Cross-modal influences on attentional asymmetries: Additive effects of attentional orienting and arousal

Neuropsychologia 96 (2017) 39–51

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Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia

Cross-modal influences on attentional asymmetries: Additive effects of attentional orienting and arousal☆

MARK

⁎

Nicole A. Thomas , Alexander J. Barone, Alexandra H. Flew, Michael E.R. Nicholls School of Psychology, Flinders University, Adelaide, Australia

A R T I C L E I N F O

A BS T RAC T

Keywords: Pseudoneglect Auditory distractors Lateral biases Landmark task Distractibility

Attention is asymmetrically distributed across the visual field, such that left side stimuli are more salient, which causes a spatial bias known as pseudoneglect. Although auditory cues can be used to direct visual attention to a location, the influence of auditory distractors on visuospatial asymmetries remains unknown. We examined whether attentional orienting or arousal effects occur when either left or right auditory distractors are presented during the landmark task. We also categorised participants based on the baseline direction of pseudoneglect. Experiment 1 showed a strong attentional orienting effect. A slightly weaker arousal effect was also observed. Interestingly, these effects appear to be additive, such that infrequent right ear distractors rendered leftward biases non-significant. A second experiment, using centralised auditory distractors, was conducted to isolate the role of arousal. A strong arousal effect occurred, which was mediated by baseline direction of pseudoneglect. Left- and right-responders showed parallel decreases in the strength of attentional asymmetries, as biases decreased in the presence of distractors. Importantly, these decreases were not accompanied by an increase in accuracy. We conclude that both attentional orienting and arousal mechanisms contribute to the cross-modal integration of auditory and visual information during visuospatial processing, with the role of attentional orienting being more dominant.

1. Cross-modal influences on attentional asymmetries: additive effects of attentional orienting and arousal Everyday, we are faced with an overwhelming amount of information. Although we are able to accurately direct our attentional resources toward stimuli of interest, our ability to control our attention is not perfect and distractors interfere with our capacity to perform tasks successfully. The way in which we distribute spatial attention affects how we perceive characteristics of the environment, such that some information is overattended, while other stimuli are ignored (Nicholls et al., 2004). Damage to the right hemisphere, particularly the superior temporal gyrus and temporoparietal junction, can lead to an attentional imbalance where the right side is overattended, which is referred to as hemispatial neglect (Adair and Barrett, 2008; Behrmann et al., 2004; Corbetta and Shulman, 2011; Heilman and Valenstein, 1979; Karnath and Rorden, 2012; Marotta, McKeef, and Behrmann, 2003; Vallar and Perani, 1986). These attentional imbalances can be quite severe,

causing sufferers great difficulty in carrying out everyday tasks, such as getting dressed or reading a clock (Marotta et al., 2003). Although left hemisphere damage can lead to neglect-type symptoms, the frequency of right neglect is much lower (Beis et al., 2004; Kleinman et al., 2007; Vallar et al., 1991). Egocentric neglect, which more often results from right hemisphere damage (Hillis et al., 2005; Kleinman et al., 2007), is an analogue for the attentional asymmetries that are observed amongst healthy individuals, known as pseudoneglect (Bowers and Heilman, 1980). Pseudoneglect is a small, but reliable, asymmetry in the distribution of attention, where attention is preferentially directed toward the left side (Bowers and Heilman, 1980; Jewell and McCourt, 2000; Nicholls et al., 2012; Thomas et al., 2016). Although a variety of tasks show similar attentional asymmetries (Learmonth et al., 2015), the most commonly used tasks are line bisection (see Jewell and McCourt, 2000 for a review) and the landmark task (Nicholls et al., 2012; Thomas et al., 2012; Thomas et al., 2015; Thomas et al., 2016). When performing the landmark task, participants determine whether the left

☆ Although participants were able to listen to the sounds an unlimited number of times in the pilot study, none of the participants listened to any of the tones more than 5 times, which is significantly less than the 216 times that participants in Experiment 1 were exposed to the auditory distractor. The aim of this pilot experiment was to identify a sound with the potential to create maximal distraction during the experiment. Given that participants in the actual experiment repeatedly heard the same tone, it was not plausible to entirely eliminate the possibility of habituation; however, our goal was to minimise its likelihood. ⁎ Correspondence to: School of Psychology, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia. E-mail address: nicole.thomas@flinders.edu.au (N.A. Thomas).

http://dx.doi.org/10.1016/j.neuropsychologia.2017.01.002 Received 24 June 2016; Received in revised form 21 December 2016; Accepted 4 January 2017 Available online 05 January 2017 0028-3932/ © 2017 Elsevier Ltd. All rights reserved.

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(Behrmann et al., 2004; Calvert, 2001; Driver and Spence, 1998; Spence, 2011). For example, auditory cues improve visual target detection by directing attention towards a particular spatial location (Driver and Spence, 1998; Macaluso et al., 2003). Further, an uninformative sound presented shortly before a visual stimulus speeds up processing (Keetles and Vroomen, 2011). In contrast, sounds presented during a visual temporal order judgment task negatively affected performance (Morein-Zamir et al., 2003), which suggests auditory and visual information might not always be used in concert and auditory information can slow visual processing if it creates distraction. Both cues and distractors can create hemispheric imbalances by differentially engaging the left and right hemispheres and subsequently influencing the magnitude and direction of pseudoneglect (Bultitude and Aimola Davies, 2006; McCourt et al., 2005; McCourt and Jewell, 1999; Milner et al., 1992; Nicholls et al., 2012; Thomas et al., 2015, 2016). Cues signal upcoming information, allowing individuals to interpret the significance of the cue, based on prior knowledge and experience, and decide upon an action. Further, a cue is a stimulus that is designed to encourage participants voluntarily and deliberately shift their attention (i.e., overtly attend to; Munneke, Van der Stigchel, and Theeuwes, 2008; Posner, 1980; Thomas et al., 2015, 2016). In contrast, a distractor is a stimulus that decreases one's ability to pay attention by preventing focus and decreasing the receipt of incoming information. Distractors, which are generally uninformative, automatically and involuntarily shift our attention (this can be overt or covert; Munneke et al., 2008; Schreij et al., 2008; Theeuwes, 1992; Theeuwes et al., 1998; Thomas et al., 2015). Distractors differ from cues in that they are task-irrelevant, do not provide any predictive information, and participants are instructed to ignore them (Corral and Escera, 2008; Escera et al., 1998; Schroger and Wolff, 1998; Thomas et al., 2015, 2016). This difference has been clarified by recent work, which highlights the fact that cueing a distractor reduces distractor interference by providing advance knowledge of its spatial location (Munneke et al., 2008; Ruff, 2006, Van der Stigchel and Theeuwes, 2006; Van der Stigchel et al., 2006). Peripheral stimuli have the ability to affect task performance by influencing either attentional orienting or arousal (Max et al., 2015). Orienting attention toward a distractor causes a performance decrease, as distractors are non-informative and task-irrelevant. In contrast, by increasing arousal, a task benefit could be expected, as performance should improve in the presence of the alerting stimulus. To date, there is evidence for both attentional orienting and arousal effects on attentional asymmetries, which raises the question of whether it might be possible to dissociate these effects.

or the right side of a pre-transected line is longer. Most often, the left side of the line is chosen as being longer, as this side of the stimulus receives more attention, and consequently becomes perceptually elongated (Nicholls et al., 2012; Thomas et al., 2012, 2015, 2016). Kinsbourne 1970 (see also Reuter-Lorenz et al., 1990) developed the activation-orienting hypothesis, which argued that cognitive functions are asymmetrically represented, and competing activations between the left and right hemispheres determine lateralisation. Activation within the right hemisphere during visuospatial attention tasks (Corbetta and Shulman, 2011; Corbetta et al., 1995; Fink, Marshall et al., 2001) causes an attentional bias towards the contralateral (i.e., left) hemispace (Kinsbourne, 1970). Although the right hemisphere predominantly attends to the left side, this hemisphere is able to direct attention to both sides of space, whereas the left hemisphere only directs attention to the right side (Corbetta and Shulman, 2011; Reuter-Lorenz et al., 1990). Neuroimaging data show preferential activation of the intraparietal sulcus, temporoparietal junction, and lateral peristriate cortex within the right hemisphere during visuospatial attention tasks (Çiçek et al., 2009; Fink et al., 2000, 2001; Foxe et al., 2003; Zago et al., 2017). Specifically, Thiebaut de Schotten et al. (2011) showed that larger parieto-frontal connections in the right hemisphere, compared to the left, led to more leftward line bisection errors. More recently, Zago et al. (2017) found a positive correlation between rightward cerebral activity and the degree of leftward asymmetry on line bisection. Techniques that directly manipulate hemispheric activation, such as transcranial magnetic stimulation (Bjoertomt et al., 2002; Hilgetag et al., 2001) and direct current stimulation (Loftus and Nicholls, 2012), demonstrate the interhemispheric competition that underlies attentional asymmetries. As the same cortical areas are implicated in pseudoneglect and hemispatial neglect (Corbetta and Shulman, 2011; Marotta et al., 2003; Vallar and Perani, 1986), similar neural mechanisms are believed to underlie these phenomena (McCourt and Jewell, 1999; Nicholls et al., 2005; Nicholls and Roberts, 2002). Corbetta and Shulman (2011) proposed that attentional asymmetries are the result of an interaction between two separate frontoparietal networks: a bilateral dorsal attention network, which controls visuospatial attention across space, and a right-lateralised ventral attention network. The ventral attention network modulates interhemispheric rivalry in the dorsal orienting network (Corbetta and Shulman, 2011), biases the dorsal network towards novel stimuli and is strongly associated with attentional load and arousal (Duecker and Sack, 2015; Thiebaut de Schotten et al., 2011). Decreasing activation within the right lateralised ventral network causes a global decrease in right hemisphere activation, which affords the left dorsal network a competitive advantage and biases attention to the right side (Corbetta and Shulman, 2011; Duecker and Sack, 2015). The imbalance between these two attentional networks explains why hemispatial neglect if most prevalent following right hemisphere damage (Husain and Rorden, 2003), and also provides a neuroanatomical explanation for pseudoneglect (Thiebaut de Schotten et al., 2011). The parietal cortex, which is located between the auditory and visual cortices (Behrmann et al., 2004; Fink et al., 2000, 2001), is not only involved in visuospatial attention, but also plays an important role in cross-modal integration. The anterior intraparietal sulcus has been implicated in cross-modal integration, specifically of visual and auditory information during spatial processing (Behrmann et al., 2004; Macaluso et al., 2003); this area also produces eye movements and performs attentional shifts (Behrmann et al., 2004). As the intraparietal sulcus has been linked to both hemispatial neglect (Behrmann et al., 2004; Corbetta et al., 2000; Husain and Rorden, 2003; Mesulam, 1981) and pseudoneglect (Çiçek et al., 2009; Fink et al., 2000, 2001; Foxe et al., 2003), engaging cross-modal processing could improve attentional asymmetries. Prior research employing both auditory and visual stimuli illustrates that cross-modal stimuli can enhance visual processing

1.1. Attentional orienting effects Prior research has demonstrated that visually cueing the left and right ends of a line causes an attentional shift towards the cued side, which results in increased salience and subsequent overestimation of the length of the cued side (Chieffi et al., 2014; Harvey et al., 1995; McCourt et al., 2005; McCourt and Jewell, 1999; McCourt and Olafson, 1997; Milner et al., 1992; Nichelli et al., 1989; Nicholls et al., 2005; Pizzamiglio et al., 1990; Reuter-Lorenz et al., 1990). The influence of auditory cues is less clear. Sosa, Clarke, and McCourt (2011) examined the influence of auditory and visual cues, both in conjunction and independently, to determine whether audiospatial cues bias visual attention. They demonstrated that visual cues are more potent than auditory cues in the left hemispace, whereas visual and auditory cues are equally influential in the right hemispace. Overall, both visual and auditory cues can direct attentional resources toward their spatial location, with left side cues increasing pseudoneglect and right side cues leading to a decrease. Visual distractors also influence attentional asymmetries (Nicholls et al., 2012; Thomas et al., 2015, 2016). Distractors that either precede (Nicholls et al., 2012; Thomas et al., 2015) or are presented in 40

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1989; Nicholls et al., 2005; Pizzamiglio et al., 1990; Reuter-Lorenz et al., 1990; Sosa et al., 2011). Certainly the relationship between arousal and performance is multidimensional, with peak performance occurring when arousal levels are at 60–70% (Arent and Landers, 2003). Although some research suggests that task irrelevant emotion information negatively influences performance by distracting participants (Hindi Attar et al., 2010; Most et al., 2005; Most et al., 2007), there is a great deal of evidence that suggests arousing images and words, particularly if they are negative, provide a performance benefit (Lungberg and Parmentier, 2012; Okon-Singer et al., 2013; Max et al., 2015; Zeelenberg and Bocanegra, 2010). Importantly, the argument can be made that stimuli that signal general situational awareness, regardless of their taskrelevance, have the ability to keep attentional resources focussed on the current task (Okon-Singer et al., 2013). As such, there is sufficient evidence to support the possibility of a performance increase when arousal is increased. Furthermore, a number of studies have shown that infrequent auditory distractors lead to an increase in task performance as a result of their higher salience (Ruhnau et al., 2010; San Miguel et al., 2010a, 2010b; Wetzel et al., 2012; Zink et al., 2003). The saliency of infrequent distractors causes an increase in nucleus accumbens activity (Zink et al., 2003) and dopamine release (Horvitz, 2000). Elevations in dopamine also correspond with increases in arousal (Horvitz, 2000). As the same neural areas (e.g., the amygdala) are activated by uncertainty, novelty, salience, and arousal (Blackford et al., 2010; Ewbank et al., 2009; Kensinger and Schachter, 2006; Lewis, Critchley et al., 2007; Mendes et al., 2007; Weierich et al., 2010), it is plausible that infrequent and therefore more salient distractors, will increase arousal. If auditory distractors influence arousal, a difference should emerge based on distractor frequency; asymmetries should be stronger for infrequent distractors (i.e., closer to no asymmetry) relative to the frequent distractors. Fatigue decreases leftward biases (Bellgrove et al., 2004; Benwell et al., 2013; Dodds et al., 2008; Dodds et al., 2009; Dufour et al., 2007b; Fimm and Blankenheim,, in press; Manly et al., 2005; Newman et al., 2013; Paladini et al., in press), and arousal increases activity within the right lateralised ventral attention network (Corbetta et al., 2008; Corbetta and Shulman, 2011), which suggests that increased arousal should also exacerbate leftward biases. This would be consistent with prior work looking at the role of arousal in both neglect and pseudoneglect (Benwell et al., 2013; Dodds et al., 2008; Dodds et al., 2009; Dufour et al., 2007b; Fimm and Blankenheim,, in press; Husain and Nachev, 2007; Manly et al., 2005; Mukand et al., 2001; Newman et al., 2013; Paladini et al., in press; Peers et al., 2006; Pérez et al., 2009).

conjunction with line stimuli (Thomas et al., 2016) exacerbate pseudoneglect, therefore influencing both preparatory and exogenous attention (Thomas et al., 2016). In addition, distractors that automatically capture attention, such as brief flashes of light (Jonides, 1981; Klein et al., 1992), differentially influence asymmetries in relation to the direction of pseudoneglect at baseline (Thomas et al., 2016). 1.2. Arousal effects Arousal significantly influences pseudoneglect (Dodds et al., 2008, 2009; Dufour et al., 2007b; Manly et al., 2005; Peers et al., 2006; Pérez et al., 2009) by increasing activation within the right lateralised ventral attention network (Corbetta, Patel, and Shulman, 2008; Corbetta and Shulman, 2011), which controls vigilance and alertness (Paus et al., 1997; Sturm and Willmes, 2001). This increased demand on the ventral network causes a global decrease in right hemisphere activation as the inter-hemispheric rivalry in the bilateral dorsal orienting network becomes deregulated (Corbetta et al., 2008; Corbetta and Shulman, 2011; Coull, Frackowiak, and Frith, 1998; Husain and Nachev, 2007; Pardo et al., 1991; Sturm et al., 1999, 2004). The left dorsal orienting network then possesses a competitive advantage that drives attention rightward (Corbetta and Shulman, 2011). Amongst neglect patients, both increased alertness and psychostimulants reduce left inattention, whereas sedatives exacerbate this asymmetry (Fleet et al., 1987; Geminiani et al., 1998; George et al., 2008; Grujic et al., 1998; Lazar et al., 2002; Malhotra et al., 2006; Mukand et al., 2001; Robertson et al., 1998). Indeed, presenting sounds simultaneously with visual stimuli also improves detection of previously neglected visual targets amongst hemispatial neglect patients (Frassinetti et al., 2002). Further, both tonic and phasic alertness training temporarily improves hemispatial neglect symptoms (Chica et al., 2011; DeGutis and Van Vleet, 2010; Thimm et al., 2006). In healthy populations, the effects of fatigue and time-on-task have also been explored. Across a growing number of studies, it has been shown that leftward biases decrease as a result of sleeplessness as well as timeon-task (Bellgrove et al., 2004; Benwell et al., 2013; Dodds et al., 2008; Dodds et al., 2009; Dufour et al., 2007b; Fimm and Blankenheim,, in press; Manly et al., 2005; Newman, O’Connell, and Bellgrove, 2013; Paladini et al., in press). Research examining the effects of heightened arousal amongst healthy individuals is currently lacking. Given that activation within the right lateralised ventral attention network is increased by arousal, it is plausible that pseudoneglect will be increased in situations of heightened arousal. To date, the influence of auditory distractors on attentional asymmetries remains unexplored. To determine whether attentional orienting or arousal effects might be stronger, we presented auditory distractors to the left and right ears separately. This manipulation allowed us to determine whether auditory distractors influence attentional orienting, or whether they serve a more generalised arousal function. The predictability of audiospatial location is important (Matusz et al., 2016), in that task-irrelevant sounds must be spatially unpredictable to avoid habituation and remain distracting. Therefore, we presented auditory stimuli asymmetrically between the ears to decrease predictability. In one condition, 78% of distractors were presented to the left ear and 22% were presented to the right and vice versa in the other condition. If auditory distractors influence attentional asymmetries by orienting attention toward their audiospatial location, left ear distractors should increase pseudoneglect, whereas right ear distractors should decrease pseudoneglect. In this instance, distractor frequency should not influence asymmetries, as the ear of presentation should be the predominantly influential factor. Such an effect would mirror prior work examining the role of auditory and visual cues (Chieffi et al., 2014; Harvey et al., 1995; McCourt et al., 2005; McCourt and Jewell, 1999; McCourt and Olafson, 1997; Milner et al., 1992; Nichelli et al.,

2. Method 2.1. Participants Thirty-six undergraduate Flinders University students (8 males, Mage =21.06, SD =3.79) completed the experiment in exchange for either $15.00AUD or course credit. All participants had normal hearing, normal or corrected-to-normal vision, and were right-handed, as measured by the FLANDERS handedness survey (M =9.81, SD =.58; Nicholls et al., 2013). The Flinders University Social and Behavioural Research Ethics Committee granted ethical approval and the experiment was performed in accordance with the ethical standards of the 1964 Declaration of Helsinki. 2.2. Apparatus Stimuli were presented on an LCD screen (470 mm×270 mm), at a distance of 500 mm, using E-prime 2.0 software (Psychology Software Tools, Inc.; www.pstnet.com/E- prime/e-prime.htm). An adjustable chin-rest controlled the viewing angle and ensured the eyes were in line 41

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Table 1 Pilot study statistics. Sound name

Mean rating

Standard deviation

Boing Sci-Fi Alarm Old Car Horn Sonar Digital Pinball

4.40 5.53 5.73 6.13 6.13 6.20 6.87

2.06 2.42 2.02 1.92 2.42 2.21 1.73t(14) = −2.47, p = .027, d = .34

Note. The main effect of auditory stimulus was significant (F(3.64, 50.98) =3.63, p=.013, η2 =.206). A paired-samples t-test was used to compare mean ratings for the two sounds with the highest ratings.

to consider how difficult it would be to ignore the tone when they were engaged in another task. We used this as our operational definition of distractibility. Ratings for each auditory stimulus were analysed to determine which stimulus was most distracting (see Table 1). The tone “Pinball” was given the highest mean rating (6.87 out of 10), indicating a moderate to high distractibility rating. This tone was edited to obtain two separate sound files: one left channel sound file, and one right channel sound file, allowing the tone to be presented to one ear at a time. Note that this process did not change the properties of the sound, only the side of the headphones in which it was heard. In the left ear condition, 78% of the sounds were presented to the left ear (n =84) and 22% to the right ear (n =24), and vice versa for the right ear condition.

Fig. 1. Visual depiction of the procedure. An example stimulus can be seen as part of this diagram.

with the middle of the screen. All participants wore Sennheiser HD 201 over ear headphones (108 dB SPL; 21–18000 Hz) during both silent and auditory trials. Participant responses were recorded using a model 200 A PST Serial Response Box, placed in line with the midsagittal plane. Participants were monitored via a closed-circuit video system to ensure they remained in the chin rest and completed the task without interruption (e.g., on their mobile phone).

2.4. Design 2.3. Stimuli A 3 (auditory distractor: silent, left ear, right ear) × 2 (polarity: black, white) × 6 (deviation: −2, −1, −.5, .5, 1, 2 mm) × 3 (line shift: left, centre, right) within-participants factorial design was used. As polarity and line shift were included to ensure a completely counterbalanced design, but were not factors of interest, they were not considered in the analyses. Three blocks of trials, separated by auditory distractor, were completed. The silent block was always completed first, to determine baseline performance. The order of the left and right ear auditory distractors blocks was counterbalanced across participants. The basic factorial combination (excluding auditory distractor) of 36 was repeated 3 times, resulting in 108 randomly presented trials per block, for a total of 324 trials. For the 24 infrequent trials, participants saw 4 trials at each deviation (6 levels), 12 trials of each polarity (2 levels), and 8 trials with each line shift (3 levels). Note that this was randomised and partially counterbalanced via Latin square method, as a complete counterbalance would have resulted in too many trials across the experiment.

2.3.1. Visual stimuli Pre-bisected lines consisted of diagonally opposite pairs of black and white segments (see Fig. 1; McCourt and Jewell, 1999), which were presented on a grey background. Half of the line was white on the top and black on the bottom, while the other half was black on top and white on the bottom. The location of black and white segments was counterbalanced, such that the black section appeared on the top left and on the top right an equal number of times. The point where the polarity of the line segments changed indicated the bisection point. Lines were 140 mm long (33° visual angle) and 2.1 mm high (.48°; Nicholls et al., 2012; Thomas et al., 2015). Six bisection points with deviations of 2 mm (.47°), 1 mm (.24°), and .5 mm (.12°) to the left and right of centre were used. Bisections were never located in the true centre, leading one side of the line to always be longer than the other. To eliminate the use of external cues in making bisection judgments, the horizontal location of the line was varied randomly across three locations: in the horizontal centre, or shifted .5 mm (.12°) to the left or right of centre.

2.5. Procedure

2.3.2. Auditory stimuli A pilot study (n =15) was conducted to select an auditory distractor. A stimulus that was not highly susceptible to habituation was desired. Although we wanted to examine the role of distractor frequency, we did not want participants to be able to easily ignore the distractor, even when it was frequent. For this reason, we did not want to use a stimulus that participants could easily habituate to. Seven Apple iPhone® tones were edited using Audacity® to create 250 ms auditory stimuli. As only 250 ms stimuli were used, the tones were not familiar to participants. Auditory stimuli were presented using Microsoft PowerPoint® as it allowed participants to control the pace of the experiment. Participants were able to listen to the sounds an unlimited number of times in order to maximise the validity of their ratings. A paper-pencil questionnaire was used to rate the distractibility of each auditory stimulus, on a scale from 1 “not distracting” to 10 “very distracting”. Participants were told

After obtaining informed consent, participants completed the FLANDERS handedness survey (Nicholls et al., 2013). Participants then completed the silent (baseline) block of trials, followed by the two blocks of auditory distractor trials. Each trial began with a fixation cross, which was presented for 500 ms, followed by a blank screen for 250 ms, which minimised visual aftereffects of the central fixation cross. In the silent condition, line stimuli then appeared for 250 ms, whereas, the line and auditory distractor were presented simultaneously for 250 ms in the auditory distractor conditions. Following the disappearance of the line, participants had a maximum of 2000 ms to indicate whether the left or the right side of the line was longer. A forced-choice paradigm was employed and each trial had a true correct response (i.e., one side of the line was always longer than the other). Participants responded with their right index finger on the rightmost response key when selecting the right side as longer and their 42

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left index finger on the leftmost response key for left longer responses. Participants were told to respond as quickly and as accurately as possible and response times (in ms) were recorded. Reponses that were too early (i.e., while the stimulus was visible), or too late (i.e., after 2000 ms), were rejected and repeated later in the block. In order to avoid intentional repetition of trials that were perceived to be difficult, participants were not informed that missed trials would be repeated.

× 2 (baseline direction: left-responder, right-responder) mixed-model ANOVA examined whether auditory distractors influenced response asymmetries. The interactions of ear by baseline direction, F(1,31) =.077, p=.784, η2 =.002; distractor frequency by baseline direction, F(1,31) =2.250, p=.144, η2 =.068; ear by distractor frequency by baseline direction, F(1,31) =3.067, p=.090, η2 =.090 were nonsignificant. Importantly, there were main effects of baseline direction, F(1,31) =25.506, p < .001, η2 =.451, ear, F(1,31) =11.337, p=.002, η2 =.268, and distractor frequency, F(1,31) =4.494, p=.042, η2 =.127. The main effect of baseline direction showed that left-responders differed from right-responders. Mean biases among left-responders remained significantly leftward for the auditory distractor trials, t(24) =6.032, p < .001, d =2.463, whereas biases among right-responders showed only a trend for a rightward bias, t(7) =2.340, p=.052, d =1.769. The main effect of ear revealed mean biases were more leftward for left ear (M =−18.78, SD =28.04) compared to right ear (M =−8.04, SD =25.64) distractors. One-sample t-tests indicated significant pseudoneglect occurred for left ear distractors, t(32) =3.847, p=.001, d =1.360, whereas the leftward bias for right ear distractors was not significant, t(32) =1.803, p=.081, d =.637, illustrating that pseudoneglect was accentuated by left ear distractors, and reduced by right ear distractors. The main effect of distractor frequency showed leftward biases were stronger for frequent (M =−15.58, SD =26.17) than for infrequent (M =−11.24, SD =27.55) distractors, with pseudoneglect being significant in both instances [frequent: t(32) =3.420, p=.002, d =1.209; infrequent: t(32) =2.343, p=.026, d =.828]. The latter two main effects were qualified by an interaction of ear and distractor frequency, F(1,31) =5.034, p=.032, η2 =.140. Pairedsamples t-tests were used for post hoc comparisons (Bonferroni corrected p value of .013). Only one comparison reached significance (see Fig. 2). Infrequent right ear distractors (M =−3.54, SD =32.28), as compared to infrequent left ear distractors (M =−18.94, SD =28.51), significantly decreased leftward biases, t(32) =3.410, p=.002, d =.599. Distractors to the right ear decreased the strength of pseudoneglect, with this effect being stronger when distractors were infrequent, and therefore more salient. Remaining comparisons were non-significant (frequent left and frequent right: t(32) =1.598, p=.120, d =.287; frequent right and infrequent right: t(32) =1.910, p=.065, d =.341; frequent left and infrequent left, t(32) =.092, p=.928, d =.015.

3. Results 3.1. Accuracy Accuracy data were analysed by auditory distractor (silent, left ear, right ear) and deviation (.5 mm, 1 mm, 2 mm) using a 3×3 repeatedmeasures ANOVA as a manipulation check. The interaction of auditory distractor and deviation was non-significant, F(4,140) =.734, p=.570, η2 =.021. The main effect of auditory distractor, F(2,70) =2.165, p=.122, η2 =.058 was also non-significant. Importantly, the main effect of deviation was significant, F(2,70) =107.492, p < .001, η2 =.754. Pairwise comparisons (p's < .001 for all comparisons) showed participants were more accurate for 2 mm bisections (M =79.74, SD =11.61) than for 1 mm bisections (M =66.94, SD =7.57). Furthermore, accuracy was higher for 1 mm bisections than .5 mm bisections (M =61.66, SD =8.12). Performance was more accurate when bisections were further from centre and the task was easier, verifying participants performed as expected. 3.2. Response asymmetry Landmark task responses were scored as leftward when the left side was chosen as longer and rightward when the right side was chosen as longer. Response asymmetry scores were calculated by subtracting the number of leftward responses from the number of rightward responses, dividing by the total number of trials, and then multiplying by 100. As such, asymmetry scores could range from −100 (always chose left) to +100 (always responded right), with a score of zero indicating no directional asymmetry. A number of studies have indicated that a substantial proportion of individuals (between 5% and 50%) present with rightward attentional biases at baseline, instead of the typical leftward bias (Benwell et al., 2013; Braun and Kirk, 1999; Cowie and Hamil, 1998; Dellatolas et al., 1996; Halligan et al., 1990; Halligan and Marshall, 1993; Jewell and McCourt, 2000; Manning et al., 1990; McCourt, 2001; Szczepanski and Kastner, 2013; Thomas et al., 2016). This often-neglected individual difference points to a potentially important source of variability in pseudoneglect (see also Chechlacz et al., 2015a; Chechlacz et al., 2015b; Szczepanski and Kastner, 2013; Thiebaut de Schotten et al., 2011, who discuss individual differences), with recent research suggesting that the direction of asymmetries at baseline influences how attention is distributed across the visual field during distraction (Thomas et al., 2016). As the importance of individual differences in the direction of attentional asymmetries at baseline cannot be underplayed, we accounted for these differences. Baseline asymmetry scores were used to separate participants into left- (n =25) and rightresponder (n =8) groups (see Thomas et al., 2016). As only 3 participants presented with no bias, there were too few in this group to be considered in the omnibus ANOVA and they were removed from analyses. To establish whether directional biases were significant for each group at baseline, one-sample t-tests compared baseline response asymmetries to zero. Left-responders showed a significant leftward bias (M =−25.41, SD =15.684), t(24) =8.022, p < .001, d =3.275, and right-responders showed a significant rightward bias (M =18.98, SD =13.64), t(7) =3.937, p=.006, d =2.976, indicating that both groups presented with significant asymmetries at baseline. A 2 (ear: left, right) × 2 (distractor frequency: frequent, infrequent)

3.3. Response time (RT) RTs were subjected to a 2 (ear: left, right) × 2 (distractor frequency: frequent, infrequent) × 2 (baseline direction: left-responder, rightresponder) mixed-model ANOVA as it was believed that arousal effects might be more visible for response times. All main effects and lower order interactions failed to reach significance (p's > .098); however, the three-way interaction was significant, F(1,31) =6.299, p=.018, η2 =.169. Initial examination of the means indicated that it was, in fact, the trial block (i.e., primarily left ear or primarily right ear distractors) that differed between left- and right-responders (see Fig. 3). Amongst left-responders (i.e., the typical response), RTs were significantly faster when 78% of distractors were presented to the right ear, t(24) =2.385, p=.025, d =.479, compared to when left ear distractors were frequent. In contrast, RTs were faster (non-significant) for right-responders when 78% of distractors were presented to the left ear, t(7) =1.178, p=.277, d =.835, compared to when right ear distractors were frequent. 4. Discussion In order to assess individual differences in the direction of response asymmetries at baseline, we split participants into left- and rightresponder groups. Stability in the direction of asymmetries over time can be seen across both groups by examining the means (leftresponders: baseline M =−26.235, SD =15.616, distractor M =−24.591, SD =17.700; right-responders: baseline M =18.981, SD 43

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Left Ear

30 20 10 0 -10 -20 -30 -40 Frequent

Infrequent

Frequent

Left-Responder b) Mean Change in Response Asymmetry

2001; Szczepanski and Kastner, 2013; Thiebaut de Schotten et al., 2011; Thomas et al., 2016). We observed a congruency between the spatial location of the auditory distractor and the direction of attention, which points to an attentional orienting effect. Although tones were presented in conjunction with lines, sounds still could have signalled participants to respond toward a particular side. It is possible that upon hearing the tones, exogenous attention was directed to the audiospatial location of the distractor and participants then responded that this side of the line was perceived as being longer (i.e., leftward biases for left ear distractors and reduced leftward biased for right ear distractors). The influence of distractor frequency argues against this effect – if participants were simply more likely to press the key on the side of the tone, distractor frequency would not have interacted with ear to influence asymmetries. This finding could also be the result of an asymmetry in hemispheric activation. Left ear distractors increase right hemisphere activation, which directs attention to the left side, whereas right ear distractors increase left hemisphere activation and direct attention to the right. The pattern of the RT data supports the intriguing possibility of differences in hemispheric activation amongst left- and rightresponders. Responses were faster when auditory distractors were presented to the same side as the more activated hemisphere (i.e., right ear and right hemisphere). As the typical leftward bias results from predominant right hemisphere activation, the current data suggest that when the majority of auditory distractors are presented to the right ear, RTs are faster amongst these left-responders. Mean RTs suggest the opposite occurs amongst right-responders, pointing to the possibility of preferential left hemisphere activation during the landmark task, such that left ear auditory signals speed up reaction times. These data provide an interesting and novel suggestion for why baseline asymmetries might be biased toward the right side amongst a subset of individuals; possibly these participants are engaging a strategy that increases left hemisphere activation, and draws attention toward the right side. This finding is consistent with the correlation between larger SLF II volumes in the left hemisphere and a rightward response bias observed by Thiebaut de Schotten et al. (2011). Importantly, there were no accuracy differences between the left and right ear blocks of trials, confirming that a speed-accuracy trade-off does not account for RT differences. Further, response asymmetries did not differ between left- and right-responders, which suggest speeded responses did not correspond with facilitated attentional orienting. Instead, these data point to an increase in arousal, as a result of increasing activation, when distractors are presented to the hemisphere that is more engaged in the task. The observed effect of distractor frequency is inconsistent with the hypothesis that the saliency of the infrequent distractors would increase attentional asymmetries by increasing activation within the right lateralised ventral attention network (Corbetta and Shulman, 2011). Instead, attentional asymmetries were decreased as arousal increased. It is possible that attention is drawn back toward the centre during high arousal, if indeed the right hemisphere becomes overloaded. In this case, an opportunity for dysregulation within the bilateral dorsal attention network could occur, such that left hemisphere activation also increases and a attention is oriented back toward centre. Following from the suggestion that arousal might unexpectedly decrease leftward biases, the interaction of ear and distractor frequency suggests additive arousal and attentional orienting effects. Right ear distractors oriented attention to the right side, but only significantly decreased leftward biases when they were infrequent and therefore arousing. One-sample t-tests were used to confirm this suggestion (see Table 1). Significant leftward biases were observed for most conditions with the exception being infrequent right ear distractors, where leftward biases were no longer significant. It is possible that the attentional orienting effect is stronger than the arousal effect, which

Right Ear

Frequent

Infrequent

Right-Responder

Infrequent

0 -5 -10 -15 -20 -25 Left Ear

Right Ear

Fig. 2. a) Mean response asymmetry scores, based on direction of asymmetries at baseline, for auditory distractor trials. Trials are separated by ear (left, right) and distractor frequency (frequent, infrequent). Negative scores indicate leftward asymmetries, whereas positive scores indicate rightward asymmetries. Error bars represent standard error of the mean. b) Interaction of ear and distractor frequency. The contrast between infrequent left ear and infrequent right ear distractors shows a significant reduction in pseudoneglect. Error bars represent within-participants standard error of the mean.

400

Right Ear Block

Left Ear Block

Mean Response Time (ms)

350 300 250 200 150 100 50 0 Left-Responders

Right-Responders

Fig. 3. Mean response times, based on direction of asymmetries at baseline, and auditory distractor block (i.e., primarily left ear or primarily right ear). Error bars represent standard error of the mean.

=13.638, distractor M =16.554, SD =20.006). The lack of a significant bias amongst right-responders in the second block of trials is likely due to a slight decrease in asymmetry scores (decrease in M =2.427), an increase in variance during the distractor trials (increase in SD =6.368) and the small sample size of this group (n =8). This finding provides additional support for the idea that response asymmetries are stable over time (McCourt, 2001) and further, that a subset of participants reliably show rightward biases (Benwell et al., 2013; Braun and Kirk, 1999; Chechlacz et al., 2015a, 2015b; Cowie and Hamil, 1998; Dellatolas et al., 1996; Halligan et al., 1990; Halligan and Marshall, 1993; Jewell and McCourt, 2000; Manning et al., 1990; McCourt,

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prohibited the occurrence of this effect on the left side, where attention is dominant. This suggestion is intriguing, as it indicates why prior research has shown both attentional orienting and arousal effects on attentional asymmetries; methodology could dictate which effect is stronger and ultimately emerges as significant. Given that infrequent tones to the right ear rendered leftward biases non-significant, infrequent distractors, which are more salient as a result of their unexpected nature (Zink et al., 2003), arousal surprisingly appears to decrease attentional asymmetries. Consistent with this suggestion, RT data suggest that participants responded faster when distractors were presented to the more engaged hemisphere. However, auditory distractors were spatial in nature and evidence in favour of an attentional orienting effect was also observed. In order to isolate the role of arousal more directly, a second experiment, wherein auditory distractors were non-spatial, was conducted.

Table 2 Statistics for one-sample t-tests comparing response asymmetry scores for each distractor condition, based on distractor frequency. Distractor condition

Distractor Frequency

Statistic

Baseline Left Ear

No distractors present Frequent Infrequent

t(34) = 3.348, p = .002, d = 1.148 t(34) = 3.571, p = .001, d = 1.225 t(34) = 3.134, p = .004, d = 1.075

Right Ear

Frequent Infrequent

t(34) = 2.336, p = .026, d = .801 t(34) = .661, p = .513, d = .227

distractors during the landmark task. As our findings from Experiment 1 were unexpected, we also wanted to determine whether we could replicate this effect. As such, we expected auditory distractors would reduce attentional asymmetries, mimicking the effect we observed in Experiment 1 (Table 2). The inclusion of handedness allowed us to explore attentional asymmetries amongst left-handers, as well as whether this subgroup is more likely to show rightward biases. Given the novelty of this manipulation, we did not make directional hypotheses in relation to distractor effects and handedness.

5. Experiment 2 The mounting evidence in favour of consistent individual differences in the direction of attentional asymmetries at baseline remains perplexing. Although there has been some suggestion that these differences relate to dopaminergic asymmetries within the brain (Greene et al., 2010; Newman et al., 2012; Tomer et al., 2013; Zozulinsky et al., 2014), the RT data from Experiment 1 suggest that right-responders might engage in more left hemisphere processing, which draws attention toward the right side. To investigate this possibility, we examined left-handed, as well as right-handed, participants in Experiment 2. Left-handed participants are more likely to present with left hemisphere visuospatial processing (BadzakovaTrajkov et al., 2010; Vingerhoets et al., 2013), and therefore, this subgroup might also be more likely to show rightward biases. Previous research examining visuospatial attention amongst lefthanded participants is inconsistent and methodologically limited, with most studies failing to operationalize handedness with a comprehensive questionnaire (Jewell and McCourt, 2000). A meta-analysis by Voyer, Voyer, and Tramonte (2012) showed larger attentional asymmetries amongst right-handers; however, they reported very few studies that addressed the effects of handedness on line bisection directly. In relation to manual bisection, when left-handers bisect with their left hand they make a leftward bisection error, but a rightward bisection error occurs when using the right hand (Bradshaw et al., 1987; Luh, 1995). This finding is not particularly telling as it likely indicates a motor asymmetry, rather than an attentional one. Dufour et al. (2007a) found a rightward shift in perceived sound location that was stronger amongst left-handers, suggesting that inter-aural signal processing might differ based on handedness. Although some researchers argue left-handers show smaller biases as a result of more bilateral hemispheric function (Brodie and Dunn, 2005), differences in cortical activation for language and emotion based on handedness appear to be more prominent than visuospatial differences (Badzakova-Trajkov et al., 2010; Powell et al., 2012; Zago et al., 2017). Although Badzakova-Trajkov et al. (2010) examined differences in brain activation during visuospatial processing, they did not examine attentional asymmetries on the landmark task based on handedness. More recently, Zago et al. (2017) failed to find any handedness based differences on a computerised line bisection task; however, they employed a 3-response paradigm, asking participants whether the line was bisected in the centre, or to the left or right, which differs from the typical forced-choice task. Therefore, our inclusion lefthanders will provide important evidence as to whether, and in what capacity, handedness influences attentional asymmetries on a standard landmark task. As highlighted above, attentional orienting and arousal mechanisms both influence distractor effects on attentional asymmetries. To determine whether arousal effects occur in the absence of possible attentional orienting events, we employed centrally presented auditory

6. Method 6.1. Participants Forty-eight undergraduate Flinders University students (12 males, Mage =24.52, SD =8.49) completed the experiment in exchange for $10.00AUD. All participants had normal hearing, and normal or corrected-to-normal vision. Half of the participants were right-handed, as measured by the FLANDERS handedness survey (M =9.79, SD =.59; Nicholls et al., 2013), and half were left-handed (M =−9.04, SD =1.46). The Flinders University Social and Behavioural Research Ethics Committee granted ethical approval. 6.2. Apparatus and stimuli The apparatus was as in Experiment 1, with two exceptions. Responses were recorded on a standard keyboard and auditory stimuli were presented via two speakers that were positioned directly underneath the participant's chair. The speakers were affixed in the exact middle of the underside of the chair, to remove all audiospatial location cues. The visual and auditory stimuli were both identical to those used in Experiment 1. 6.3. Design A 3 (auditory distractor: baseline, distractor absent, distractor present) × 2 (polarity: black, white) × 6 (deviation: −2, −1, −0.5, .5, 1, 2 mm) × 3 (line shift: left, centre, right) within-participants factorial design was used. Two blocks of trials were completed, with the baseline block being performed first, to determine the direction of asymmetry (left-responder, right-responder). The basic factorial combination (excluding auditory distractor) of 36 was repeated 3 times in the baseline block (n =108 trials). In the auditory distractor block, distractors were heard on 25% of trials (distractor present: n =108), with the remaining 75% of trials being silent (distractor absent: n =324). Trials were randomly presented in each block, and the total number of trials across both blocks was 540. 6.4. Procedure After obtaining informed consent, participants completed the 45

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this group for analysis. One-sample t-tests demonstrated that leftresponders showed significant leftward biases (M =−24.02, SD =16.46), t(36) =8.880, p < .001, d =2.960, and right-responders showed significant rightward biases (M =18.72, SD =12.71), t(8) =4.419, p=.002, d =3.125, at baseline, indicating asymmetries were different from zero in both groups. A 2 (distractor: absent, present) × 2 (baseline direction: leftresponder, right-responder) × 2 (handedness: left, right) repeatedmeasures ANOVA was used to examine whether auditory distractors influenced response asymmetries. As none of the effects relating to handedness reached significance (all p's > .260), the analysis was repeated without this factor. The main effect of distractor was nonsignificant, F(1,42) =1.830, p=.183, η2 =.042, showing that response asymmetries did not differ between the silent and auditory distractor trials when left- and right-responders were considered together. The main effect of baseline direction was significant, F(1,42) =6.532, p=.014, η2 =.135, indicating that left-responders differed from right-responders during the distractor block of trials. Mean biases among left-responders remained significantly leftward for the second block of trials, t(36) =5.696, p < .001, d =1.899, whereas biases among right-responders were non-significantly rightward, t(8) =.525, p=.614, d =.371. This finding shows that the direction of attentional asymmetries was consistent over time. Critically, there was an interaction between distractor and baseline direction, F(1,42) =10.985, p=.002, η2 =.207 (see Fig. 4). Pairedsamples t-tests illustrated that leftward biases were significantly decreased by when distractors were presented compared to when they were absent amongst left-responders, t(36) =2.559, p=.015, d =.423. Similarly, amongst right-responders, auditory distractors led rightward biases to be decreased compared when distractors were absent, as evidenced by a trend, t(8) =2.037, p=.076, d =.887.

FLANDERS handedness survey (Nicholls et al., 2013). Participants then completed the baseline and auditory distractor blocks of trials. The presentation sequence was identical to Experiment 1 (see Fig. 1). The response paradigm was as in Experiment 1; however, participants used their right index finger on the “l” key to indicate the right side of the line was longer and their left index finger on the “a” key to indicate the left side was longer. Landmark task responses were scored as in Experiment 1. 7. Results 7.1. Accuracy Accuracy data were analysed by distractor condition (baseline, distractor absent, distractor present) and deviation (.5 mm, 1 mm, 2 mm) using a 3×3 repeated-measures ANOVA. As expected, the main effect of deviation was significant, F(2,94) =178.314, p < .001, η2 =.791. Pairwise comparisons (p's < .001 for all comparisons) showed participants were more accurate for 2 mm bisections (M =81.19, SD =9.47) than for 1 mm bisections (M =69.13, SD =7.10). Furthermore, accuracy was higher for 1 mm bisections than .5 mm bisections (M =61.58, SD =8.77). Performance was more accurate when bisections were further from centre and the task was easier, verifying participants performed as expected. There was also a main effect of distractor condition, F(2,94) =11.725, p < .001, η2 =.200. Pairwise comparisons indicated a significant decrease in accuracy for both distractor absent (M =69.35, SD =7.71) and distractor present trials (M =69.51, SD =8.08) compared to the baseline block (M =73.05, SD =8.68), p's < .001. Accuracy did not differ between the distractor absent and distractor present trials, p=.789. The interaction between auditory distractor and deviation was also significant, F(4,188) =4.940, p=.001, η2 =.095. Pairedsamples t-tests were used to explore this interaction. The same pattern wherein 1 mm bisections were more accurate than .5 mm bisections, and 2 mm bisections were more accurate than 1 mm bisections was observed for all 3 distractor conditions (see Table 3 for statistics, means, and standard deviations).

7.3. Response time As in Experiment 1, we conducted a 2 (distractor condition: silent, auditory distractor) × 2 (baseline direction: left-responder, rightresponder) × 2 (handedness: left, right) mixed-model ANOVA to explore whether arousal influenced RTs. As none of the effects in relation to baseline direction and handedness reached significance, these factors were removed. RTs differed significantly based on distractor condition, F(1,45) =12.576, p=.001, η2 =.218, with responses being significantly faster for when distractors were absent than when they were present (see Fig. 5).

7.2. Response asymmetry Baseline response asymmetry scores were used to separate participants into left- (n =37) and right-responder (n =9) groups. The proportion of right-responders (19%) in our sample was well within the range of previous reports (between 5% and 50%; Benwell et al., 2013; Braun and Kirk, 1999; Cowie and Hamil, 1998; Dellatolas et al., 1996; Halligan et al., 1990; Halligan and Marshall, 1993; Jewell and McCourt, 2000; Manning et al., 1990; McCourt, 2001; Szczepanski and Kastner, 2013; Thomas et al., 2016). Intriguingly, the inclusion of lefthanders did not increase the number of right-responders. As only 2 participants presented with no bias at baseline, there were too few in

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Table 3 Statistics for paired-sample t-tests comparing accuracy for each distractor condition, based on deviation from the true midpoint. Distractor condition

Contrast

Statistic

Baseline

.5 mm and 1 mm .5 mm and 2 mm 1 mm and 2 mm

t(47) = 6.432, p < .001, d = .930 t(47) = 15.496, p < .001, d = 2.240 t(47) = 10.378, p < .001, d = 1.498

Silent

.5 mm and 1 mm .5 mm and 2 mm 1 mm and 2 mm

t(47) = 4.366, p < .001, d = .631 t(47) = 13.455, p < .001, d = 1.965 t(47) = 14.756, p < .001, d = 2.253

.5 mm and 1 mm .5 mm and 2 mm 1 mm and 2 mm

t(47) = 3.846, p < .001, d = .563 t(47) = 8.733, p < .001, d = 1.266 t(47) = 6.174, p < .001, d = .947

Auditory Distractor

Silent Auditory Distractor

5 0 -5 -10 -15 -20 -25 Left-Responders

Right-Responders

Fig. 4. Mean response asymmetry, based on direction of asymmetries at baseline, for silent and auditory distractor trials. Note that baseline scores are not presented on this figure. Negative scores indicate leftward biases, whereas positive scores indicate rightward biases. Error bars represent standard error of the mean.

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Mean Reaction Time (ms)

600

Distractor Absent Distractor Present

450

sented, which generates a startle effect and slows RTs. Importantly, by employing centralised auditory distractors, the hemispheric activation differences that we observed in Experiment 1 between left- and rightresponders were not expected to occur here. We conclude that auditory distractors cause both attentional orienting and arousal effects, with arousal effects emerging more strongly when attentional orienting is eliminated.

400

9. General discussion

350

9.1. Handedness

550 500

300 Left-Responder

Handedness failed to elicit any differences in response asymmetries, suggesting that left- and right-handers do not present with different visuospatial biases on the landmark task. This finding is consistent with recent data reported by Zago et al. (2016) using a different visuospatial task. Although various measures of visuospatial processing fail to show a correlation (Learmonth et al., 2015), there appears to be growing evidence that left-handers show similar attentional asymmetries to right-handers on visuospatial tasks. Furthermore, these behavioural data are consistent with neuroimaging data showing that the majority of both left- and right-handers exhibit right hemisphere activation during visuospatial processing (Badzakova-Trajkov et al., 2010; Powell et al., 2012; Zago et al., 2017).

Right-Responder

Fig. 5. Mean response times, based on auditory distractor condition and direction of asymmetries at baseline. Error bars represent standard error of the mean.

8. Discussion None of the effects in relation to handedness were significant, illustrating that left- and right-handers did not differ in the strength of their response asymmetry scores. This finding is both intriguing and informative as it suggests that left- and right-handers do not show directionally different attentional asymmetries on the landmark task. Many prior investigations that have indicated an influence of handedness on attentional asymmetries have used either manual or computerised line bisection tasks (see Jewell and McCourt, 2000). Manual tasks are subject to motor biases, which makes it difficult to determine what might be a true attentional difference, as compared to a consequence of the response paradigm. As visuospatial tasks show poor correlational relationships (Learmonth et al., 2015), and it appears that the asymmetries observed on these tasks do not rely on a single underlying mechanism, handedness might differentially influence computerised line bisection and the landmark task. The current results provide no evidence to support any handedness-based differences on the landmark task. Future research, which targets lefthanders and makes use of various visuospatial measures, will be needed to determine whether there are, in fact, handedness-based differences in the direction of asymmetries at baseline on other measures. As in Experiment 1, the general direction of attentional asymmetries (i.e., right versus left) remained stable across blocks, suggesting right-responders represent a reliable subgroup. Centrally presented auditory distractors decreased attentional asymmetries, providing evidence in favour of a general arousal effect that was interestingly mediated by baseline direction of asymmetry. Salient non-spatial auditory distractors decreased attentional asymmetries across both left- and right-responder groups by drawing attention toward the centre. Importantly, this difference cannot be explained by an increase in accuracy, as accuracy did not differ between the distractor absent and distractor present trials. Thiebaut de Schotten et al. (2011) have provided initial evidence that left- and right-responders show greater activation in opposing hemispheres during line bisection tasks. The current behavioural data fit well with these neuroimaging findings, showing that direction of asymmetries at baseline plays an important role in how distractors influence pseudoneglect. Arousal causes an overload of the dominant ventral attention network, which allows disinhibition of the bilateral dorsal network and drives attention in the opposing direction. RT data are consistent with prior research showing that reaction times are slower in the presence of infrequent or novel sounds (Corral and Escera, 2008). The auditory distractors in the current experiment only appeared on 25% of trials. Interestingly, there were no differences in RTs based on baseline direction of asymmetry. This result suggests a generalised increase in arousal when an auditory distractor is pre-

9.2. Responder groups Participants in both experiments were separated into left- and right-responder groups. Left-responders showed significant leftward biases across all blocks of trials in both experiments. Right-responders showed significant rightward biases at baseline, which did not reach significance in subsequent blocks. This result is believed to be the result of a slight decrease in mean asymmetries, combined with an increase in variance and the small number of right-responders. Importantly the direction of mean asymmetry remained consistent with that observed at baseline, even though biases did not reach significance. As the number of right-responders was small, it is important to interpret these effects with caution. The RT data suggest the interesting possibility that right-responders might show greater left hemisphere activation during the landmark task, which is consistent with recent neuroimaging data (Thiebaut de Schotten et al., 2011) and provides an avenue for future research. 9.3. Attentional orienting effects Overall, left ear distractors accentuated attentional asymmetries, whereas right ear distractors decreased pseudoneglect. Auditory distractors activated an attentional orienting mechanism, leading attention to be directed toward the audiospatial location of the distractor. We suggest this effect results from a hemispheric asymmetry, wherein left ear distractors increase right hemisphere activation and therefore direct attention toward the left. In contrast, right ear distractors lead to increased activation in the left hemisphere and subsequently direct attention rightward. Auditory and visual stimuli were presented simultaneously, for only 250 ms, which argues against an endogenous cueing effect; however, the cross-modal integration of these stimuli could have directed visual attention to the audiospatial location of the cue and led participants to respond that this side of the line was longer. Such an effect would not reflect a true asymmetry, but would simply be a bias to press the key on the side of the distractor (Thomas et al., in press). As infrequent and centrally presented distractors reduced asymmetries to a greater extent, such a key press bias appears to be rather unlikely. Instead, our findings suggest a genuine attentional orienting effect, with hemispheric activation driving attention toward the contralateral side. 47

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tones to the more activated hemisphere. When attentional orienting mechanisms were eliminated, a strong arousal effect was observed. Interestingly, this effect was modulated by the baseline direction of asymmetry, with both responder groups showing a decrease in asymmetry. RT data once again confirmed the occurrence of an arousal effect, wherein unpredictable and infrequent auditory distractors generated a startle arousal response and slowed RTs. The current findings illustrate that auditory distractors engage cross-modal processing to influence visuospatial asymmetries via both attentional orienting and arousal effects, with the dominant mechanism most likely being attentional orienting.

9.4. Arousal effects We hypothesised that infrequent, and therefore more salient, distractors would increase both arousal and attentional asymmetries. We failed to observe any such effect; instead, the data suggest that increases in arousal decreased asymmetries. We suggest that by increasing arousal, the right lateralised ventral attention network became overloaded, allowing for the bilateral dorsal attention network to also become activated and drive attention back toward the centre. Leftward biases were stronger for frequent than infrequent distractors. Furthermore, infrequent right ear distractors decreased the strength of pseudoneglect to the extent that asymmetries were non-significant. We believe this illustrates an additive effect of attentional orienting and arousal, such that right ear distractors directed attention to the right side, but distractors only significantly decreased leftward biases when they were infrequent and therefore arousing. In fact, this distractor condition was the only one wherein leftward biases were non-significant. In Experiment 2, spatial information was removed from distractors by presenting auditory stimuli from underneath the participant's chair. We found that asymmetries were decreased in the presence of auditory distractors, suggesting that the infrequent, irrelevant sounds increased arousal and allowed the dorsal attention network within the left hemisphere to become engaged (Corbetta and Shulman, 2011). Reduced asymmetries were not attributable to increased accuracy; in fact, accuracy decreased during the distractor block of trials.

Acknowledgements An Australian Research Council (ARC) Discovery Early Career Research Award (DECRA) to NAT (DE150101108) supported this research. There are no relationships, financial or otherwise, that could be interpreted as a conflict of interest. References Adair, J.C., Barrett, A.M., 2008. Spatial neglect: Clinical and neuroscience review. Ann. New Y. Acad. Sci. 1142, 21–43. http://dx.doi.org/10.1196/annals.1444.008. Arent, S.M., Landers, D.M., 2003. Arousal, anxiety, and performance: a re-examination of the inverted-u hypothesis. Res. Q. Exerc. Sport 74, 436–444. http://dx.doi.org/ 10.1080/02701367.2003.10609113. Badzakova-Trajkov, G., Häberling, I.S., Roberts, R.P., Corballis, M.C., 2010. Cerebral asymmetries: complementary and independent processes. PLoS One 5, 1–9. http:// dx.doi.org/10.1371/journal.pone.0009682. Behrmann, M., Geng, J.J., Shomstein, S., 2004. Parietal cortex and attention. Curr. Opin. Neurobiol. 14, 212–217. http://dx.doi.org/10.1016/j.conb.2004.03.012. Beis, J.M., Keller, C., Morin, N., Bartolomeo, P., Bernati, T., Chokron, S., Azouvi, P., 2004. Right spatial neglect after left hemisphere stroke: qualitative and quantitative study. Neurology 63, 1600–1605. http://dx.doi.org/10.1212/ 01.WNL.0000142967.60579.32. Bellgrove, M.A., Dockree, P.M., Aimola, L., Robertson, I.H., 2004. Attenuation of spatial attentional asymmetries with poor sustained attention. Neuroreport 15, 1065–1069. http://dx.doi.org/10.1097/00001756-200404290-00027. Benwell, C.S.Y., Thut, G., Learmonth, G., Harvey, M., 2013. Spatial attention: differential shifts in pseudoneglect direction with time-on-task and initial bias support the idea of observer subtypes. Neuropsychologia 51, 2747–2756. http://dx.doi.org/10.1016/ j.neuropsychologia.2013.09.030. Bjoertomt, O., Cowey, A., Walsh, V., 2002. Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation. Brain 125, 2012–2022. http://dx.doi.org/10.1093/brain/awf211. Blackford, J.U., Buckholtz, J.W., Avery, S.N., Zald, D.H., 2010. A unique role for the human amygdala in novelty detection. Neuroimage 50, 1188–1193. http:// dx.doi.org/10.1016/j.neuroimage.2009.12.083. Bowers, D., Heilman, K.M., 1980. Pseudoneglect: effects of hemispace on a tactile line bisection task. Neuropsychologia 18, 491–498. http://dx.doi.org/10.1016/00283932(80)90151-7. Bradshaw, J.L., Nettleton, N.C., Wilson, L.E., Bradshaw, C.S., 1987. Line bisection by left-handed preschoolers: a phenomenon of symmetrical neglect. Brain Cogn. 6, 377–385. http://dx.doi.org/10.1016/0278-2626(87)90134-5. Braun, J.G., Kirk, A., 1999. Line bisection performance of normal adults. Neurology 53, 527–532. http://dx.doi.org/10.1212/WNL.53.3.527. Brodie, E.E., Dunn, E.M., 2005. Visual line bisection in sinistrals and dextrals as a function of hemispace, hand, and scan direction. Brain Cogn. 58, 149–156. http:// dx.doi.org/10.1016/j.bandc.2004.09.019. Bultitude, J.H., Aimola Davies, A.M., 2006. Putting attention on the line: investigating the activation-orientation hypothesis of pseudoneglect. Neuropsychologia 44, 1849–1858. http://dx.doi.org/10.1016/j.neuropsychologia.2206.03.001. Calvert, G.A., 2001. Crossmodal processing in the human brain: Insights from functional neuroimaging studies. Cereb. Cortex 11, 1110–1123. http://dx.doi.org/10.1093/ cercor/11.12.1110. Chechlacz, M., Gillebert, C.R., Vangkilde, S.A., Petersen, A., Humphreys, G.W., 2015a. Structural variability within frontoparietal networks and individual differences in attentional functions: an approach using the theory of visual attention. J. Neurosci. 35, 10647–10658. http://dx.doi.org/10.1523/JNEUROSCI.0210-15.2015. Chechlacz, M., Humphreys, G.W., Sotiropoulos, S.N., Kennard, C., Cazzoli, D., 2015b. Structural organisation of the corpus callosum predicts attentional shifts after continuous theta burst stimulation. J. Neurosci. 35, 15353–15368. http:// dx.doi.org/10.1523/JNEUROSCI.2610-15.2015. Chica, A.B., Thiebaut de Schotten, M., Toba, M., Malhotra, P., Lupiáñez, J., Bartolomeo, P., 2011. Attention networks and their interactions after right-hemisphere damage. Cortex 48, 654–663. http://dx.doi.org/10.1016/j.cortex.2011.01.009. Chieffi, S., Iachini, T., Iavarone, A., Messina, G., Viggiano, A., Monda, M., 2014. Flanker interference effects in a line bisection task. Exp. Brain Res. 232, 1327–1334. http:// dx.doi.org/10.1007/s00221-014-3851-y.

9.5. Reaction time Interestingly, RT data suggest distractors led to a difference in hemispheric activation, based on baseline direction of asymmetry. Right hemisphere activation is believed to underlie the typical leftward bias (Corbetta and Shulman, 2011; Kinsbourne, 1970), meaning that this hemisphere is more activated amongst left-responders. When the majority of auditory distractors were heard in the right ear, RTs were faster for this responder group. In contrast, right-responders showed the opposite effect, such that, when the majority of auditory distractors were presented to the left ear, RTs were faster. Response asymmetry data pointed to the occurrence of a dominant attentional orienting effect, in conjunction with a weaker arousal effect; the RT data provide additional support for arousal effects. In Experiment 2, RTs were slowed in the presence of auditory distractors, compared when distractors were absent, which is consistent with prior work showing RTs are slowed by infrequent auditory stimuli (Corral and Escera, 2008). Given that auditory distractors were unpredictable, the generation of a startle arousal response would have slowed RTs. 10. Conclusion Prior research has provided evidence in favour of both attentional orienting and arousal effects on attentional asymmetries (Chieffi et al., 2014; Dodds et al., 2008, 2009; Dufour et al., 2007b; Harvey et al., 1995; Manly et al., 2005; Max et al., 2015; McCourt et al., 2005; McCourt and Jewell, 1999; McCourt and Olafson, 1997; Milner et al., 1992; Nichelli et al., 1989; Nicholls et al., 2005; Peers et al., 2006; Pérez et al., 2009; Pizzamiglio et al., 1990; Reuter-Lorenz et al., 1990; Sosa et al., 2011) and we suggest that methodological choices likely determine which effect is more dominant. In the current study, the attentional orienting effect was more dominant; however, evidence an additive effect of attentional orienting and arousal occurred. Given that infrequent right ear tones rendered leftward biases non-significant, the saliency of infrequent distractors makes them more unexpected and leads them to be more arousing. RT data indicated arousal-based differences, which suggested that left-responders and right-responders show differential hemispheric activation that is increased by frequent 48

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