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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen20
Visual attention shifting in autism spectrum disorders a
a
Annette E. Richard & Renee Lajiness-O’Neill a
Department of Psychology, Science Complex, Eastern Michigan University, Ypsilanti, MI, USA Published online: 09 Jul 2015.
Click for updates To cite this article: Annette E. Richard & Renee Lajiness-O’Neill (2015): Visual attention shifting in autism spectrum disorders, Journal of Clinical and Experimental Neuropsychology, DOI: 10.1080/13803395.2015.1042838 To link to this article: http://dx.doi.org/10.1080/13803395.2015.1042838
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
Journal of Clinical and Experimental Neuropsychology, 2015 http://dx.doi.org/10.1080/13803395.2015.1042838
Visual attention shifting in autism spectrum disorders Annette E. Richard
and Renee Lajiness-O’Neill
Department of Psychology, Science Complex, Eastern Michigan University, Ypsilanti, MI, USA
Downloaded by [University of Otago] at 08:22 20 July 2015
(Received 23 September 2014; accepted 15 April 2015) Introduction: Abnormal visual attention has been frequently observed in autism spectrum disorders (ASD). Abnormal shifting of visual attention is related to abnormal development of social cognition and has been identified as a key neuropsychological finding in ASD. Better characterizing attention shifting in ASD and its relationship with social functioning may help to identify new targets for intervention and improving social communication in these disorders. Thus, the current study investigated deficits in attention shifting in ASD as well as relationships between attention shifting and social communication in ASD and neurotypicals (NT). Method: To investigate deficits in visual attention shifting in ASD, 20 ASD and 20 age- and gender-matched NT completed visual search (VS) and Navon tasks with attention-shifting demands as well as a set-shifting task. VS was a feature search task with targets defined in one of two dimensions; Navon required identification of a target letter presented at the global or local level. Psychomotor and processing speed were entered as covariates. Relationships between visual attention shifting, set shifting, and social functioning were also examined. Results: ASD and NT showed comparable costs of shifting attention. However, psychomotor and processing speed were slower in ASD than in NT, and psychomotor and processing speed were positively correlated with attention-shifting costs on Navon and VS, respectively, for both groups. Attention shifting on VS and Navon were correlated among NT, while attention shifting on Navon was correlated with set shifting among ASD. Attentionshifting costs on Navon were positively correlated with restricted and repetitive behaviors among ASD. Conclusions: Relationships between attention shifting and psychomotor and processing speed, as well as relationships between measures of different aspects of visual attention shifting, suggest inefficient top-down influences over preattentive visual processing in ASD. Inefficient attention shifting may be related to restricted and repetitive behaviors in these disorders. Keywords: Autism spectrum disorder; Attention; Executive function; Visual search; Navon.
Autism spectrum disorders (ASD) are characterized by impairments in social functioning, communication, and restricted range of behaviors and interests (American Psychiatric Association, 2013), with a wide range of symptom severity and functional outcomes. The incidence for these disorders have recently been estimated at 1 in 68 children (Centers for Disease Control and Prevention, 2014), necessitating heightened efforts to clarify the neurocognitive underpinnings of ASD in order to inform early
diagnosis and treatment. Mixed findings on the nature of cognitive abnormalities in ASD include both accelerated (e.g., visuospatial abilities including Block Design, visual search, and Embedded Figures Test performance; Muth, Hönekopp, & Falter, 2014; O’Riordan, Plaisted, Driver, & Baron-Cohen, 2001; Plaisted, O’Riordan, & Baron-Cohen, 1998) and impaired abilities (e.g., slowed psychomotor and processing speed, impaired spatial orienting of attention; Keehn,
The current manuscript was prepared from the first author’s doctoral dissertation, completed at Eastern Michigan University in partial fulfillment of the requirements of the Clinical Psychology doctoral degree. Results were presented in part at the annual meeting of the International Neuropsychological Society in Denver, CO, USA. No potential conflict of interest was reported by the author(s). This work was supported by a Blue Cross Blue Shield of Michigan Foundation Student AwardProgram [grant number 1986.SAP awarded to the first author]. Address correspondence to: Annette E. Richard, Eastern Michigan University, Department of Psychology, Science Complex, Ypsilanti, MI 48197, USA (E‑mail: [email protected]).
© 2015 Taylor & Francis
Downloaded by [University of Otago] at 08:22 20 July 2015
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RICHARD AND LAJINESS-O’NEILL
Lincoln, Muller, & Townsend, 2010; Minshew & Goldstein, 1998). Among these mixed findings, visual attention has emerged as a potentially vital construct that has consistently been found to be abnormal in ASD (e.g., Allen & Courchesne, 2001; Courchesne et al., 1994; Harris, Courchesne, Townsend, Carper, & Lord, 1999; Johnson et al., 2007; Keehn et al., 2010; Renner, Klinger, & Klinger, 2006; Townsend et al., 1999). From the perspective of neurodevelopmental models of ASD (e.g., Belmonte et al., 2004; Keehn, Müller, & Townsend, 2013; Rippon, Brock, Brown, & Boucher, 2007), visual attention is one of the early-developing, fundamental aspects of cognition in which a small abnormality could potentially have cascading effects on the development of higher order cognitive processing, including social cognition. Specifically, visual attention is thought to play an integral role in the development of social functioning through the mediating process of joint attention (Mundy & Jarrold, 2010), which has consistently been found to be impaired in ASD (Charman et al., 1997; Dawson et al., 2004; Leekam, Lopez, & Moore, 2000). A limited number of studies have investigated the relationship between executive attention and joint attention in individuals with ASD, indicating a positive correlation between the two skills (Dawson et al., 2002; Griffith & Pennington, 2003); however, a direct relationship between executive attention and more general social functioning in children with ASD has not yet been addressed by the literature. An aspect of visual attention that may be particularly relevant to social impairment in ASD is deficient shifting in volitional attentional processes (Keehn et al., 2013), in which multiple stimuli are presented simultaneously, and task demands require processing of an unattended stimulus (Fan, 2013). Examples of volitional shifting of attention include endogenous spatial orienting and adjusting the spotlight of attention. Endogenous spatial orienting refers to the voluntary orienting of visual attention to a particular location, often in response to a directional cue such as an arrow. The spotlight of attention refers to an attentional “spotlight,” inside of which stimulus processing is enhanced and outside of which stimulus processing is inhibited; this spotlight can be broadened or narrowed, facilitating processing of either global or local aspects of a stimulus. Despite emerging evidence that attention shifting is impaired in ASD, a coherent understanding of deficits in visual attention shifting in ASD remains elusive. Evidence for impairment in various cognitive functions related to visual attention shifting in
ASD is mixed. Deficits in endogenous spatial orienting have been primarily seen with short cue–target intervals, with less evidence for impairment at longer cue–target intervals (Landry, Mitchell, & Burack, 2009; Senju, Tojo, Dairoku, & Hasegawa, 2004; Wainwright-Sharp & Bryson, 1993). Findings on adjustment of the spotlight of attention have been more consistent, with multiple studies confirming deficits (Mann & Walker, 2003; Remington, Swettenham, Campbell, & Coleman, 2009; Rinehart, Bradshaw, Moss, Brereton, & Tonge, 2001). Findings on set shifting, which requires shifting between tasks rather than stimuli or stimulus features and may encompass some higher order cognitive functions, have also been mixed. There is consistent evidence for difficulty switching tasks (i.e., perseverating) on the Wisconsin Card Sorting task (WCST; Sanders, Johnson, Garavan, Gill, & Gallagher, 2008). However, there is mixed evidence for difficulty with task switching on another measure of set shifting, the Intradimensional/Extradimensional Shift Test, with some studies finding impaired performance in ASD (Ozonoff et al., 2004; Yerys et al., 2009) and others finding no impairment (Corbett, Constantine, Hendren, Rocke, & Ozonoff, 2009; Happé, Booth, Charlton, & Hughes, 2006). Other modified measures of set shifting have not found evidence for set-shifting deficits in ASD (Dichter et al., 2010; Poljac et al., 2010). Particularly notable is a finding that performance on a modified set-shifting task in preschoolage children with ASD was not impaired, but was also not correlated with joint attention skills as it was in neurotypical (NT) controls (Stahl & Pry, 2002). To investigate a potential deficit in attention shifting underlying a variety of observed attentional abnormalities in children with ASD (e.g., mixed findings on Navon task performance, enhanced visual search but impaired psychomotor and processing speed, and behavioral symptoms including visual stimulus seeking, restricted attention to specific visual stimuli, and difficulty transitioning attention to new stimuli), the present study investigated volitional attentional shifting at two levels of visual information processing. Models such as feature integration theory (FIT; Treisman, 1998) propose that visual processing consists of two stages: First, stimuli over a broad range of the visual field are processed in parallel (referred to as preattention), then focused attention is directed at a particular location. According to this model, simple tasks requiring only information about whether a feature is present or absent (e.g., identifying a red item amongst gray items) can be
Downloaded by [University of Otago] at 08:22 20 July 2015
VISUAL ATTENTION SHIFTING IN ASD
done at a preattentive level, while tasks that require more complex information about whether two features are present in the same object require focused attention. Top-down control over visual processing can be exerted at the level of preattention as well as at the level of focused attention (Wolfe, Cave, & Franzel, 1989). Thus, at the level of preattention, visual search performance is significantly slower when a target is defined within a dimension other than one that is expected based on a previous target (Chan & Hayward, 2009; Found & Muller, 1996; Müller, Heller, & Ziegler, 1995; Treisman & Gormican, 1988). Both functional magnetic resonance imaging (fMRI) evidence and electroencephalography (EEG) evidence point to the role of left frontopolar cortex (Brodmann area, BA 10) in exerting top-down control over the attended visual dimension—that is, shifting visual preattention between stimulus dimensions (Pollmann, Weidner, Müller, & von Cramon, 2000; Gramann, Töllner, & Müller, 2010). While those with ASD have consistently been found to show enhanced performance on difficult visual search tasks (O’Riordan, 2000, 2004; O’Riordan & Plaisted, 2001; Plaisted et al., 1998), dimension switching during visual search has not been investigated in ASD. Given evidence of hypoactivation of BA 10 in ASD during tasks requiring cognitive control (Solomon et al., 2009), it was hypothesized that ASD would show greater dimension-switching costs than NT, where dimension-switching costs are defined as the difference in reaction time between trials requiring a shift between stimulus dimensions and trials that do not require a shift. The present study also investigated shifting during focused attention, specifically adjusting the spotlight of attention. This aspect of attention is one of the primary functions encompassed by the “executive attention” or “shift” aspect of Posner’s model of attention (Posner & Fan, 2008). Adjusting the spotlight of attention facilitates processing of either the local or global aspects of a stimulus, and it is voluntary and effortful, as evidenced by longer reaction times when attention must be redirected from global to local features of a stimulus, or vice versa (Robertson, Egly, Lamb, & Kerth, 1993; Ward, 1982). It has been widely theorized that an abnormal balance between attention to global and local features of stimuli, often conceptualized as “weak central coherence” or impaired ability to perceive a whole stimulus rather than its separate parts, may be a core feature of ASD (Happé & Frith, 2006). A related theory proposes that enhanced perceptual functioning is a core feature of ASD (Caron,
3
Mottron, Berthiaume, & Dawson, 2006; Mottron, Dawson, Soulières, Hubert, & Burack, 2006; Samson, Mottron, Soulières, & Zeffiro, 2012) and accounts for findings of both superior processing of the local stimulus level (Dakin & Frith, 2005; Muth et al., 2014) and superior visual search compared to NT (O’Riordan, 2000, 2004; O’Riordan et al., 2001; Plaisted et al., 1998). However, while it has been established that NT performance is slower when a switch of attention from the global to the local stimulus level, or vice versa, is required (Ward, 1982), what little evidence is currently available on shifting between global and local stimulus levels in ASD is mixed. One study found no difference in shifting ability between young adults with ASD and NT (Hayward et al., 2012), while another found slower performance in ASD than in NT when a shift from the local to the global stimulus level was required (Rinehart et al., 2001). To illustrate the intersections between the various aspects of visual attention addressed in the current study, a model integrating the two-stage FIT model of preattention and focused attention with Posner’s three-level model of attention is proposed (see Posner & Fan, 2008, for a detailed description of this model). A schematic of this model, including all tasks used in the present study, is presented in Figure 1. Given findings of slowed psychomotor and processing speed in ASD (Goldstein, Johnson, & Minshew, 2001; Mayes & Calhoun, 2007), thought to correspond to the “alert” component of Posner’s model of attention, the present study utilized measures of these functions in order to dissociate the alert component from the shift component at the levels of both preattention and focused attention (CogState Detection and Identification tasks, respectively; Maruff et al., 2009). A measure of higher order attention shifting at the level of focused attention, which has consistently been shown to be impaired in ASD (Sanders et al., 2008), was also included (CogState Set Shifting task; Maruff et al., 2009). To address social functioning, the current study employed two parent report measures of social impairment (Social Communication Questionnaire, SCQ; Rutter, Bailey, Lord, & Berument, 2003; and Social Responsiveness Scale, SRS; Constantino, 2002) and two objective measures of social cognition (A Developmental Neuropsychological Assessment, NEPSY, Affect Recognition and Theory of Mind subtests; Brooks, Sherman, & Strauss, 2009). The SCQ is a screening measure for ASD, and the SRS is a measure of social communication difficulties and restricted and repetitive behaviors associated with ASD. NEPSY Affect Recognition is designed to
4
RICHARD AND LAJINESS-O’NEILL
Downloaded by [University of Otago] at 08:22 20 July 2015
Figure 1. Proposed model of visual attention. Schematic of the hypothesized intersection of the preattention/focused attention aspects of feature integration theory (FIT) with Posner’s three-component model of attention. Tasks that were used in the present study to index the intersection of each of these components are noted. The present study focused primarily on the intersection of executive attention with preattention and focused attention.
measure facial affect identification, and NEPSY Theory of Mind is designed to measure understanding of others’ perspectives, intentions, and beliefs (Brooks et al., 2009). The Autism Diagnostic Observation Schedule (ADOS–2; Rutter, DiLavore, Risi, Gotham, & Bishop, 2012), a structured play-based assessment designed to allow direct observation of ASD symptoms, was used to confirm diagnosis and as an additional measure of social cognitive abilities in the ASD group. The primary aim of the present study was to investigate a general deficit in shifting attention at both the level of preattention and the level of focused attention in children with ASD as compared to age- and gender-matched neurotypical controls (NT). For the purposes of this study, visual attention shifting was measured by both a visual search task with a dimensional shift component and a Navon-type letter task requiring participants to shift attention between global and local levels of a visual stimulus. A secondary aim was to investigate a potential relationship between social impairment and deficits in attention shifting. It was hypothesized that (a) ASD would show a significantly larger difference in reaction time (RT) between trials requiring a shift of attention and trials with no shifting demands than would NT on measures of executive attention at both the level of preattention and the level of focused attention; (b) measures of executive attention at the levels of preattention and focused attention would be significantly positively correlated with each other among the ASD group, consistent with use of more effortful, higher order processing to accomplish preattentive visual shifting in ASD; (c) measures of executive attention at the level of focused attention would be significantly positively correlated with each other among both ASD and NT; and (d) among the ASD group, measures of executive attention at both the level of preattention
and the level of focused attention would be correlated with measures of social impairment, such that better performance on executive attention tasks would be associated with less social impairment. METHOD Participants Participants were 20 children with ASD and 20 age- and gender-matched NT children. Exclusion criteria for both ASD and NT participants included intellectual functioning below the low average range (
Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen20
Visual attention shifting in autism spectrum disorders a
a
Annette E. Richard & Renee Lajiness-O’Neill a
Department of Psychology, Science Complex, Eastern Michigan University, Ypsilanti, MI, USA Published online: 09 Jul 2015.
Click for updates To cite this article: Annette E. Richard & Renee Lajiness-O’Neill (2015): Visual attention shifting in autism spectrum disorders, Journal of Clinical and Experimental Neuropsychology, DOI: 10.1080/13803395.2015.1042838 To link to this article: http://dx.doi.org/10.1080/13803395.2015.1042838
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
Journal of Clinical and Experimental Neuropsychology, 2015 http://dx.doi.org/10.1080/13803395.2015.1042838
Visual attention shifting in autism spectrum disorders Annette E. Richard
and Renee Lajiness-O’Neill
Department of Psychology, Science Complex, Eastern Michigan University, Ypsilanti, MI, USA
Downloaded by [University of Otago] at 08:22 20 July 2015
(Received 23 September 2014; accepted 15 April 2015) Introduction: Abnormal visual attention has been frequently observed in autism spectrum disorders (ASD). Abnormal shifting of visual attention is related to abnormal development of social cognition and has been identified as a key neuropsychological finding in ASD. Better characterizing attention shifting in ASD and its relationship with social functioning may help to identify new targets for intervention and improving social communication in these disorders. Thus, the current study investigated deficits in attention shifting in ASD as well as relationships between attention shifting and social communication in ASD and neurotypicals (NT). Method: To investigate deficits in visual attention shifting in ASD, 20 ASD and 20 age- and gender-matched NT completed visual search (VS) and Navon tasks with attention-shifting demands as well as a set-shifting task. VS was a feature search task with targets defined in one of two dimensions; Navon required identification of a target letter presented at the global or local level. Psychomotor and processing speed were entered as covariates. Relationships between visual attention shifting, set shifting, and social functioning were also examined. Results: ASD and NT showed comparable costs of shifting attention. However, psychomotor and processing speed were slower in ASD than in NT, and psychomotor and processing speed were positively correlated with attention-shifting costs on Navon and VS, respectively, for both groups. Attention shifting on VS and Navon were correlated among NT, while attention shifting on Navon was correlated with set shifting among ASD. Attentionshifting costs on Navon were positively correlated with restricted and repetitive behaviors among ASD. Conclusions: Relationships between attention shifting and psychomotor and processing speed, as well as relationships between measures of different aspects of visual attention shifting, suggest inefficient top-down influences over preattentive visual processing in ASD. Inefficient attention shifting may be related to restricted and repetitive behaviors in these disorders. Keywords: Autism spectrum disorder; Attention; Executive function; Visual search; Navon.
Autism spectrum disorders (ASD) are characterized by impairments in social functioning, communication, and restricted range of behaviors and interests (American Psychiatric Association, 2013), with a wide range of symptom severity and functional outcomes. The incidence for these disorders have recently been estimated at 1 in 68 children (Centers for Disease Control and Prevention, 2014), necessitating heightened efforts to clarify the neurocognitive underpinnings of ASD in order to inform early
diagnosis and treatment. Mixed findings on the nature of cognitive abnormalities in ASD include both accelerated (e.g., visuospatial abilities including Block Design, visual search, and Embedded Figures Test performance; Muth, Hönekopp, & Falter, 2014; O’Riordan, Plaisted, Driver, & Baron-Cohen, 2001; Plaisted, O’Riordan, & Baron-Cohen, 1998) and impaired abilities (e.g., slowed psychomotor and processing speed, impaired spatial orienting of attention; Keehn,
The current manuscript was prepared from the first author’s doctoral dissertation, completed at Eastern Michigan University in partial fulfillment of the requirements of the Clinical Psychology doctoral degree. Results were presented in part at the annual meeting of the International Neuropsychological Society in Denver, CO, USA. No potential conflict of interest was reported by the author(s). This work was supported by a Blue Cross Blue Shield of Michigan Foundation Student AwardProgram [grant number 1986.SAP awarded to the first author]. Address correspondence to: Annette E. Richard, Eastern Michigan University, Department of Psychology, Science Complex, Ypsilanti, MI 48197, USA (E‑mail: [email protected]).
© 2015 Taylor & Francis
Downloaded by [University of Otago] at 08:22 20 July 2015
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RICHARD AND LAJINESS-O’NEILL
Lincoln, Muller, & Townsend, 2010; Minshew & Goldstein, 1998). Among these mixed findings, visual attention has emerged as a potentially vital construct that has consistently been found to be abnormal in ASD (e.g., Allen & Courchesne, 2001; Courchesne et al., 1994; Harris, Courchesne, Townsend, Carper, & Lord, 1999; Johnson et al., 2007; Keehn et al., 2010; Renner, Klinger, & Klinger, 2006; Townsend et al., 1999). From the perspective of neurodevelopmental models of ASD (e.g., Belmonte et al., 2004; Keehn, Müller, & Townsend, 2013; Rippon, Brock, Brown, & Boucher, 2007), visual attention is one of the early-developing, fundamental aspects of cognition in which a small abnormality could potentially have cascading effects on the development of higher order cognitive processing, including social cognition. Specifically, visual attention is thought to play an integral role in the development of social functioning through the mediating process of joint attention (Mundy & Jarrold, 2010), which has consistently been found to be impaired in ASD (Charman et al., 1997; Dawson et al., 2004; Leekam, Lopez, & Moore, 2000). A limited number of studies have investigated the relationship between executive attention and joint attention in individuals with ASD, indicating a positive correlation between the two skills (Dawson et al., 2002; Griffith & Pennington, 2003); however, a direct relationship between executive attention and more general social functioning in children with ASD has not yet been addressed by the literature. An aspect of visual attention that may be particularly relevant to social impairment in ASD is deficient shifting in volitional attentional processes (Keehn et al., 2013), in which multiple stimuli are presented simultaneously, and task demands require processing of an unattended stimulus (Fan, 2013). Examples of volitional shifting of attention include endogenous spatial orienting and adjusting the spotlight of attention. Endogenous spatial orienting refers to the voluntary orienting of visual attention to a particular location, often in response to a directional cue such as an arrow. The spotlight of attention refers to an attentional “spotlight,” inside of which stimulus processing is enhanced and outside of which stimulus processing is inhibited; this spotlight can be broadened or narrowed, facilitating processing of either global or local aspects of a stimulus. Despite emerging evidence that attention shifting is impaired in ASD, a coherent understanding of deficits in visual attention shifting in ASD remains elusive. Evidence for impairment in various cognitive functions related to visual attention shifting in
ASD is mixed. Deficits in endogenous spatial orienting have been primarily seen with short cue–target intervals, with less evidence for impairment at longer cue–target intervals (Landry, Mitchell, & Burack, 2009; Senju, Tojo, Dairoku, & Hasegawa, 2004; Wainwright-Sharp & Bryson, 1993). Findings on adjustment of the spotlight of attention have been more consistent, with multiple studies confirming deficits (Mann & Walker, 2003; Remington, Swettenham, Campbell, & Coleman, 2009; Rinehart, Bradshaw, Moss, Brereton, & Tonge, 2001). Findings on set shifting, which requires shifting between tasks rather than stimuli or stimulus features and may encompass some higher order cognitive functions, have also been mixed. There is consistent evidence for difficulty switching tasks (i.e., perseverating) on the Wisconsin Card Sorting task (WCST; Sanders, Johnson, Garavan, Gill, & Gallagher, 2008). However, there is mixed evidence for difficulty with task switching on another measure of set shifting, the Intradimensional/Extradimensional Shift Test, with some studies finding impaired performance in ASD (Ozonoff et al., 2004; Yerys et al., 2009) and others finding no impairment (Corbett, Constantine, Hendren, Rocke, & Ozonoff, 2009; Happé, Booth, Charlton, & Hughes, 2006). Other modified measures of set shifting have not found evidence for set-shifting deficits in ASD (Dichter et al., 2010; Poljac et al., 2010). Particularly notable is a finding that performance on a modified set-shifting task in preschoolage children with ASD was not impaired, but was also not correlated with joint attention skills as it was in neurotypical (NT) controls (Stahl & Pry, 2002). To investigate a potential deficit in attention shifting underlying a variety of observed attentional abnormalities in children with ASD (e.g., mixed findings on Navon task performance, enhanced visual search but impaired psychomotor and processing speed, and behavioral symptoms including visual stimulus seeking, restricted attention to specific visual stimuli, and difficulty transitioning attention to new stimuli), the present study investigated volitional attentional shifting at two levels of visual information processing. Models such as feature integration theory (FIT; Treisman, 1998) propose that visual processing consists of two stages: First, stimuli over a broad range of the visual field are processed in parallel (referred to as preattention), then focused attention is directed at a particular location. According to this model, simple tasks requiring only information about whether a feature is present or absent (e.g., identifying a red item amongst gray items) can be
Downloaded by [University of Otago] at 08:22 20 July 2015
VISUAL ATTENTION SHIFTING IN ASD
done at a preattentive level, while tasks that require more complex information about whether two features are present in the same object require focused attention. Top-down control over visual processing can be exerted at the level of preattention as well as at the level of focused attention (Wolfe, Cave, & Franzel, 1989). Thus, at the level of preattention, visual search performance is significantly slower when a target is defined within a dimension other than one that is expected based on a previous target (Chan & Hayward, 2009; Found & Muller, 1996; Müller, Heller, & Ziegler, 1995; Treisman & Gormican, 1988). Both functional magnetic resonance imaging (fMRI) evidence and electroencephalography (EEG) evidence point to the role of left frontopolar cortex (Brodmann area, BA 10) in exerting top-down control over the attended visual dimension—that is, shifting visual preattention between stimulus dimensions (Pollmann, Weidner, Müller, & von Cramon, 2000; Gramann, Töllner, & Müller, 2010). While those with ASD have consistently been found to show enhanced performance on difficult visual search tasks (O’Riordan, 2000, 2004; O’Riordan & Plaisted, 2001; Plaisted et al., 1998), dimension switching during visual search has not been investigated in ASD. Given evidence of hypoactivation of BA 10 in ASD during tasks requiring cognitive control (Solomon et al., 2009), it was hypothesized that ASD would show greater dimension-switching costs than NT, where dimension-switching costs are defined as the difference in reaction time between trials requiring a shift between stimulus dimensions and trials that do not require a shift. The present study also investigated shifting during focused attention, specifically adjusting the spotlight of attention. This aspect of attention is one of the primary functions encompassed by the “executive attention” or “shift” aspect of Posner’s model of attention (Posner & Fan, 2008). Adjusting the spotlight of attention facilitates processing of either the local or global aspects of a stimulus, and it is voluntary and effortful, as evidenced by longer reaction times when attention must be redirected from global to local features of a stimulus, or vice versa (Robertson, Egly, Lamb, & Kerth, 1993; Ward, 1982). It has been widely theorized that an abnormal balance between attention to global and local features of stimuli, often conceptualized as “weak central coherence” or impaired ability to perceive a whole stimulus rather than its separate parts, may be a core feature of ASD (Happé & Frith, 2006). A related theory proposes that enhanced perceptual functioning is a core feature of ASD (Caron,
3
Mottron, Berthiaume, & Dawson, 2006; Mottron, Dawson, Soulières, Hubert, & Burack, 2006; Samson, Mottron, Soulières, & Zeffiro, 2012) and accounts for findings of both superior processing of the local stimulus level (Dakin & Frith, 2005; Muth et al., 2014) and superior visual search compared to NT (O’Riordan, 2000, 2004; O’Riordan et al., 2001; Plaisted et al., 1998). However, while it has been established that NT performance is slower when a switch of attention from the global to the local stimulus level, or vice versa, is required (Ward, 1982), what little evidence is currently available on shifting between global and local stimulus levels in ASD is mixed. One study found no difference in shifting ability between young adults with ASD and NT (Hayward et al., 2012), while another found slower performance in ASD than in NT when a shift from the local to the global stimulus level was required (Rinehart et al., 2001). To illustrate the intersections between the various aspects of visual attention addressed in the current study, a model integrating the two-stage FIT model of preattention and focused attention with Posner’s three-level model of attention is proposed (see Posner & Fan, 2008, for a detailed description of this model). A schematic of this model, including all tasks used in the present study, is presented in Figure 1. Given findings of slowed psychomotor and processing speed in ASD (Goldstein, Johnson, & Minshew, 2001; Mayes & Calhoun, 2007), thought to correspond to the “alert” component of Posner’s model of attention, the present study utilized measures of these functions in order to dissociate the alert component from the shift component at the levels of both preattention and focused attention (CogState Detection and Identification tasks, respectively; Maruff et al., 2009). A measure of higher order attention shifting at the level of focused attention, which has consistently been shown to be impaired in ASD (Sanders et al., 2008), was also included (CogState Set Shifting task; Maruff et al., 2009). To address social functioning, the current study employed two parent report measures of social impairment (Social Communication Questionnaire, SCQ; Rutter, Bailey, Lord, & Berument, 2003; and Social Responsiveness Scale, SRS; Constantino, 2002) and two objective measures of social cognition (A Developmental Neuropsychological Assessment, NEPSY, Affect Recognition and Theory of Mind subtests; Brooks, Sherman, & Strauss, 2009). The SCQ is a screening measure for ASD, and the SRS is a measure of social communication difficulties and restricted and repetitive behaviors associated with ASD. NEPSY Affect Recognition is designed to
4
RICHARD AND LAJINESS-O’NEILL
Downloaded by [University of Otago] at 08:22 20 July 2015
Figure 1. Proposed model of visual attention. Schematic of the hypothesized intersection of the preattention/focused attention aspects of feature integration theory (FIT) with Posner’s three-component model of attention. Tasks that were used in the present study to index the intersection of each of these components are noted. The present study focused primarily on the intersection of executive attention with preattention and focused attention.
measure facial affect identification, and NEPSY Theory of Mind is designed to measure understanding of others’ perspectives, intentions, and beliefs (Brooks et al., 2009). The Autism Diagnostic Observation Schedule (ADOS–2; Rutter, DiLavore, Risi, Gotham, & Bishop, 2012), a structured play-based assessment designed to allow direct observation of ASD symptoms, was used to confirm diagnosis and as an additional measure of social cognitive abilities in the ASD group. The primary aim of the present study was to investigate a general deficit in shifting attention at both the level of preattention and the level of focused attention in children with ASD as compared to age- and gender-matched neurotypical controls (NT). For the purposes of this study, visual attention shifting was measured by both a visual search task with a dimensional shift component and a Navon-type letter task requiring participants to shift attention between global and local levels of a visual stimulus. A secondary aim was to investigate a potential relationship between social impairment and deficits in attention shifting. It was hypothesized that (a) ASD would show a significantly larger difference in reaction time (RT) between trials requiring a shift of attention and trials with no shifting demands than would NT on measures of executive attention at both the level of preattention and the level of focused attention; (b) measures of executive attention at the levels of preattention and focused attention would be significantly positively correlated with each other among the ASD group, consistent with use of more effortful, higher order processing to accomplish preattentive visual shifting in ASD; (c) measures of executive attention at the level of focused attention would be significantly positively correlated with each other among both ASD and NT; and (d) among the ASD group, measures of executive attention at both the level of preattention
and the level of focused attention would be correlated with measures of social impairment, such that better performance on executive attention tasks would be associated with less social impairment. METHOD Participants Participants were 20 children with ASD and 20 age- and gender-matched NT children. Exclusion criteria for both ASD and NT participants included intellectual functioning below the low average range (
