Elsevier

Neuropsychologia

Volume 99, May 2017, Pages 12-23
Neuropsychologia

Altered perceptual pseudoneglect in ADHD: Evidence for a functional disconnection from early visual activation

https://doi.org/10.1016/j.neuropsychologia.2017.02.022Get rights and content

Highlights

  • Perceptual pseudoneglect is altered in ADHD independent of deficits of vigilance.

  • Pixel noise increases leftward biases of attention via sensory activation.

  • Attention deficits in ADHD might reflect a disconnection syndrome.

Abstract

Novel insights into the right-brain dominant functions of spatial attention and visual awareness may come from the peculiar observation that the attentional bias to the left in healthy individuals, called “pseudoneglect,” increases with visual noise superimposed onto test stimuli. However, it is unclear if this effect originates from noise activating early visual areas or causing higher-level cognitive interference. Cognitive distraction and load are known to induce neglect-like rightward biases in attention deficit hyperactivity disorder (ADHD). Therefore, here we tested pseudoneglect in 21 adults with ADHD using a grating-scales task (GST) in a high (HI) and a low (LO) spatial-frequency condition with superimposed pixel noise. As expected, we found that healthy participants (n =32) displayed a “cross-over” of HI vs. LO biases that increased significantly with noise. However, the ADHD group exhibited no pseudoneglect or cross-over, and noise caused neither rightward nor leftward biases. Furthermore, ADHD individuals produced psychometric functions with normal slopes, indicating normal perceptual sensitivity. Our results show that pseudoneglect is altered in ADHD, but that pixel noise induces no neglect-like rightward biases as this would be expected if pixel noise caused cognitive interference. This suggests that pixel noise has a bottom-up perceptual effect on pseudoneglect. What is more, individuals with ADHD seem to lack activation of attentional functions via sensory stimulation despite intact visual processes. Our study adds to the growing literature of right hemisphere pathology in ADHD and the understanding of sensory noise as an activating factor of visuospatial attention and awareness.

Introduction

Seemingly paradoxically, pseudoneglect encompasses a variety of imperfections of spatial attention and visual awareness that are a signature feature of the normally functioning brain and that can be described as a subtle but robust leftward attentional bias commonly observed in the normal population (Bowers and Heilman, 1980; Jewell and McCourt, 2000). That is, healthy individuals show pseudoneglect in visuospatial tasks where they prefer stimuli on the left side to those on the right. For example, in the line bisection task they set the mark slightly to the left of the true midline (Binder et al., 1992, McCourt and Jewell, 1999, Schenkenberg et al., 1980). Similarly, they prefer the left side in perceptual tasks that require judgments of horizontal brightness gradients (“greyscales task”; Mattingley et al., 2004; Mattingley et al., 1994), spatial frequencies (“grating-scales task”; Niemeier et al., 2007), distance or size (“landmark task”; Benwell et al., 2013; Harvey and Milner, 1995), and numerosity (Nicholls et al., 1999). These biases have been found to be systematically influenced by several intrapersonal factors such as age, sex, and handedness (for a review Jewell and McCourt, 2000). Further, pseudoneglect is not restricted to the visual domain. Tactile tasks also reveal biases to the left (Brooks et al., 2011a) as well as tasks that involve mental representations and imagery (Bourlon et al., 2011, Brooks et al., 2011b, Dehaene et al., 1993, Della Sala et al., 2006, Dickinson and Intraub, 2009, Friedman et al., 2012, Loftus et al., 2009, McGeorge et al., 2007; for a review: Brooks et al., 2014). These different forms of pseudoneglect may be in part due to different underlying processes.

Nevertheless, generally speaking the processes underlying pseudoneglect appear to involve functions of attention and awareness that are predominantly associated with the right hemisphere (McCourt et al., 2005), because right-brain damage causes spatial neglect, a severe deficit of visual attention and spatial awareness (Karnath et al., 2004, Mort et al., 2003, Verdon et al., 2010) that produces pathological biases to the right, complementary to the biases observed in pseudoneglect (e.g., McCourt and Jewell, 1999). What is more, pseudoneglect interacts with exogenous forms of attention in that cues on the right side reduce leftward biases, whereas cues on the left do not increase them (Bultitude and Aimola Davies, 2006, McCourt et al., 2005, Singh et al., 2011; for other attentional phenomena, e.g., Toba et al., 2011). This indicates that pseudoneglect reflects an underlying asymmetry in attentional functions rather than perceptual asymmetries (for a discussion see McCourt et al., 2005). For example, there is at times a concern that lateral attentional cues have non-attentional effects in that perception groups the cues and test stimuli into gestalts that as a whole have a shifted midpoint that alters responses (Brooks et al., 2011b). However, this perceptual grouping cannot explain the fact that cueing effects can be very specific in that the cues interact with pseudoneglect (see above) as measured with the recently developed grating-scales task (GST; Niemeier et al., 2007) but only in one of its two conditions. In the control condition of the GST cues show additive cueing effects in that the magnitude of the effect does not depend on the lateral position of the cue (Singh et al., 2011; also see below).

However, the specific neural and computational mechanisms of attention underlying pseudoneglect remain incompletely understood. In terms of neural structures, several imaging studies have found that pseudoneglect involves dorsal parietal regions, such as the intraparietal sulcus (Cavézian et al., 2012, Ciçek et al., 2009, Fink et al., 2000, Foxe et al., 2003, Waberski et al., 2008) that constitute portions of the dorsal attentional network (“DAN”, e.g., Corbetta and Shulman, 2002; Mesulam, 1999). However, to some extend the results may reflect contrasts of pseudoneglect tests with unspecific control tests (e.g., see control analysis in Le et al., 2015) that include functions that merely co-occur with the core processes of pseudoneglect. One example is that experimental and control tasks can greatly differ in the afforded distribution of attention and the manner in which stimuli are scanned by attention (also see McCourt and Jewell, 1999, who used masking to show that biases do not change when scanning is prevented). Furthermore, lesions in the DAN appear to rarely cause spatial neglect whereas damage to the right-brain dominant ventral attentional network (VAN) might trigger a significant breakdown of right-brain attentional functions (Corbetta and Shulman, 2002, He et al., 2007). Consistent with the idea that pseudoneglect involves ventral areas are the results of two recent EEG studies (Benwell et al., 2014, Le et al., 2015). Also, studies using intracranial stimulation (Thiebaut de Schotten et al., 2005, Vallar et al., 2014) and anatomical studies (Thiebaut de Schotten et al., 2011) suggest that postero-frontal fiber tracts targeting ventral regions in right frontal cortex may be associated with the attentional asymmetries of pseudoneglect.

To conceptualize the computational processes underlying pseudoneglect and neglect, the activation-orientation hypothesis can serve as a helpful start point (e.g., Kinsbourne, 1987; Reuter-Lorenz et al., 1990). It proposes that each hemisphere generates a contralateral attentional bias and that these biases, governed by sensory stimulation, operate in a mutually inhibitory fashion thereby determining a net attentional bias that is reflected in a directional vector of attentional orienting (Kinsbourne, 1987). In support of this idea there now is very good evidence for interhemispheric competition underlying attentional mechanisms (e.g., Hilgetag et al., 2001, Koch et al., 2008, Le et al., 2015, Vesia et al., 2015).

However, several aspects of the hypothesis remain unclear or require updates. One is the model's assumed behavioural output feature of orienting (i.e., shifting one's attention and overt behaviour in some direction away from the current fixation point). The assumption implies that right-brain damaged patients with neglect should continuously direct overt attention further and further to the right side and, thus, engage in clockwise spinning behaviour. However, there is no evidence that patients do turn around their axis. Even when seated in a spherical, uniformly textured environment patients turn their heads and eyes not much further than 45 degrees to the right, well within the range of space that they could scan comfortably (Karnath et al., 1998). Furthermore, the patients’ spontaneous gaze shifts do not reveal a cascadic pattern of rightward saccades (Niemeier and Karnath, 2000, Niemeier and Karnath, 2003). Therefore, a system of attentional biases cannot operate in a merely directional fashion but seems to take body-centred (and possibly allocentric) coordinates into account (e.g., Li et al., 2014; Niemeier and Karnath, 2002, note though that there is still a dearth of evidence for the intact brain: Chen and Niemeier, 2014a, Rorden et al., 2001).

A second aspect of the activation-orientation hypothesis that requires further scrutiny are its interactions with sensory processes in terms of (a) the perceptual consequences of the attentional bias, and (b) the sensory (and cognitive) forms of stimulation that activate the biases in the two hemispheres in the first place. In both these contexts the recently developed grating-scales task (GST) offers new evidence.

The GST (Niemeier et al., 2007), derived from the greyscales task (Mattingley et al., 1994, Nicholls et al., 1999), presents pairs of horizontal bar-shaped gratings that smoothly increase in spatial frequency in opposite directions and that vary in asymmetry from trial to trial (Fig. 1). Each time participants judge this asymmetry either while they direct their attention to the gratings’ high or to their low spatial frequency (HiSF or LoSF) components. These components are placed at an eccentricity where the visual system shows marked differences in contrast sensitivity (Rovamo et al., 1978). Thus, when participants judge which of the two bars has the larger HiSF component (GST-HI task) they typically prefer the bar whose HiSF component is located on the left side, reflecting a leftward bias or pseudoneglect (Niemeier et al., 2007). In contrast, in the GST-LO task where participants judge which bar has a larger LoSF component they show no preference or smaller rightward biases (Chen and Niemeier, 2014b; Niemeier et al., 2008a). Consequently, across tasks participants might report the same bar as having a larger HiSF component, and paradoxically, also a larger LoSF component. What is crucial, the Hi and Lo biases and their differences have important properties: Only the Hi bias measures attention because only this bias interacts with attentional cues, as mentioned above (Singh et al., 2011). Nevertheless, Hi and Lo biases are positively correlated, that is, people with strong leftward Hi biases tend to have smaller rightward Lo biases and vice versa. Hence, the GST-Lo is an excellent control task for the GST-Hi with the Hi/Lo difference revealing differences in activation in ventral cortical regions (Le et al., 2015). Finally, the effect size of the Hi/Lo difference in biases increases when certain proportions of pixels of the test stimuli are set to random levels of noise, similar to a TV image with poor reception (Chen and Niemeier, 2014b; Niemeier, Singh, Keough, & Akbar, 2008b). This opens the possibility for more detailed studies of the modestly sized pseudoneglect in the future.

These results obtained with the GST offer important new insights into the activation-orientation hypothesis (Reuter-Lorenz et al., 1990). As for the hypothesis’ assumed sensory consequences of pseudoneglect, initial ideas suggested that attention biased to one end of a stimulus might cause the stimulus to appear larger on that side so that, e.g., healthy people with a natural bias to the left bisect lines slightly too far to the left side (e.g., Reuter-Lorenz et al., 1990). A modified version of this idea compatible with pseudoneglect in tasks other than the landmark task (Mattingley et al., 1994, Nicholls et al., 1999, Niemeier et al., 2007) might suggest that attention increases the apparent spatial resolution of visual stimuli. Indeed there is evidence for such an effect of attention (Carrasco and Yeshurun, 1998, Gobell and Carrasco, 2005). However, increased spatial resolution cannot be a significant component of the perceptual consequences of pseudoneglect because it would imply that the Hi and Lo biases in the GST are negatively correlated, contrary to our observations (Chen and Niemeier, 2014b, Singh et al., 2011). Instead, biased attention might alter apparent salience (Singh et al., 2011) although more research is needed to confirm this possibility.

Finally and most relevant for the current study, the activation-orientation hypothesis does not specify what sensory (and/or cognitive) forms of stimulation activate the biases in the two hemispheres. With respect to the GST, Hi biases differ from Lo biases because spatial frequencies at certain visual eccentricities differ in perceptibility (Rovamo et al., 1978). Nonetheless, additional factors likely play a role as well and require further investigation (for a systematic model discussion of “one-mechanism” and “two-mechanisms models” see Chen and Niemeier, 2014b). For the current study however, we have focused on the pixel noise effect that increases the difference between Hi and Lo biases (Chen and Niemeier, 2014b, Niemeier et al., 2008a; also see Valadao et al., 2010; see Cattaneo et al., 2012 for opposite effect of auditory white noise on visual and haptic pseudoneglect). The finding is significant for methodological reasons because pixel noise can help neuropsychological studies of pseudoneglect to increase their (often modest) effect sizes. Furthermore, the noise effect is conceptually relevant because it can help to narrow down the mechanisms that may underlie pseudoneglect. Given these benefits of the noise effect, future progress critically depends on clarifying how pixel noise causes pseudoneglect to increase.

In principle, the noise effect could be conveyed through basic visual processes (sensory activation assumption) or through higher-level, cognitive functions (cognitive interference assumption). In support of the former assumption, pixel noise could influence attentional biases via basic visual processes because noisy pixels create visual features such as small, disjointed edges that increase neural activity in the early visual cortex. Indeed, there is evidence that noisy images with reduced higher-order correlations excite neurons in early visual areas (Kayser et al., 2003; Murray et al., 2002) and this greater activation could snowball into greater right-brain dominance via interhemispheric competition (Hilgetag et al., 2001, Kinsbourne, 1977, Le et al., 2015, Vesia et al., 2015).

On the other hand, pixel noise could bias attention via higher-level cognitive processes (cognitive interference assumption). That is, the noise might trigger unwanted cognitive processes, for example the noise could attract attention such that participants involuntarily engage in an activity of scrutinizing the noisy pixels and direct less cognitive resources to the main task, i.e., the GST. In essence the noise would cause participants to engage in a secondary task that creates cognitive interference with the actual task. Arguably, cognitive interference is fundamentally different from sensory activation and associated sensory interference because sensory processes can occur in a massively parallel, preattentive fashion (Treisman and Gelade, 1980). In contrast, a given cognitive task involves several processes (working memory, goal representations, etc.), each of which can only be dedicated to a single or very few different tasks so that it is difficult to pursue more than one task at the same time and perhaps impossible to pursue more than two (Charron and Koechlin, 2010). Therefore, if pixel noise impinged on cognitive resources it might trigger executive functions in frontal areas to deal with the cognitive interference. These functions could be right-dominant themselves (e.g., Bunge et al., 2002; Bush and Shin, 2006; Bush et al., 2000; Heckers et al., 2004; Leung et al., 2000) or they could set off interhemispheric competition and this way lead to greater right-brain activation as mentioned above. Consistent with an influence of higher-level functions, pseudoneglect has been recently suggested to involve ventral posterior as well as frontal cortex (Le et al., 2015), and the connecting fibre tracts (Thiebaut de Schotten et al., 2005, Thiebaut de Schotten et al., 2011, Vallar et al., 2014). Furthermore, neglect after right frontal damage can be exacerbated by distractors (Husain and Kennard, 1997), although this was shown only in a single patient and only for neglect in cancellation tasks which could be different from neglect in the line bisection task and in similar perceptual judgment tasks (Verdon et al., 2010).

To test whether perceptual forms of pseudoneglect vary with cognitive distraction, here we studied individuals with attention deficit hyperactivity disorder (ADHD) who have trouble with various forms of cognitive interference. For example, they perform poorly in tasks that are presented in the context of incongruent stimuli such as the Stroop task (e.g., Lansbergen et al., 2007), or the flanker as well as the Simon task (Mullane et al., 2009). These difficulties may be related to deficits in maintaining attentional control (Mason et al., 2005), and in ecologically valid settings they may reduce sustained attention (Adams et al., 2009). Also, salient attentional distracters such as novel sounds cause higher omission rates in visual discrimination tasks as well as altered electrophysiological patterns (Gumenyuk et al., 2005), and auditory and visual distraction impacts short-term recall in ADHD (Higginbotham and Bartling, 1993). What is more, a secondary task presented centrally to cause cognitive interference impacts detection of transient stimuli more in the left than the right periphery, resembling symptoms in patients with neglect after brain damage (Bellgrove et al., 2013; also see Silk et al., 2014) (consistent with these observations, it has been suggested that ADHD is associated with impaired engagement of right fronto-striatal, fronto-parietal, and fronto-cerebellar networks with the caveat that numerous other anomalies are found; Cubillo et al., 2010; Konrad and Eickhoff, 2010; Rubia et al., 2010; Schneider et al., 2010).

Neglect-like symptoms (or at least the absence of pseudoneglect) in ADHD have been also shown in cancellation tasks (Jones et al., 2008, Manly et al., 1997, Sandson et al., 2000, Voeller and Heilman, 1988) and in the line bisection task (Manly et al., 1997; Sheppard et al., 1999; Waldie and Hausmann, 2010). However, evidence is not always consistent (Ben-Artsy et al., 1996) perhaps because deficient pseudoneglect in ADHD becomes more apparent in studies that require participants to sustain attention for longer stretches of time (George et al., 2005). Because such a time-on-task effect on pseudoneglect is well documented for healthy individuals as well (Benwell et al., 2013, Manly et al., 2005, Matthias et al., 2009) it casts doubt on the idea that the functions underlying pseudoneglect are actually altered in ADHD. Alternatively, altered pseudoneglect could be due to greater difficulties sustaining attention in ADHD (Adams et al., 2009). Furthermore, Klimkeit et al. (2003) have argued that pseudoneglect shows up only when pseudoneglect tests have a motor component but not in perceptual measures. However, these authors tested children with and without ADHD who might show greater variability in their responses and poorer signal to noise ratios.

Therefore, the first objective of the present study was to revisit the question whether perceptual pseudoneglect is altered in ADHD by testing young adults without impacting their sustained attention. We predicted that individuals with ADHD would show less pronounced leftward biases than control subjects or even rightward biases in the GST-HI. Further, we predicted that the ADHD group would exhibit difficulties with performing the GST (HI and LO), that is, poor perceptual sensitivity revealed through “flat” psychometrical functions (Section 2.5 for how to measure task difficulty or sensitivity). Our second and theoretically crucial objective was to utilize the results in the ADHD group to better understand the pixel noise effect in the GST (Chen and Niemeier, 2014b, Niemeier et al., 2008a) and, thus, to attain a better understanding of the forms of stimulation that activate the functions of attention underlying pseudoneglect (e.g., Reuter-Lorenz et al., 1990) so as to inform future models of pseudoneglect and neglect. Our rationale was that if the cognitive interference assumption was correct, then people with ADHD should exhibit rightward biases in the GST-HI that increase with increasing levels of noise just like cognitive interference has been previously demonstrated to bias attention to the right in ADHD (Bellgrove et al., 2013, Silk et al., 2014). Alternatively, if pixel noise did not increase rightward biases in ADHD, this would argue against the cognitive interference assumption and in favour of the sensory activation assumption. Our data support the latter hypothesis. Further, the data suggest that perceptual forms of pseudoneglect are altered in ADHD, independent of difficulties with sustained attention and that ADHD might be characterized by functional disconnection that creates a lack of visual activation of attentional processes.

Section snippets

Participants

Twenty-one students (current enrolment in University of Toronto) with ADHD ranging in age from 19 to 27 years (6 males; median age =21 years) were recruited from University of Toronto Student Services. Another 32 undergraduate students recruited from the University of Toronto at Scarborough served as control participants (8 males; median age =19 years; 6 additional control subjects were excluded because they exhibited high “ADHD scores” in the ASRS-A scale, also see below). All participants

Neuropsychological assessment

Table 1 provides a summary of demographic data for every subject in the ADHD group. Table 2A, Table 2B, Table 2C presents group information of the Edinburgh Handedness Inventory (EHI), the ASRS, and the MoCA. As expected, there was no group difference on the Laterality Quotient: t (51) =−0.347, p=0.730. One-way ANOVA showed the ADHD group scored significantly higher on the ASRS-A compared to the control group, F (1, 51) =20.83, p<0.001, η2 =0.29, observed power =0.994. No group differences were

Discussion

Pseudoneglect, and therefore spatial neglect, remains incompletely understood. Importantly, it is unclear what tasks or stimuli activate the right-brain dominant mechanisms of attention and awareness underlying pseudoneglect. As recently shown, pixel noise superimposed onto test stimuli can increase overt biases to the left in healthy participants (Chen and Niemeier, 2014b, Niemeier et al., 2008a), either because pixel noise causes sensory activation (sensory activation assumption) or because

Acknowledgements

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). We thank Adam Frost and Lawrence Guo for comments on an early version of this manuscript.

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