Autism spectrum disorder (ASD) is characterized by repetitive behaviors and difficulty with social interactions, communication, and the development of interpersonal relationships. The recently reported prevalence of ASD is high, with one in 54 children who are 8 years old meeting the diagnostic criteria (Maenner et al, 2020).
The neurobehavioral mechanisms responsible for challenges with social interactions in individuals with ASD are not yet fully understood. However, effective social communication and the development of interpersonal relationships are correlated with the ability to interpret facial expressions. Individuals with ASD often have facial-emotion recognition deficits (Lozier et al, 2014). When interacting with others, typical individuals without autism are more likely to focus their attention on another person’s eyes, in the upper portion of the face (Neumann et al, 2006), whereas individuals with ASD are more likely to focus their attention on the mouth, in the lower portion of the face (Neumann et al, 2006). Therefore, with social interactions, the facial-emotion recognition deficits associated with ASD might be related to the individual attending more to the mouth than the eyes.
Because perception depends on the allocation of spatial attention, atypical biases in spatial attention could contribute to altered patterns of visual scanning, which might partly contribute to impairments in facial-emotion recognition. Recent work has revealed a high degree of inconsistency in the finding of decreased eye viewing in individuals with ASD (Vettori et al, 2020). However, because eye contact is part of the diagnostic criteria for ASD (American Psychiatric Association, 2013), and because this increasing eye contact is often a very active target of behavioral therapy, such intervention may decrease the incidence of eye viewing findings in research (Zamzow et al, 2014). Therefore, it remains of interest to determine whether altered allocation of spatial attention might contribute to prepotent facial scanning tendencies in individuals with ASD.
To effectively interact with the environment, an individual must be able to attend to stimuli in both the left and right space as well as higher and lower space. Spatial neglect is the inability of individuals with cerebral damage to attend to certain areas of visual space, with neglect of horizontal space being well documented (Corbetta and Shulman, 2011; Li and Malhotra, 2015). Recent findings have suggested an atypical bias pattern with horizontal line bisection in individuals with ASD (Liu et al, 2021). However, neglect can also occur in vertical line bisection (Michael et al, 2020; Rapcsak et al, 1988).
Line bisection tasks are used to determine whether individuals have a spatial attentional bias. These tasks are simple to perform and are effective clinical markers of visuospatial bias in individuals with neglect. During vertical line bisection and quadrisection tasks, typical individuals without autism demonstrate a subtle upward bias, termed altitudinal pseudoneglect, and this tendency has provided some insights into the typical allocation of vertical attention (Falchook et al, 2013; Heber et al, 2010; Jewell and McCourt, 2000).
Typical Allocation of Vertical Attention
During visual scanning, after visual information is processed by the primary visual cortex, the information is then processed by the visual association cortex, which is subdivided into two extrastriate areas: The dorsal (where) stream is where visual stimuli are further processed by the parietal lobe, and the ventral (what) stream is where visual stimuli are further processed by the temporal lobe (Fellman and Van Essen, 1991; Young, 1992). The dorsal stream processes the relative spatial location of objects, and the ventral stream processes specific stimuli such as faces and objects (Mishkin et al, 1983).
Additionally, evidence from individuals with bilateral hemispheric focal lesions has revealed that the dorsal stream appears to process and mediate attention to lower visual space (Butter et al, 1989; Rapcsak et al, 1988), and the ventral stream appears to process and mediate attention to upper visual space (Shelton et al, 1990). Thus, the altitudinal pseudoneglect displayed by nonautistic individuals during vertical line bisection tasks is proposed to result from the ventral stream’s dominance in allocating vertical object attention (Drain and Reuter-Lorenz, 1996). Furthermore, allocentric (object-to-object) representations in space are processed by the ventral stream, and egocentric (self-to-object) representations in space are processed by the dorsal stream (Neggers et al, 2006).
Falchook et al (2013) proposed that the upward bias during vertical line bisection tasks is due to the allocentric (object-based) nature of the bisection task, which would preferentially activate the ventral stream over the dorsal stream. Local versus global attentional demands of a task may also influence line bisection and quadrisection judgments. For example, when nonautistic individuals perform vertical line quadrisection tasks, which require more focal attention than bisection tasks, they usually exhibit a greater upward bias than individuals with ASD.
Studies of individuals with ASD have proposed differences in the dorsal and ventral visual association networks. Motion-processing experiments revealed altered performance on tasks that were associated with the dorsal stream in individuals with ASD compared with controls (Spencer et al, 2000). However, in other studies of individuals with ASD, the data did not point to a clear alteration specific to the dorsal stream (Chung and Sun, 2020). Previous fMRI research has also shown that the ventral visual association cortex appears to be organized differently in individuals with ASD compared with nonautistic individuals, which may relate to the well-established finding that individuals with ASD have reduced activation within face-selective regions (Humphreys et al, 2008).
Given that ventral portions of the visual processing network mediate upward attention, the primary aim of this study was to determine if individuals with ASD have altered vertical attention, as evidenced by a downward vertical attentional bias. It is possible that a downward vertical attentional bias may account for individuals with ASD attending to the mouth, which is commonly observed in studies where individuals with ASD are asked to visually scan faces.
To investigate this spatial attentional hypothesis, we asked individuals with ASD and nonautistic controls to perform vertical line bisection and vertical line quadrisection tasks. If facial scanning findings in ASD are, in part, driven by vertical attentional bias, we would expect the individuals with ASD to exhibit a downward vertical bias on line bisection and quadrisection tasks.
Based on previous work reporting on the difference between individuals with ASD and control groups on fixation time looking at eyes (Neumann et al, 2006), if this finding is entirely driven by a spatial bias, 11 individuals per group should be sufficient to 80% power to detect a difference between groups with a significance level of α = 0.05. Therefore, we recruited 20 individuals per group in order to allow for the possibility of detecting more subtle partial effects.
We recruited individuals with ASD through a registry of patients who had consented to be contacted for research purposes at the Thompson Center for Autism and Neurodevelopmental Disorders in Columbia, Missouri. Control participants were recruited via flyers that were posted in clinics and email announcements.
Autism spectrum diagnosis was confirmed with the Autism Diagnostic Observation Scale (Lord et al, 1989) in 18 individuals, with the remaining two diagnosed by developmental pediatricians and psychologists according to the criteria in the fifth edition of the Diagnostic and Statistical Manual (American Psychiatric Association, 2013). All of the participants were right-handed and had a full-scale IQ >85. Controls were matched on a case-by-case basis for sex and age, with control participants being individually matched to within 1 year of age compared with their matched ASD individuals. The two groups had comparable Mfull-scale IQ scores as measured by the Wechsler Abbreviated Scale of Intelligence–II (Wechsler, 2011) (ASD = 107.0 ± 2.61 SD, control = 107.7 ± 2.36 SD).
Participants were also screened for their ability to follow the instructions, and the task was observed to be easy to perform across all ages. Nonautistic individuals had no history of any neuropsychiatric or neurodevelopmental disorders by self-report.
The study was approved by the University of Missouri Health Sciences Institutional Review Board in Columbia, Missouri, and all of the participants volunteered and provided informed consent (assent for participants under 18).
We used a 121.9 cm × 91.4 cm trifold white poster board as a hanging platform for the stimuli. Each wing of the poster board was 30.5 cm wide, and the center section was 61 cm wide. We placed the poster board on a cabinet with its back aligned with the vertical and pressed against a wall (Figure 1). Pieces of paper 21.6 cm × 27.9 cm, each with a centered black vertical line 22.7 cm in length and 1 cm in width, were used for the bisection and quadrisection tasks.
During the tasks, we used tacks to pin the pieces of paper to the board and adjusted the height of the paper such that the center of the line was at each individual’s eye level. As with Falchook and colleagues (2013), we had established each individual’s eye level at the beginning of the study visits by instructing the individuals to stand up straight and measuring the height at which their gaze fell in order to position the paper properly. For bisection and quadrisection tasks in the center visual space, the black vertical line to be bisected was located at the individual’s midsagittal plane. For bisection and quadrisection tasks in the left and right visual spaces, the black vertical line was located 19.7 cm to the left or right of an individual’s midsagittal plane.
Each participant completed a total of 36 bisection trials and 72 quadrisection trials in one 2-hour session at the Thompson Center. We adapted the methodology used by Falchook and colleagues (2013) and instructed each individual to stand 45.7 cm from the board with their midsagittal plane facing the center of the board. A distance of 45.7 cm allowed individuals of all ages to be close enough to the board to perform the task, while also having enough space to see the visual stimuli from a moderate distance. This distance also seemed to increase the comfort level of the ASD group.
We then placed pieces of paper with a vertical line one at a time in the center, left, or right hemispace. The order in which the vertical lines were presented was randomized both within and across individuals. To better isolate possible hemispace differences for each task, we instructed each individual to not move their feet, body, or head, and to keep their eyes fixated on the center panel. Therefore, during the bisection tasks, the individual’s eyes were directed toward the sheet of paper, and during the quadrisection tasks, the individuals’ eye gaze was still fixated forward, requiring them to use their peripheral vision. Trials where the individuals did not follow these instructions were excluded, which resulted in 0.32% of the trials being excluded.
We asked each individual to bisect (mark a line through the middle) and quadrisect (mark a line 25% from the top or 25% from the bottom) the vertical lines using a pen. Practice trials were performed to ensure each individual understood the meaning of the quadrisection task. For each trial, we instructed the individuals about which hand to use, which was also randomized within and between individuals. After each trial, the piece of paper was removed and a new unmarked piece of paper with a vertical line was presented.
As with prior line bisection studies (Falchook et al, 2013), we did not provide feedback to the individuals about their performance. Each individual completed six trials for each condition (left, center, and right hemispaces) using each hand.
We analyzed each attempted bisection and quadrisection by comparing each individual’s marks to the true bisection or quadrisection. Bisection trials and top quadrisection trials were measured from the top of the line; bottom quadrisection trials were measured from the bottom of the line. Using the strategy presented by Falchook and colleagues (2013), we calculated error ratios for each trial. We used the equation ([113.5 mm − x mm]/113.5 mm) for the line bisections, the equation ([56.75 mm − x mm]/56.75 mm) for the top quadrisections, and the equation ([x mm − 56.75 mm]/56.75 mm) for the bottom quadrisections; x denoting the distance from the individual’s mark to the top of the line for bisections and top quadrisections and the distance to the bottom of the line for bottom quadrisections.
For all of the conditions (bisection, top quadrisection, and bottom quadrisection), a positive error ratio represented an upward bias from the true midpoint or quadripoint, and a negative error ratio represented a downward bias from the true midpoint or quadripoint. For the bisection, top quadrisection, and bottom quadrisection, a 2 (control vs ASD) × 2 (left hand vs right hand) × 3 (left visual space vs center visual space vs right visual space) ANOVA was performed to assess group differences and to look for any interaction effects.
Participants included 20 individuals with ASD and 20 age- and sex-matched nonautistic individuals, ages 6–23 years (ASD Mage = 14.3 ± 5.26 SD, control Mage = 14.3 ± 4.99 SD), with 32 males and 8 females (4 ASD and 4 controls).
Top Vertical Quadrisection
Using an ANOVA, there were no significant effects of the hand that was used for the task (left vs right) (F1,222 = 0.02, P = 0.88) or for visual space (left vs center vs right) (F2,222 = 0.47, P = 0.63) for the top line quadrisection. There also were no significant Hand Used × Visual Space (F2,222 = 0.004, P = 0.996), Hand Used × Diagnosis (ASD vs control) (F1,222 = 0.016, P = 0.90), or Visual Space × Diagnosis (F2,222 = 0.51, P = 0.60) interaction effects for the top quadrisection, nor was there a Hand Used × Visual Space × Diagnosis 3-way interaction for the top quadrisection (F2,222 = 0.08, P = 0.92). However, while both groups demonstrated an upward bias for the top quadrisections, as illustrated in Figure 2, there was a statistically significant difference for the top quadrisections: The ASD group had a greater deviation above the true top quadripoint than the control group (F1,222 = 9.95, P = 0.018, Cohen’s d = 1.023) (Table 1, Figure 2).
TABLE 1 -
Error Ratios for Each Condition—top Quadrisection, Line Bisection
, and Bottom Quadrisection—for the ASD and Control Groups
||0.261 ± 0.119
||0.186 ± 0.206
||0.056 ± 0.029
||0.059 ± 0.036
||–0.109 ± 0.21
||–0.072 ± 0.185
Values are presented as M ± SD unless noted otherwise.
ASD = autism spectrum disorder.
Using an ANOVA, there were no significant effects of the hand that was used for the task (left vs right) (F1,228 = 0.24, P = 0.62) or for visual space (left vs center vs right) (F2,228 = 0.35, P = 0.71) for the line bisection. There also were no significant Hand Used × Visual Space (F2,228 = 0.15, P = 0.86), Hand Used × Diagnosis (ASD vs control) (F1,228 = 1.29, P = 0.26), or Visual Space × Diagnosis (F2,228 = 0.05, P = 0.95) interaction effects for the bisection, nor was there a Hand Used × Visual Space × Diagnosis 3-way interaction for the bisection (F2,228 = 0.20, P = 0.82). For the main effect of group, there was no significant difference between the ASD and control groups for the Mbisection (F1,228 = 0.19, P = 0.66, Cohen’s d = 0.14).
Bottom Vertical Quadrisection
Using an ANOVA, there were no significant effects of the hand that was used for the task (left vs right) (F1,222 = 0.42, P = 0.52) or for visual space (left vs center vs right) (F1,222 = 0.09, P = 0.91) for the bottom line quadrisection. There also were no significant Hand Used × Visual Space (F2,222 = 0.10, P = 0.90), Hand Used × Diagnosis (ASD vs control) (F1,222 = 0.30, P = 0.58), or Visual Space × Diagnosis (F2,222 = 0.21, P = 0.81) interaction effects for the bottom quadrisection, nor was there a Hand Used × Visual Space × Diagnosis 3-way interaction for the bottom quadrisection (F2,222 = 0.13, P = 0.88). For the main effect of group, there was no significant difference between the ASD and control groups for the Mbottom quadrisection (F1,222 = 1.86, P = 0.17, Cohen’s d = 0.44).
A post hoc analysis was conducted to confirm that younger individuals were able to perform the tasks. We compared the performance of individuals <12 years of age with that of individuals >13 years of age. No difference was seen in performance on the more challenging quadrisection task between age groups (P > 0.5 for all conditions), and SDs were similar for both age groups as well (range = 0.15–0.25).
Because the atypical gaze pattern in many studies of individuals with ASD suggests preference for the mouth rather than the eyes during social communication, we aimed to determine if individuals with ASD have a downward vertical attentional bias. Our results found no significant difference between the ASD and control groups for either vertical line bisections or bottom vertical quadrisections. Thus, our results suggest that a downward vertical attentional bias is not responsible for the mouth preference that is exhibited by individuals with ASD during social communication.
Findings on facial scanning preferences in individuals with ASD are somewhat mixed. While numerous studies have reported a preference for gazing at the mouth in individuals with ASD (Klin et al, 2002; Neumann et al, 2006), a recent study that investigated facial scanning did not support the finding of excess mouth/diminished eye gaze in individuals with ASD, but rather suggested a more exploratory facial scanning style (Vettori et al, 2020). However, eye contact is part of the diagnostic criteria for ASD (American Psychiatric Association, 2013). Furthermore, one of the active targets of behavioral therapy for individuals with ASD is interventions to increase eye contact. Therefore, the impact of this intervention could decrease the incidence of eye viewing findings in research (Zamzow et al, 2014). As a result, it remains of interest to determine whether altered allocation of spatial attention might be present in individuals with ASD as a contributor to any prepotent facial scanning tendencies.
The results of this study did reveal a difference between the ASD and control groups on the top quadrisection tasks, with the ASD group deviating more toward the top of the line, and therefore exhibiting greater upward spatial bias, compared with the control group. These results are opposite of what would be expected if a vertical attentional spatial bias was responsible for the mouth preference in individuals with ASD.
Falchook and colleagues (2013) demonstrated that nonautistic individuals exhibit an upward vertical bias during both bisection and quadrisection tasks, with a greater upward bias for quadrisections compared with bisections. Researchers have postulated that this greater upward bias for quadrisection tasks was due to the more local–focal attentional demands of the task leading to a greater activation of the ventral stream (Falchook et al, 2013).
In our results, the individuals with ASD demonstrated an even greater upward bias on the top quadrisection tasks compared with the typical upward bias that is exhibited by nonautistic individuals performing the task. Because the dorsal visual stream allocates global attention, and the ventral visual stream allocates focal attention, the greater upward bias during the top quadrisection tasks exhibited by the ASD group may be related to the bias toward local over global visuospatial processing in individuals with ASD (Bertone et al, 2005; Joseph et al, 2009; Nayar et al, 2017). However, discussions focusing on the dorsal and ventral visual streams must be interpreted with caution given the considerable overlap and interaction between these two streams (Vossel et al, 2014).
This greater upward visuospatial bias, with a bias to allocate focal attention, might relate to reports that individuals with ASD have weak central coherence and therefore have difficulties “seeing the big picture” (Happé and Frith, 2006). However, studies have reported mixed findings regarding whether visual scanning patterns can be explained by a local bias (Bertone et al, 2005; Joseph et al, 2009) versus impairment in global processing (Nayar et al, 2017). These varied findings could be due to different methods for assessing and analyzing global versus local processing, such as using visual search tasks and embedded figure tasks.
These differences may also be related to the diverse nature of ASD symptomatology. For example, Stevenson et al (2018) found that enhanced local processing does not come at the expense of global processing, but rather reflects a default in the processing strategy. Because bisection tasks require more global processing, and quadrisection tasks require more local processing, our findings support the postulate that individuals with ASD have exaggerated local processing biases compared with nonautistic individuals. However, there may be other alternative explanations as well, such as spatial bias being driven by variations in the degrees of arousal among individuals with ASD.
These findings need to be interpreted with caution. First, the sample size was small. This study would need to be conducted with a larger sample for confirmation. However, the findings in the opposite direction of what would be expected for spatial bias driving the facial scanning patterns in individuals with ASD remain of interest. Also of note, there were 21 comparisons across all of the ANOVAs, which raises the concern that one finding could reach significance by chance. However, we believe the fact that the one finding, which was one of only three main effect group comparisons, was clearly in the opposite direction of the hypothesis that spatial bias is driving facial viewing patterns in individuals with ASD, is of significance.
There are other factors limiting the interpretation of our results. The participants in this study were selected based on their ability to complete the instructions for this task, and they were matched for IQ with the controls, so it is not clear how the results could be generalized to the broader ASD spectrum. Furthermore, as commonly occurs because of the disproportionate number of males who are affected with ASD, our sample had a limited number of females, which further limits generalizability of the findings. Finally, this study did not simultaneously examine facial scanning in the participants. Future studies need to incorporate this aspect in order to address potential questions, such as whether upward spatial bias might be a compensatory strategy to enhance viewing of the eye regions in individuals with ASD, which may also relate to past behavioral training efforts instructing individuals with ASD to look at people’s eyes.
Our results suggest that individuals with ASD have different perceptual strategies, regardless of their impact on facial scanning during social communication. One fMRI study found that individuals with ASD have lower activation of the face-selective fusiform gyrus during facial processing and higher activation of the object-related medial occipital gyrus (Hubl et al, 2003). Additionally, these authors found that individuals with ASD had higher cortical activation of the regions associated with visual search during the time the individuals with ASD were processing faces, supporting a local-processing bias. Another study that investigated visual processing along different areas of the ventral stream in individuals with ASD found enhanced fine-form (local) processing in the primary visual cortex and deficits in gestalt face-processing in the fusiform gyrus (Yamasaki et al, 2017). These studies may relate to our findings, suggesting enhanced local processing in individuals with ASD.
The results of our study appear to support a focal–local attentional processing bias in individuals with ASD. However, these results are the opposite of what would be expected for spatial orientation being a factor in the mouth versus eye preference that is typically exhibited in individuals with ASD. If the greater upward bias in the top quadrisection tasks was impacting facial scanning, then studies should have observed greater eye gazing and less mouth gazing in the individuals with ASD. Because this is not the case, there must be other factors contributing to the atypical facial scanning in the individuals with ASD, such as a decrease in social salience of the eyes.
Future studies of individuals with ASD are needed to further investigate the upward vertical bias during quadrisection tasks reported here, as this bias might have other impacts on visuospatial perception. However, one potential implication of this study is that efforts to train individuals with ASD to increase eye contact by training them to look upward, such as by using methods like prism adaptation for individuals who have spatial neglect caused by stroke (Barrett et al, 2012), might not be beneficial for individuals with ASD. Additionally, future studies in larger samples would need to thoughtfully place these findings into context of the high degree of heterogeneity of ASD (Beversdorf et al, 2016), as findings may vary in subsets of this heterogeneous patient population.
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