

Acknowledgments

This research was supported by the CNRS (Centre National de la Recherche Scientifique) and by the University Pierre Mendès France (“Indoc” grant obtained in 2007). Marie Lallier is chercheur-boursier of the French Research Ministry. We thank all the dyslexic and the control participants for their help and participation in this research.

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