Neuropsychol Rev DOI 10.1007/s11065-013-9245-2

REVIEW

Representational Pseudoneglect: A Review Joanna L. Brooks & Sergio Della Sala & Stephen Darling

Received: 12 September 2013 / Accepted: 23 December 2013 # Springer Science+Business Media New York 2014

Abstract Pseudoneglect, the tendency to be biased towards the left-hand side of space, is a robust and consistent behavioural observation best demonstrated on the task of visuospatial line bisection, where participants are asked to centrally bisect visually presented horizontal lines at the perceived centre. A number of studies have revealed that a representational form of pseudoneglect exists, occurring when participants are asked to either mentally represent a stimulus or explore a stimulus using touch in the complete absence of direct visuospatial processing. Despite the growing number of studies that have demonstrated representational pseudoneglect there exists no current and comprehensive review of these findings and no discussion of a theoretical framework into which these findings may fall. An important gap in the current representational pseudoneglect literature is a discussion of the developmental trajectory of the bias. The focus of the current review is to outline studies that have observed representational pseudoneglect in healthy

J. L. Brooks (*) School of Psychology, University of Adelaide, Hughes Building, North Terrace, Adelaide, South Australia, Australia e-mail: [email protected] S. Della Sala Human Cognitive Neuroscience, Psychology, University of Edinburgh, Edinburgh, UK S. Della Sala Centre for Cognitive Ageing and Cognitive Epidemiology, Psychology, University of Edinburgh, Edinburgh, UK J. L. Brooks Experimental Psychology, Universita’ Suor Orsola Benincasa, Naples, Italy S. Darling Psychology and Sociology, School of Arts and Social Sciences, Queen Margaret University, Musselburgh, UK

participants, consider a theoretical framework for these observations, and address the impact of lifespan factors such as cognitive ageing on the phenomenon. Keywords Pseudoneglect . Attention . Spatial awareness . Representational . Cognitive ageing

Introduction When healthy participants are asked to bisect a visually presented horizontal line they show a tendency to bisect the line towards the left-hand side of true centre. This spatial bias to the left hand side in line bisection has been referred to as ‘pseudoneglect’ (Bowers and Heilman 1980) by analogy to the performance of right-hemisphere impaired patients with left unilateral spatial neglect who show spatial biases towards the right hand-side of space (Robertson and Marshall 1993; Nijboer et al. 2013). The term now refers to the general tendency of healthy people to preferentially attend to the left side of space (Hatin et al. 2012). Pseudoneglect is not as severe as neglect but it is nevertheless a robust and consistent behavioural phenomenon in healthy participants with measurable behavioural consequences (Turnbull and McGeorge 1998). It has also been demonstrated in non-human animals (Regolin 2006). The most recent review and meta-analysis of pseudoneglect, and certainly the most well known, was conducted by Jewell and McCourt (2000). The review included the results from 2191 healthy participants across a range of studies—the majority of studies being visuospatial in nature. Leftward biases in healthy adults were found to be very robust. The authors noted that forced choice bisection methods produced larger effect sizes than manual method of adjustment procedures; that visuospatial line bisection and tactile rod bisection typically elicit leftward biases while

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kinaesthetic matching tasks often produce rightward biases; that male participants may show a larger magnitude of pseudoneglect than females; that right-handed participants may show an elevated magnitude of pseudoneglect compared to left-handed participants; and that using the left hand to respond may significantly increase the degree of pseudoneglect compared to using the right hand to respond. In addition, starting visuospatial line bisection on the left side of space was reported to induce greater leftward error than starting on the right side of space. The authors also emphasised that age has a significant effect on pseudoneglect with the leftward bias becoming less overt with ageing. Jewell and McCourt’s (2000) review provides a good understanding of the different types of methods that have been employed to explore visuospatial pseudoneglect, though a number of other methods have since been developed for measuring visuospatial pseudoneglect (Brodie 2010; Gamberini et al. 2008; Heber et al. 2010; Longo and Lourenco 2006; McCourt and Garlinghouse 2000; Varnava et al. 2002) as well as alternative methods of interpreting the bias (McIntosh et al. 2005). Pseudoneglect has also been demonstrated in the absence of direct visuospatial processing—when a person is required to mentally represent a stimulus. The term ‘representational pseudoneglect’ was coined to reflect this (McGeorge et al. 2007), again in analogy with the notion of a representational form of neglect as observed in brain damaged patients (Bisiach and Luzzatti 1978; Beschin et al. 1997a; Guariglia et al. 1993). A good illustration of a representational neglect is provided in Fig. 1 (reproduced with permission from Beschin et al. 1997a). There exists no current comprehensive review of representational pseudoneglect. In the present article we therefore seek to outline the studies that have explored representational pseudoneglect, consider a theoretical framework for the phenomenon and discuss how and why age impacts the bias— the development trajectory of the bias is an important emerging theme in the field. We first focus on the mental representation of visuospatial information in the absence of direct perception, mental representation driven by touch, and then the representation of numbers on a mental number line.

Fig. 1 Illustration of a case of representational neglect. Note: Figure from Beschin et al. (1997a, b) reproduced with permission, where more details are recalled from the right-hand side of the imagined scene regardless of imagined viewing perspective

The Mental Representation of Stimuli in Memory One of the clearest demonstrations of representational pseudoneglect is when participants are asked to mentally represent a stimulus that has been previously seen and retrieve it from memory. McGeorge et al. (2007) asked healthy participants aged 20 to 86 years old, living in Milan, Italy to imagine the highly familiar scene of the Piazza del Duomo (Cathedral Square) in Milan and to describe the landmarks on each side from two opposite viewing perspectives (see also original study with neglect patients by Bisiach and Luzzatti 1978). More landmarks were reported from the left side of the image than from the right, irrespective of the viewpoint. Given that the bias was based on a visuospatial mental representation, this suggests a representational form of pseudoneglect. Other studies have attempted, with some success, to replicate this finding. Bourlon et al. (2010) found that healthy control participants who were asked to describe from memory geographical landmarks in France showed a nonsignificant trend to report more elements from the left-hand side. Friedman et al. (2012) demonstrated a significant tendency of Canadian participants to locate various North American cities too far to the west (i.e. the left), consistent in part to the presence of a representational pseudoneglect. Representational pseudoneglect has also been shown for completely novel material. Dickinson and Intraub (2009) showed that undergraduate students could recall more details from the left hand side of photographs of real-world indoor and outdoor scenes compared to the right hand side, while a lateralised performance favouring the left side has been previously observed on the Corsi block-tapping task (Nalcaci et al. 1997). Della Sala et al. (2010) asked participants to view artificial spatial arrays containing objects of different shape and colour; once the array was removed participants were asked to recall the characteristics of the previously seen objects by choosing the relevant characteristics from subsequently presented exemplars (i.e., six possible colours and six possible shapes). There were more errors for recalling the characteristics of objects on the right side of the visual display. Relatedly, when participants judged the orientation of novel

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stimuli, they were most easily recognised when the body was oriented leftward (Barnett-Cowan et al. 2013). It has been suggested that mentally representing spatial layouts from highly familiar scenes may activate a visuospatial representation (McGeorge et al. 2007), which causes the mental representation to ‘behave’ in the same way as a visuospatial stimulus. One way to avoid this difficulty is to side-step any form of visual presentation by using completely novel mental representations created from aural-verbal descriptions in the complete absence of visual processing. Brooks et al. (2011b) asked healthy participants to listen, either monaurally or binaurally, to verbal descriptions of matrix patterns which were described as having ‘empty’ or ‘filled in’ cells, as illustrated in Fig. 2 (based on Della Sala et al. 1999; see also Brooks 1968). Participants were asked to form a mental representation of each pattern and judged which half of the matrix, left or right, was ‘fuller’ (i.e., contained more filled-in cells). On average participants judged that the left side was ‘fuller’ than the right; this asymmetry was particularly strong for left ear presentation—a condition that preferentially favoured the activation of the right cerebral hemisphere. Monaural presentation has been recently shown to induce contralateral hemispheric activity via the anatomical connections of hemispace to hemisphere (Gilmore et al. 2009; Lazzouni et al. 2010; Paiement et al. 2008; Schoenwiesner et al. 2007). Nevertheless, despite the strong leftward bias in mental representation there was no bias in lateralised memory recall—there was no difference in the detail actually recalled from the left versus right side of the mental representation. Similar findings were demonstrated by Brooks and Brandimonte (2013) where participants were asked to mentally represent real-world scenes consisting of streets with landmarks (i.e., shop, school, church, park) from auralverbal description: participants responded that the left side of the imagined street contained more landmarks than the right; but, again, there was no difference in lateralised recall. It could therefore be argued that the left side of a mentally represented stimulus may indeed be more perceptually salient than the

Fig. 2 Illustration of the pattern stimulus in Brooks et al. (2011b). Note: Figure reproduced with permission. The right side of the pattern (defined within a 3×3 matrix) is physically fuller than the left side (also defined within a 3×3 matrix), but the left side is perceived as fuller by participants

right side, but there may not be the capacity for retrieving greater detail from the more salient half (Brooks et al. 2011b). Reading direction is one candidate for explaining the origins of lateral biases like those summarised above: when the precise location of items in a described array is not constrained, preferred reading direction influences the pattern represented. Roman et al. (2013) showed that Spanishspeaking participants and Arabic speakers living in Spain tended to reproduce arrays aural-verbally described in Spanish in a left-right order, whilst Arabic speakers reproduced arrays aural-verbally described in Arabic in a right-left direction. Furthermore, for bilinguals, the language used at presentation determined the direction of recall. Although reading direction can impact visual line bisection (Chokron and De Agostini 1995; Chokron and Imbert 1993; Zivotofsky 2004), it is important to note that its influence has been separated from an overall left bias in bisection (Nicholls and Roberts 2002). It remains to be seen if these strong directional effects in recall of mental images on the Roman et al. (2013) task are accompanied by a smaller systematic representational pseudoneglect irrespective of preferred reading direction. The problem of ruling out a role for visuospatial perception at the root of lateralised biases is difficult, and progress is most likely if multiple sources of evidence from different manipulations converge. Recently, a paradigm based on visuospatial line bisection was used by Darling et al. (2012) to address this issue. Horizontal lines were presented for bisection in two conditions, a visuospatial condition (participants bisected a visible line) and a memory condition (participants identified where the mid point of a line had been from memory only after the line to be bisected disappeared). The lines were presented in extrapersonal space, at a distance where there is evidence that typical patterns of left bias in visuospatial pseudoneglect either disappear or reverse to become right-bias (e.g. Longo and Lourenco 2006). No significant bias was observed in the perception condition, but a significant leftward bias was observed in the memory condition. Additionally, there were

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differences in the relationship between line length and left bias between the memory and perception conditions. This study suggests that there was a marked, qualitative, difference between the characteristics of lateral bias between memory and perceptual conditions, arguing for an identifiably and specifically representational lateral bias when bisecting remembered lines in far space. The Mental Representation of a Stimulus Driven by Touch A representational form of pseudoneglect has also been demonstrated in the absence of direct visuospatial processing on tactile rod bisection. Tactile rod bisection conducted in the complete absence of direct visual processing can be referred to as a representational task where the representation of spatial layout is driven through touch and not vision. Bowers and Heilman (1980), who coined the term ‘pseudoneglect’, were among the first to demonstrate that college-aged participants bisected centrally presented wooden rods of different lengths—in the absence of vision—with the index finger of both the left and right hand, significantly towards the left hand-side of true centre. Pseudoneglect was also greatest when starting the exploration from the right hand side of the rod, though in this study participants were allowed to scan the rod as many times as preferred so the starting position for exploration did not necessarily equate to the direction that the bisection was made from. Research conducted since this original study has produced largely consistent results, though some studies that systematically controlled hand used have not observed pseudoneglect across both hands at response (e.g. Brodie and Pettigrew 1996; Chokron and Imbert 1993; Hatta and Yamamoyto 1986; Laeng et al. 1996), though some have (e.g. Sampaio and Philip 1991), whilst others provide data that are inconclusive (Sampaio and Chokron 1992; Levander et al. 1993). An evaluation of scanning direction, starting position, bisection direction, and the number of scans on tactile rod bisection was conducted by Baek et al. (2002), who found that when participants tactilely scanned horizontal rods once (left-right, right-left) before bisecting ‘on the way back’ there was a bias in the direction of the current movement—referred to as a possible ‘overshoot’ phenomenon (see also Philip and Hatwell 1998). At first glance, this would appear to be in line with a scanning theory of pseudoneglect; but bisecting from the right hand-side induced greater overshooting than bisecting from the left. A similar pattern of results was seen for multiple scans of the rod and, for both conditions, bias did not scale with rod length. Brooks et al. (2011a) conducted tactile rod bisection with healthy participants aged between 3 and 84 years of age, who used touch alone without vision for bisection. Participants across all age groups, except those approaching or in adolescence, showed pseudoneglect on tactile rod bisection. The

authors also found that starting on the right side of the rod and bisecting from the right enhanced the magnitude of pseudoneglect. Other studies that have controlled the starting position but not the final direction from which the bisection is made report no effect of start side (Bowers and Heilman 1980; Laeng et al. 1996), likely because sometimes participants bisected from the left and sometimes from the right. The start right effect on tactile rod bisection is difficult to explain as simply ‘overshooting’ the middle of the rod (i.e., Baek et al. 2002) since there is not symmetrical ‘overshooting’ bias when starting left and starting right (Brooks et al. 2011a). Hach and Schütz-Bosbach (2012) manipulated stimulus location (left – right), stimulus length, start side and participant handedness to observe effects on tactile bisection. Overall, performance on the tactile bisection task was modulated by these factors in a broadly similar manner as is typically seen in visuospatial bisection. However, there were also differences in the effects of these mediators compared to typical visuospatial bisection patterns: biases were pronounced only in the longest lines (as was ‘centrifugal’ error where lines presented in left hemispace show bias to the left, and those presented to the right show deviations to the right). Two further aspects of this study are noteworthy: firstly, there was no significant leftward deviation across all participants when lines were presented midsagitally (though a bias did emerge when location was collapsed across all positions). Secondly, mixed-handers showed comparatively minimal evidence of lateral bias as opposed to left and right handed participants. When considering the effect of factors like rod or line length on the magnitude of pseudoneglect, it is worth remembering that the bias may be expressed differently between studies. For example, the magnitude of pseudoneglect may be expressed as ‘percentage deviation’ (i.e., Brooks et al. 2011a) or signed error to the nearest centimetre (i.e., Bowers and Heilman 1980). One outstanding question relates to the strategy employed during tactile rod bisection. Sampaio and Chokron (1992) found leftward biases on a range of ten rods (14 to 32 cm) presented only at midline in the absence of vision when the index finger was used to bisect the rod for both left and right handed participants—but when a cursor was used for bisection the directional error was contralateral to response hand. In this study, participants reported that directly using their index finger prompted them to imagine the stimulus as a whole prior to bisecting, but using the cursor induced perceived duration movement to be transferred into a length estimate. The former sensory strategy is perhaps more consistent with visuospatial line bisection in which the whole stimulus is perceived all at once. The latter strategy could be interpreted as a temporal order strategy and could potentially be consistent with participants overestimating the duration of movement. Laeng et al. (1996) also found, in the absence of vision, leftward biases for rods of different lengths (24, 28, 30, 35, and 40 cm) but that a secondary verbal task, designed to boost activation of the left

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hemisphere, had no influence on bisection performance. Importantly, this undermines the likelihood that a temporal order strategy such as counting was automatically used during tactile rod bisection as the secondary verbal task should, in theory, have disrupted the counting strategy. Traversing a rod in tactile rod bisection requires participants to uncover the stimulus over time: within this context it seems that the orienting of attention towards the left-hand side of a stimulus is an automatic and involuntary process. Some visuospatial line bisection experiments that have directly tested this issue still report evidence of leftward bias, even when scanning behaviour and preferred reading direction is directly controlled (Nicholls and Roberts 2002). Although the role of strategy in tactile bisection is not clear, the impact of strategy on visual bisection has been directly tested. In the ‘greyscales’ task (Nicholls et al. 2005) participants select which of two shaded lines positioned one above the other is darker or lighter: one line is always simply an identical copy of the other but mirror reflected, hence any bias in luminance judgement is thought to reflect a lateral bias. Nicholls et al. (2005) found the same performance for luminance judgements on this task when participants were forced to use a ‘comparison strategy’ (i.e., explicitly compare left and right portion of a stimulus with separated left and right portions) versus a ‘global strategy’ (i.e., view stimulus as a whole not separated). Relatedly, Varnava and Halligan (2009) asked 140 participants to perform a traditional visuospatial line bisection task with five horizontal lines (18 cm) and then report the strategies they used while doing so. Three main strategies arose from participant reports: 1) extracting the centre of the line first, 2) making a comparison between the two portions of the line, 3) using an external frame of reference such as the body, the page, or an imagined stimulus (a piece of wood that needs to be sawed in half). Regardless of the strategy used, however, participants deviated towards the left-hand side. So, for visuospatial bisection it seems that neither scan direction, reading direction or strategy application fully accounts for the leftward lateral bias—it would be of great interest to further pursue the influence of scanning direction for tasks designed to measure representational forms of pseudoneglect from either tactile rod bisection or aural-verbal description. An associated finding was reported in a study with right hemisphere damaged patients and healthy control participants (mean age 45 years) who were asked to find a marble in a tactile maze in the absence of visual input; control participants were significantly faster at finding the marble when it was placed in near space but showed no lateralised bias in accuracy (Beschin et al. 1996). However, it was later reported that while neglect patients were faster when searching on the right-hand side of the tactile maze (as might be expected), there were hints in the data that control participants were faster when searching on the left under certain conditions when gaze and the position of the head and trunk was carefully controlled (Beschin et al. 1997b).

One of the strongest lines of evidence for a purely representational form of pseudoneglect on tactile rod bisection should come from the finding that early blind participants have also been found to display leftward biases when bisecting rods (Cattaneo et al. 2010). This is of particular interest since early blind and late blind participants have been found to have superior tactile acuity skills relative to healthy sighted participants (Norman and Bartholomew 2011; Wong et al. 2011). Another early study showed that participants who were blind from birth demonstrated rightward biases on a tactile rod bisection task regardless of arm posture (i.e., whether or not the arms crossed the body midline) but participants who were early-blind (with some early vision) demonstrated both rightward and leftward biases depending on the position of the arm—crossed and uncrossed respectively (Bradshaw et al. 1986). In the same study, fully sighted participants showed consistent leftward biases regardless of arm posture (Bradshaw et al. 1986). Coudereau et al. (2006) found that only blind individuals with experience in performing tasks of a tactile nature showed a leftward bias on a tactile rod bisection task—though the direction from which the bisection was made and the hand used for bisection was found to be influential. Utilising the right hand resulted in significant leftward biases whereas utilizing the left hand resulting in significant rightward biases; the same leftward/rightward biases were observed when starting right/left respectively. Of note here is that participants were limited in the number of times they traversed the rod—it would have been interesting to compare this to a condition where there was unlimited exploration of the rod prior to bisection (i.e., Bowers and Heilman 1980). Taken together, these studies indicate that visual experience— even partial, early or limited in nature as well as tactile acuity—may influence the representation of space (i.e., Bradshaw et al. 1986; Cattaneo et al. 2010, 2011a; Sampaio et al. 1995). The performance of blind versus sighted individuals on tactile based tasks may also allow us to make some further secondary observations about how sensory information in the absence of vision is processed. Previous research has shown that tactile stimulation may be remapped into an external spatial frame of reference (Azañón et al. 2010; Azañón and Soto-Faraco 2008). The activation of spatial frames of reference, body-centred versus eye-centred, may differ for sighted versus blind individuals (Cattaneo et al. 2011a)—perhaps due to the way in which they have explored the world. To specify, sighted individuals may be more likely to use an eye-centred frame of reference whereas blind individuals may be more likely to use a body-centred frame of reference. The Mental Representation of Numbers Many studies have now indicated that a form of representational pseudoneglect occurs for tasks involving the mental

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representation of small and larger numbers. Empirical observations have indicated that smaller numbers are typically represented on the left side of space and larger numbers on the right side of space (for a review see Hubbard et al. 2005; see also Dehaene et al. 1993; Gevers et al. 2010). Despite the fact that in some of these studies the number stimuli were initially presented in visual form, the bias itself is representational in nature. One example of this was provided by Loftus et al. (2009) who asked participants to decide which flanker number was further away from the middle number in a triplet (i.e., 15-22-47) and found that there was a consistent bias in the direction of the lower numerical flanker; a similar result was found for negative numbers. Loftus et al. (2008b) also found leftward biases are influenced by the processing of large numbers (see also Longo and Lourenco 2007; Nicholls and Loftus 2007, for alphabet bisection). Furthermore, these biases are resolved by visuomotor adaptation (i.e., Loftus et al. 2008a). Consistently, Calabria and Rossetti (2005) showed that when healthy participants were asked to bisect lines of words that represented smaller numbers (i.e., ‘four’) there was a tendency to bisect towards the left but for lines of words that represented larger numbers (i.e., ‘nine’) the bias was significantly reduced. Loetscher et al. (2010) demonstrated a comparative bias when participants were asked to choose a number between 1000 and 10,000; healthy participants were biased towards choosing a smaller compared to relatively larger number. A study by Loetscher et al. (2008a) showed that the processing of small numbers elicited leftward eye movements (see also Fischer et al. 2004; Sullivan et al. 2011). Relatedly, Di Luca et al. (2013) have shown that numeric laterality effects occur when participants carry out two-dimensional cancellation tasks (modelled on the star cancellation task used in neglect assessment: Halligan et al. 1989)—participants’ attention shifted to the left hand side of the array if the star array also contained low numbers, and towards the right if it contained higher numbers. Additionally, there is evidence of a small number bias (i.e., leftward bias) in random number generation tasks (i.e., Dehaene 1997) and that this can be manipulated by rotating the head left and rightwards (Loetscher et al. 2008b). Numeric biases can be manipulated by cognitive functions which selectively affect the activation of the hemispheres—tapping on the right of space increases rightward bias whilst tapping on the left hand side of space increases leftward bias (Cattaneo et al. 2011b). Taken together, these results provide evidence of a lateral bias within a number space that clearly has spatial characteristics. One telling piece of evidence supporting this view was reported by Fischer (2008) who found that, in general, participants started counting with the fingers on their left hand independently of handedness. A detailed review of the relationship between number and spatial representation has been provided by Umilta et al. (2009).

The most powerful of evidence for a purely representational pseudoneglect on the mental number line, however, comes from the finding that blind participants display the same leftward biases when bisecting the mental number line; in the case of congenitally blind participants it is impossible that early visuospatial processing contributed to the bias (Cattaneo et al. 2011c). Although the evidence certainly points towards the existence of a mental number line with smaller numbers located on the left and larger numbers on the right, recent evidence from the neglect literature suggests an alternative theory. It has recently been shown that regardless of the represented spatial position, left or right, righthemisphere impaired patients overlook smaller numbers (Aiello et al. 2012). This suggests that there is an issue with the coding of numerical magnitude itself. When considering the neurologically healthy brain it follows that there may be a distortion for larger numerical magnitudes: a fruitful avenue for further research in the field.

An Account of Pseudoneglect: The Action Orientation Hypothesis Visual-Spatial Pseudoneglect The activation-orientation hypothesis (Reuter Lorenz et al. 1990) was originally put forward to explain the outcome of visuospatial line bisection and can be outlined as follows: contralateral attentional orienting by the right hemisphere leads to leftward bias because the leftward orientation of attention results in the left portion of the line being perceived as longer than the right portion of the line (see also Heilman and Van Den Abell 1979; Kinsbourne 1970). Hence, the perceived middle of the entire line is shifted towards the left hand side. Earlier work by Kinsbourne (1970) postulated that attention is directed to contralateral space by the most dominant hemisphere; it was thought that in right-handed participants this would be the left hemisphere which is specialised for language processing. Following this theory, we would therefore expect to observe biases in visuospatial attention towards the right hand side of space and not the left. This early theory was later revised in the light of emerging evidence that cast doubt upon the dominance of the left hemisphere for visuospatial attention. Reuter Lorenz et al. (1990) observed that left visual field presentation of lines induced pseudoneglect while the right visual field presentation of lines attenuated or reversed this bias, supporting the notion that pseudoneglect was a product of contralateral attentional orienting by the right hemisphere. In the following section we review how well this explanation accounts for representational pseudoneglect. Two critical assumptions of the activation orientation hypothesis here are: 1) that the leftward

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orientation of attention is conducted by the right hemisphere; 2) that the leftward orientation of attention by the right hemisphere leads to the left portion of a stimulus being perceived as longer than the right. The first assumption is supported by studies with right hemisphere impaired (neglect) patients confirming that the right cerebral hemisphere is involved with orienting attention towards the left side of space: when damaged it loses this capacity and a strong rightward bias is typical. Although critical lesion sites within the right hemisphere can be difficult to define (Rorden and Karnath 2004), unilateral left neglect is thought to most commonly follow a lesion to the right parietal lobe (Bartolomeo and Chokron 2002; Danckert and Ferber 2006; Halligan et al. 2003; see also Gottlieb and Snyder 2010; Mort et al. 2003; Paterson and Zangwill 1944; Posner et al. 1984). Neuro-imaging, neuro-conduction and electrophysiological studies also demonstrate that the right hemisphere itself is preferentially activated during visuospatial processing and line bisection in healthy participants (Fink et al. 2000a; see also Blankenburg et al. 2010; Çiçek et al. 2009; Fink et al. 2000b, 2001; Foxe et al. 2003). Further evidence comes from ‘knocking out’ these critical right hemisphere regions using Transcranial Magnetic Stimulation (Bjoertomt et al. 2002). Furthermore, interoperative electrical stimulation of parietal regions and in particular the superior occipitofrontal fasciculus has been observed to mediate the severity of line bisection deviation (Thiebaut de Schotten et al. 2005), pointing to subcortical (right) parietal-frontal pathways that may form the basis of a network related to the emergence of neglect-like symptoms (see also Thiebaut de Schotten et al. 2012). There is recent evidence that this parietal-frontal network is larger in the right than the left hemisphere (Thiebaut de Schotten et al. 2011), as depicted in Fig. 3. In addition, a study using parietal theta burst stimulation has indicated that neglect and pseudoneglect share common neural mechanisms (Varnava et al. 2013). Taken together these data go some distance toward understanding the relationship between pseudoneglect and clinical neglect, and provide a sound basis in brain structure to explain the righthemisphere dominance component of the actionorientation hypothesis. The second critical assumption of the activation-orientation hypothesis is supported by an experiment reported by Bultitude and Davies (2006) who showed that lateral cueing to the left or right hand end of a line prior to a bisection led to left- and right- shifts in perceived mid point respectively. These results suggest that the preceding cue biased attention towards one portion of the line which resulted in that portion being perceived as longer, and thus represents independent evidence that the second assumption is supported. Similar results have been reported since (Toba et al. 2011). In the case

of visuospatial line bisection there is evidence for both key components of the activation orientation hypothesis. Representational Pseudoneglect The two critical assumptions of the activation orientation hypothesis that the leftward orientation of attention is conducted by the right hemisphere and that the leftward orientation of attention by the right hemisphere leads to the left portion of a stimulus being perceived as longer than the right need to be evaluated for mental representation if the action orientation hypothesis is considered to be a useful basis for understanding laterally distorted representations. In relation to the right hemisphere claim, the evidence is clear. Gobel et al. (2006) found that repetitive Transcranial Magnetic Stimulation (TMS) applied over right parietal regions (but not the occipital region) during mental number line bisection induced performance consistent with ‘neglect’ - a bias towards larger numbers with the perceived numerical midpoint shifted rightward. Oliveri et al. (2004) observed that TMS over the right parietal region counteracted the typical leftward mental number line bias. Cattaneo et al. (2009) also found that TMS over the right angular gyrus, but not the left, disrupted the priming of attention towards smaller numbers on the left side of the mental number line for healthy participants. Kadosh et al. (2010) used TMS over the left and right intraparietal sulcus while participants performed a samedifferent task with visually presented digits (‘5’) or auralverbal numbers (“five”); TMS over the right parietal lobe disrupted the processing of digits but not aural-verbal numbers (see also Rusconi et al. 2013). With regard to the second assumption, Nicholls and McIlroy (2010) asked college-aged participants to bisect number triplets that were presented with or without a lateralised cue to the left or right-hand side. The leftward bias for mental number line bisection was attenuated for right lateralised cues, in-line with the notion that when attention is directed laterally that portion of the stimulus is perceived as ‘longer’. Although the cue was visual in nature the mental number line was representational. Arguably, if a common spatial representation is the source of both visuospatial and representational pseudoneglect, we might expect a similar degree of bias on these tasks. Indeed, studies employing prismatic adaptation in neurologically normal participants that cause neglect-like distortions of visual perception also produce similar distortions of representation in the number line (Nicholls et al. 2008a). Furthermore, number line asymmetry has been reported as being systematically related to lateral bias in visuospatial bisection tasks: pseudoneglect observed on the mental number line was greater for participants who also showed larger leftward biases on visual line bisection (Longo and Lourenco 2007), and mental number line bisection, like physical line bisection, shifted

Neuropsychol Rev Fig. 3 Depiction of a parietofrontal network for visuospatial attention as described in Thiebaut de Schotten et al. (2011), Fig. 1(b)

from a leftward bias at near distances (60 cm) towards a rightward bias at far distances (240 cm: Longo and Lourenco 2010)—furthermore there was a correlation between individual participants’ bias on physical and mental number line bisection. There are also similarities between the response of the two types of bisection task to visual approach (Longo et al. 2012). The commonality between the mental number line and the line bisection results here is striking, provoking the suggestion that similar attentional orienting mechanisms underlie both visuospatial and representational bisection tasks. There is also a more intricate link between these two tasks: Loftus et al. (2008b) asked healthy participants to perform a variation of the Greyscales task (i.e., lateral luminance judgements) and simultaneously to report whether an overlaid stimulus was high (the numbers 8 or 9), low (the numbers 1, 2) or neutral (the symbol #). Leftward biases on the Greyscales task were attenuated by processing a high number and vice versa. This evidence of a linkage between a measure of visuospatial pseudoneglect and the simple processing of a digit indicates an overlap between the representation of numbers and space. This finding has since been broadly replicated (Nicholls et al. 2008b) using different types of responses (i.e., parity judgement vs. linguistic labels). Similarly, Lourenco and Longo (2009) asked participants to hold in mind small or large numbers in working memory whilst performing the traditional mental number line bisection task (i.e., report the midpoint between a pair of numbers); when participants held small numbers in mind responses were further leftward.

Recent evidence also suggests that touch-driven bisection biases can be influenced by the presentation of numbers. Cattaneo et al. (2012a) replicated with control participants the typical pseudoneglect on tactile bisection. However the presentation of repetitive task irrelevant verbal stimuli modulated this bias—when a high digit was presented, bisections deviated rightwards compared to a control condition (‘blah’), whilst low digits were associated with leftward deviations, a pattern consistent with some degree of commonality between spatial and numeric representations. A broadly similar pattern was also observed in blind participants (see also Cattaneo et al. 2010). It has also been observed that binaural exposure to white noise during the conduction of both a tactile and visual bisection task reduces typical leftward biases, as binaural input activates both hemispheres bilaterally (Cattaneo et al. 2012b). It is possible that bilateral activation help balance the initial right hemisphere advantage for these spatial tasks. However, Chokron et al. (2002) found that healthy control participants showed a non-significant leftward bias on tactile bisection but a significant leftward bias on visual line bisection (somewhat in contrast to neglect patients who demonstrated rightward biases only on visuospatial bisection). Performance on these tasks did not correlate for the control participants (or the neglect patients). We also note the differences that exist between the patterns of lateral bias at perception and during representation (e.g. Brooks and Brandimonte 2013; Darling et al. 2012), which implies some difference in the system that underlies each form of the bias—a question that would be a fertile target for future research. In a recent review of neglect across different modalities, Gainotti (2010)

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argued that although left neglect is readily demonstrated in the visual, auditory and tactile domains, the severity of neglect is greater for the visual then for non-visual domain (see also Bartolomeo et al. 1994). It might be that the same is true for pseudoneglect. A further factor that may help us understand how visuospatial and representational pseudoneglect compare is the effect of starting side on lateral biases. Brooks et al. (2011b) found that imagining starting left during the creation of a mental image from aural-verbal description was found to elicit greater pseudoneglect; this is of particular interest because the start side was imagined. A number of studies with visuospatial line bisection have found that starting left elicits a greater bias (Jewell and McCourt 2000); this consistency suggests common mechanisms of bias between representations assembled through verbal-aural instruction and visual neglect. Similarly, Cocchini et al. (2007) asked participants to imagine the time that it took for a ball to rotate in a virtual trajectory around their bodies—starting left and moving to the right (anticlockwise) or starting right and moving to the left (clockwise). Participants underestimated the time that the ball took to move in a clockwise direction (starting right and moving left)—arguably consistent with the left—hand side being perceived as ‘longer’. Urbanski and Bartolomeo (2008) found no effect of starting side in a representational task: both neglect patients and healthy participants were required to first mark the left endpoint of a visual or imaginary line, then the midpoint, and then the right endpoint of the line (or vice versa starting right to left), thus allowing a comparison between visual-physical and visual-imagery conditions. The authors found that control participants erred leftward in all conditions regardless of imagined or physical starting side. Thus, while the role of starting side in tasks where a representation is held in mind is still emerging and likely influenced by the heterogeneity of tasks employed, further research in this field may help inform how representational pseudoneglect is modulated. The extent to which the lateral bias on mental number line is purely a manifestation of the same type of lateral bias observed on visuospatial bisection is somewhat unclear as there are cases of dissociation between mental number line and visuospatial line bisection, for example in the case of developmental dyscalculia (i.e., Ashkenazi and Henik 2010). Furthermore, the asymmetrical manipulation of cortical activation (via verbal and nonverbal dual tasks) alters the size of the leftward bias in random number generation (Loetscher and Brugger 2007), and this pattern varies more systematically with ‘prefrontal’ fluency rather than ‘parietal’ learning and memory tasks (Bachmann et al. 2010). Finally, individuals with amblyopia who tend to bisect lines slightly to the right of the veridical centre (Thiel and Sireteanu 2009) may show a slight left bias in numeric bisection though the size of this is less than that observed in normally-sighted controls (Mohr et al. 2010).

A recent study by van Dijck et al. (2012) has questioned the unity model of numero-spatial representation space: a principal components analysis of a number of laterality related tasks across healthy and right braininjured patients indicated that the variance in lateral bias was best accounted for using a multicomponent model rather than a single component. It has also been reported that when healthy participants bisect visually presented lines there may be individual differences in the direction and magnitude of bias (Manning et al. 1990; see also Cowie and Hamill 1998) and sometimes a reversed rightward bias or no bias at all is observed (Braun and Kirk 1999). These findings are important to consider in the current context because they indicate the dynamic nature of spatial attention. To sum up, the evidence that mental number representations mirror perceptual pseudoneglect patterns, and hence that they can be attributed to a similar explanation based on action orientation is reasonably compelling. However, whether visual-perceptual and tactile representational bisection tasks hold exactly the same processes in common is a question for future research. Other Theories of Pseudoneglect Two studies have been mentioned here that clearly demonstrate that attention can be readily cued to one side of space during visuospatial line bisection (Bultitude and Davies 2006; Toba et al. 2011) and, as a result, mediate directional error in that direction. Other demonstrations seem to support these findings. For example, Fischer (1996) presented horizontal lines in isolation or with word flankers that were either three or six letters in length and found word length significantly influenced bisection performance in the direction of the longer word. Likewise, Garza et al. (2008) found under normal viewing conditions that visual line bisection performance was significantly biased by the presence of the experimenter standing to the left or right handside of space. McCourt et al. (2005) showed that several factors, like physical cues and stimulus geometry, can combine to produce cueing effects (i.e., like leftward or rightward pointing wedges combined with lateralised cues) (see also Nichelli et al. 1989; Milner et al. 1992; Fischer and Stumpp 2001). In the cases of attentional flankers, however, it is highly possible that attentional orienting was not the driving force behind the observed pseudoneglect. Rather, the principles of perceptual grouping (see Rock and Palmer 1990) may also adequately explain the bias with the line simply being merged into the flanker and thus being perceived as longer; a result that may be more in line with ‘centroid extraction’ than attentional orienting (i.e., Morgan et al. 1990; Porac et al. 2006; Toba et al. 2011; Harvey et al. 2000). The main issue is that presenting a cue and a stimulus at the same time, or within a rapid timeframe, may allow the cue to combine with the line stimulus

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hence activating perceptual grouping, though this is more difficult to argue in the case of an actual person acting as an attentional cue (i.e., Garza et al. 2008) and there has been some discussion as to whether or not ‘invisible cues’ (i.e., a virtual bisection is traced in mid-air with the pen) can help dispel this argument (Harvey et al. 2000; see also Mattingley et al. 1993). However, it is debatable as to whether or not even so-called invisible cues may, arguably, activate perceptual grouping given the length of time that would be involved with virtually bisecting the line. Other accounts of pseudoneglect involve a relative over-activation or under-activation of motor systems in the right hemisphere (Heilman and Valenstein 1979) or an argument that the hand’s initial position and the subsequent ‘visuo-motor-scanning’ direction drive an ‘attentional spotlight’ resulting in a ‘just noticeable difference’ slightly weighted in the direction of starting position (left vs. right)—regardless of which hand is used (Halligan et al. 1991). These theories, however, are inconsistent with the literature published over the past decade in the visuospatial pseudoneglect field (see Jewell and McCourt 2000) and are also unable to explain pseudoneglect in tasks not driven by physical, motor or direct visuospatial processing—including the multiple examples of representational pseudoneglect described in this article.

The Developmental Trajectory of Pseudoneglect Across the Lifespan Models of Cognitive Ageing and Lateralisation The empirical observation of pseudoneglect across lifespan in children, mid-age, and older adults is of particular importance for this review. An understanding of how representational pseudoneglect develops, and whether or not it endures across lifespan, is relevant for understanding the phenomenon as a whole and the cognitive mechanisms that underlie it as well as contributing to models of cognitive ageing. If, for example, representational pseudoneglect is observed across lifespan, this contradicts current models of cognitive ageing which postulate that cognition becomes less lateralised with age (McGregor et al. 2009; Przybyla et al. 2011; Vallesi et al. 2010). The majority of research exploring the developmental trajectory of pseudoneglect has been conducted in the visuospatial domain, but there are hints in the literature with regards to representational pseudoneglect. Here, we summarise the visuospatial literature first to provide a framework for discussion and then present the representational literature. The Hemispheric Asymmetry Reduction in Older Adults (HAROLD) model (Cabeza 2002) is one of the most widely accepted models of cognitive ageing (see also Salthouse, 1996,

2009). HAROLD argues that with increasing age cognitive functioning becomes less lateralised at the neural level; the model would thus be inconsistent with evidence of biases that are retained or strengthened with increasing age. It is important to note that there are existing specialised papers that have provided a far more in-depth analysis of research around the HAROLD model which provide substantial support for its main claims (e.g. Cabeza 2002; Cabeza et al. 1997a, b, 2000; Jimenez-Jimenez et al. 2011; Dolcos et al. 2002; McGregor et al. 2009; Prakash et al. 2009; Przybyla, Haaland, Bagesteiro and Sainburg, 2011; Reuter-Lorenz et al. 2000; Vallesi et al. 2010; Velanova et al. 2007; Zhu et al. 2011). Cabeza et al. (2002) argue that the HAROLD model implies that older adults would recruit both hemispheres in a compensatory strategy for general lessening of lateralisation or a difficulty with accessing lateralised functions. It is possible that the less lateralised performance of older participants is due to the fact that older brains ‘compensate’ for general cognitive decline by employing additional activation from different areas and therefore recruit a greater number of regions in this ‘compensatory strategy’ (i.e., Cabeza et al. 1997a, b). It is worth noting that Cabeza et al. (2002) using PET found that the prefrontal cortex was indeed more asymmetrically active in younger versus older adults but that this was related to the level of performance; low-performing older adults and young adults both engaged similar networks whereas high-performing older adults activated additional networks. HAROLD primarily attempts to understand adult aging patterns but it has been suggested that changes in lateralisation apply throughout the lifespan, specifically that the brain gradually becomes more lateralised from birth to early adulthood and then lateralisation starts to decline again in older age due to a growing general difficulty in engaging lateralised functions (see Dolcos et al. 2002). In contrast to the HAROLD model, an alternative right hemiageing model argues that the hemispheres age differentially with the right hemisphere ageing faster or more detrimentally than the left hemisphere (see a discussion of this issue within Dolcos et al. 2002). The right hemiageing model has support from studies comparing performance on left hemisphere lateralised language tasks and right hemisphere lateralised visuospatial tasks (Goldstein and Shelly 1981; Klisz 1978). More recently, Prodan et al. (2007) presented participants aged 20 to 78 years with drawings of faces which displayed different emotions on the upper and lower halves of the face; when specifically instructed to pay attention to the upper half of the face older participants aged over 62 years showed a deficit in identifying the facial emotion relative to younger participants and this was especially noticeable in the left visual field (right hemisphere). In the following section we consider how representational pseudoneglect can potentially be understood within these models of cognitive ageing.

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Representational Pseudoneglect and Ageing In this section we address the effect of age on mental representation driven by touch and on the mental number line – the two main tasks where interesting results have recently emerged. It is very useful to review studies focusing on the effect of age on visuospatial pseudoneglect: these studies provide important insights and ideas for future research in the representational field. The representational Piazza del Duomo study of McGeorge et al. (2007) found that that the leftward bias in recall increased as age increased (the older the participant the greater the leftward bias). Brooks et al. (2011a) asked participants aged between 6 and 96 years old to bisect a wooden rod at its middle using only touch in the absence of vision (Experiment 2). There was a significant leftward bias for adult participants but most notably in the oldest participants; for the youngest participants there was no significant pseudoneglect bias, though there was a trend towards the left (Fig. 4). Chen et al. (2011) reported that for participants aged between 22 and 93, females tended to show leftward biases regardless of age—whereas males showed rightward biases in older age (see also Roig and Cicero 1994); this suggests that there is a sex-specific as well as age-specific element to the bias. It is hard to accommodate the results of these studies within the context of the HAROLD model, as these studies suggest that lateral bias should increase with age. If pseudoneglect increases with age, or even remains consistent, it follows that the theory of right hemisphere attentional orienting is the best account for the data. There is certainly no current empirical basis for a different system that underlies pseudoneglect in older versus younger adults. Brooks et al. (2011a) found that starting right significantly increased the bias—an effect also magnified for older adults. One argument is that when the

direction of physical movement was consistent with the theoretical direction of attentional orienting by the right hemisphere, right to left, then the combination of both attentional orienting and physical movement in the same direction lead to the left side of the stimulus (the rod) being more heavily weighted than the right side (Brooks et al. 2011a). The weighting of the left side may then lead to greater salience for the left side of the stimulus which induces a leftward bias when a judgement of magnitude is made. Critically, the presence of the asymmetrical modifying effect of starting on the right—a phenomenon that is not generally reported in visuospatial bisection tasks—implies that tactile bisection tasks implicate some discrete processes that are not involved in visuospatial tasks. Focusing now on the spatial representation of numbers, changes to numbers have been shown to elicit activity in right parietal and prefrontal cortex of 3 month old infants (Izard et al. 2008) and pre-schoolers have been found to search an array of boxes in a horizontal line (i.e., ‘rooms’) faster and more accurately when labelled in ascending numerical order (Opfer and Furlong 2011; see also Opfer et al. 2010). Likewise, Berch et al. (1999) found children approximately 9 years of age readily demonstrated the SNARC effect (Spatial Numerical Association of Response Codes) (i.e., Dehaene et al. 1993). While there may be an early and automatic association between numbers and space, the mental number line is difficult to assess across the entire lifespan because familiarity with numbers may strongly influence how they are mentally represented (Berteletti et al. 2010; Ebersbach et al. 2008; Moeller et al. 2009; Nuerk et al. 2004). Moreover, reading direction may also have an influence on mental number representation tasks (Kazandjian et al. 2010). van Dijck et al. (2011) showed for healthy participants aged 52 to 58 years no clear bias on mental number line bisection. Another issue concerns how working memory function declines with increasing age (Hartman and Warren 2005; Johnson et al. 2010; Park et al. 2002)—differences in performance for older compared to younger adults found on mental number line tasks may actually be reflective of unreliable working memory. Visuospatial Pseudoneglect and Ageing

Fig. 4 The mean percent deviation score for participants in each age group in Brooks et al. (2011a). Note: Figure reproduced with permission. Negative values indicate a leftward bias while positive values indicate a rightward bias

The evidence for the effect of age on visuospatial pseudoneglect is undoubtedly more abundant and can provide important insights when considering the effect of age on representational pseudoneglect from a theoretical point of view. ‘Symmetrical pseudoneglect’ refers to a pattern of leftward bias when responding with the left hand but a rightward bias when responding with the right hand (Fig. 5). Bradshaw et al. (1987) found that left-handed children around or younger than 5 years of age showed leftward bias with the left hand but rightward bias with the right hand indicating symmetrical

Neuropsychol Rev Fig. 5 A graphical illustration of symmetrical biases in a visuospatial line bisection task. Note: The values are fictitious and do not represent real magnitude of bias. Positive values are illustrative of rightward biases; negative values are illustrative of leftward biases

pseudoneglect. Dellatolas et al. (1996) also found that children aged four to 5 years demonstrated rightward biases with the right hand but leftward biases with the left hand, but children aged 10 to 12 years demonstrated leftward biases regardless of hand; this is an important observation hinting towards the fact that hemispheric maturation changes the way in which attention is directed to each side of space, though there is some discrepancy over precisely when this change actually occurs. Hausmann et al. (2003) found that participants aged 10 to 12 years showed a symmetrical line bisection bias towards the left with the left hand but to the right with the right hand; participants aged 13–15, 18–21 and 24–53 bisected towards the left with both hands—though more strongly towards the left with the left hand compared to the right hand (see also Hausmann et al. 2002). Likewise, Failla et al. (2003) found that participants aged 5 to 7 years and 60 to 70 years also showed evidence of a symmetrical bias; participants aged 10 to 12 years and 20 to 30 years showed leftward biases in general—though the greatest bias was when the left hand was used. For older adults, symmetrical biases on visuospatial line bisection are consistent with the HAROLD model of cognitive ageing as symmetrical biases represent more balanced activation of the cerebral hemispheres and a reduction in the increased activation of the right hemisphere relative to the left. For children, symmetrical biases also indicate a more balanced activation of the cerebral hemispheres but not necessarily because there has been a reduction in right hemisphere activation; rather this may indicate an immature attentional orienting system. One theory is that corpus callosum maturation can explain the symmetrical nature of the biases of younger children, with incoming visuospatial information not being immediately transferred to the right hemisphere—in this case the initially activated left hemisphere retains control of directing attention rightward (Hausmann et al. 2003). It is possible that adolescents would produce a very noisy bisection since there are many changes during adolescent at the neural and structural brain level (Sisk and Zehr 2005; see also Giorgio et al. 2010). However,

Pulsipher et al. (2009) explored corpus callosum volume in children aged 8 to 18 years but found no significant relationship between corpus callosum volume and right hand deviation, left hand deviation, or differences between directional error by hand for any age group. A direct exploration of how corpus callosum maturity directly affects representational pseudoneglect in children and adolescents would be a fervent area for future research. It is worth remembering that Wolfe (1923) also reported that on visuospatial line bisection older children in the ‘eighth grade’ (i.e., probably around 12 years old) were equivalent in their line bisection performance compared to adults, but younger children showed larger errors. Exploring the effect of age on visuospatial forms of pseudoneglect is certainly not straightforward in children. van Vugt et al. (2000) found, when exploring visuospatial line bisection in 650 participants aged 7 to 12 years, several variables such as gender, handedness, response hand, age and stimulus variables such as orientation, length, as well as position all interacted to modulate the degree and direction of pseudoneglect. Overall, the broad picture from visual pseudoneglect studies suggests a pattern of symmetrical pseudoneglect in children, which becomes increasingly biased to the left in young adulthood, and which returns to a more symmetrical pattern in older adults—a pattern that is fundamentally consistent with the HAROLD model. However some reported results do differ from this general pattern. Firstly, there is the evidence of a difference in male and female performance trajectories (Chen et al. 2011; see also Roig and Cicero 1994). Secondly, there are data suggesting that rightward bias is prevalent in older age—a pattern that might be thought of as more consistent with the right hemiageing model. Stam and Bakker (1990) demonstrated rightward biases in line bisection in older samples: participants with a mean age of 58 years demonstrated a slight rightward bisection on visual line bisection; a pattern also reported by Fujii et al. (1995) who found that older participants bisected lines significantly towards the right relative to middle-aged and younger participants. Schmitz and Peigneux (2011) explored the effect of age on pseudoneglect

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by asking participants aged 22 years or 69 years to perform a Landmark task with 100 visually presented pre-bisected lines; the results showed that, while younger participants produced the typical leftward biases, older adults showed a significantly reduced left bias which was more in line with the bias shown by neglect patients when compared against the younger participants (see also Schmitz et al. 2013). Such observations do represent a difficulty for the HAROLD interpretation, as although it predicts an ageing-related decrease in left bias, there is no reason to expect an increase in rightward deviations past the veridical midline. One explanation may be that the recruitment of the two hemispheres may be notably asymmetrical during simple motor tasks but that there is more bilateral recruitment when the task is more complex in general (Hausmann et al. 2004). It is also important to refer to a number of studies that support neither the right-hemiaging nor the HAROLD model of cognitive ageing and that have not suggested symmetrical biases in children or adults across lifespan. De Agostini et al. (1999) compared visuospatial bisection in participants aged 5 to 6 years, adults aged 20 to 45 years, and older adults 60 to 94 years and found leftward bisection error regardless of age, gender, or response hand. Varnava and Halligan (2007) conducted visuospatial line bisection with participants aged 14– 20, 21–30, 31–40, 41–50, 51–60, 61–70, 71–80 years; across all age groups participants showed leftward biases regardless of line length, age group or sex. It is also useful to explore the performance of agematched controls on visuospatial line bisection in unilateral left neglect studies. Participants aged 66 years showed leftward errors on both visuospatial bisection and a Landmark task (Harvey et al. 1995); age-matched controls aged 76 years (on average) showed leftward biases on an emotional judgement chimeric faces task - in line with younger participants (Coolican et al. 2008); control participants aged 75 years showed a leftward bias on the visuospatial Greyscales task (Mattingley et al. 2004); control participants aged 50 to 76 years showed slight leftward biases on a visuospatial task (Schindler et al. 2006). In these cases, for older participants especially, it is difficult to accept that there is a balanced activation of the cerebral hemispheres when pseudoneglect has consistently been shown in a variety of different studies using different methodologies and across a variety of different age groups. Furthermore, precisely because of these differences it is also difficult to accept a right hemisphere orienting account of pseudoneglect in these older populations. We would encourage an expanded future research effort to further explore how age impacts the magnitude of pseudoneglect in order to build a stronger and more complete understanding of this aspect of spatial attention, an enterprise that seems particularly timely given the potential impacts on independent living.

Conclusions The aim of this review was to critically appraise research on representational forms of pseudoneglect, discuss whether or not attentional orienting underlies the bias, and consider the factors that drive and mediate the bias. To this end, representational forms of pseudoneglect are clearly distinct from visual forms of pseudoneglect, occurring in the complete absence of direct visuospatial processing across a range of different tasks. Our understanding of visuospatial pseudoneglect has greatly increased over the past 30 years—we now know much about how visuospatial pseudoneglect is mediated, enhanced and attenuated through a huge number of studies conducted in the field. We argue that representational pseudoneglect should be afforded the same dedication. Within this review, empirical observations of representational pseudoneglect have been presented to show that the phenomenon occurs under a wide variety of conditions. We have shown that representational forms of pseudoneglect are observed when (1) a person is asked to mentally represent a previously seen or novel stimulus, (2) when a person explores a stimulus using touch alone, or (3) when a person activates the mental number line. Furthermore, though patterns of response with regard to representations of number largely mirror visual pseudoneglect patterns, the parameters of touch exploration and mental representation are less directly analogous to perceptual pseudoneglect. There is also clear evidence of a different pattern of relationship between visual-perceptual and representational pseudoneglect with regard to ageing—specifically that representational pseudoneglect biases do not seem to diminish with age in an analogous manner to visualperceptual biases. The body of evidence on representational pseudoneglect is best explained by an activation-orientation account of representational pseudoneglect, which is based on the left side of a mental representation being more salient compared to the right. While we argue that the activation-orientation hypothesis for representational pseudoneglect clearly holds under direct scrutiny, we acknowledge that there are outstanding questions about the extent to which it can account for the representational phenomenon. We have outlined several directions for future research throughout this review, but perhaps the most important question is why does representational pseudoneglect exist at all? In order to start answering this question, the challenge would be to explore representational pseudoneglect in real-world settings. It has been shown that, under certain conditions, healthy participants tend to bump into things more often on the right more than the left (Nicholls et al. 2007) and that bumping behaviour may be related to visuospatial line bisection performance (Nicholls et al. 2008c; see also Hatin et al. 2012). Relatedly, an interaction between visuospatial pseudoneglect, age and memory has been suggested (Schmitz et al. 2013).

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The challenge would be to explore the same real world applications for representational pseudoneglect. Overall, research to-date provides for the possibly that certain right hemisphere functions remain asymmetrical in older age, and this has theoretical implications for models of lateralisation in cognitive ageing. Acknowledgments This research was supported by a Ph.D. studentship from The Universita’ Suor Orsola Benincasa awarded to JB.

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