Investigating the spatial and temporal modulation of visuotactile interactions

in older adults

Samuel Couth a, Emma Gowen b, Ellen Poliakoff a a School of Psychological Science, University of Manchester, Zochonis building, Manchester M13 9PL, United Kingdom b Faculty of Life Sciences, University of Manchester, Carys Bannister Building, Dover Street, Manchester M13 9PL, United Kingdom

Corresponding author: Samuel Couth Tel: 0161 306 0470 Email: [email protected]

Abstract

Previous research has shown that spatially and temporally disparate multisensory events are more likely to interact for older adults. For visuotactile interactions, this suggests that the representation of peripersonal space is expanded and temporal perception within this space is less precise. Previously, visuotactile space has been found to expand horizontally into the opposite hemispace and here we seek to replicate and extend this by exploring both horizontal and vertical space from the hand. Moreover, we investigate whether both spatial and temporal domains are affected for an individual, which have previously been measured using distinct tasks and different participants. We presented a modified crossmodal congruency task (Poole et al. 2015a) to thirty older participants (age range = 65-85 years), with unisensory tactile performance equated for each individual. For the temporal manipulation, the timings of visual distractors and tactile targets were offset. For the spatial manipulation, visual distractors were presented from multiple positions in ipsilateral and contralateral hemispaces. Whilst the temporal modulation of visuotactile interactions for older adults was equivalent to that observed in young adults, spatial modulation was reduced; significant visuotactile interactions were observed for visual distractors presented in the same and opposite hemispace to the stimulated hand, in the lower visual field. This suggests an expanded representation of visuotactile space surrounding the hand in older adults, which occurs horizontally into the contralateral hemispace only, rather than expanding both vertically and horizontally. This is likely to have consequences for perception of space and goal-directed action in ageing.

Keywords: Ageing, multisensory processing, visuotactile interactions, peripersonal space, spatial, temporal

Introduction

With an ever increasing lifespan, the detrimental health effects of old age, including sensory, cognitive and motor decline, are becoming ever more relevant (Baltes and Lindenberger

1997). Age-related anatomical and physiological alterations to the central nervous system have been identified. For instance, there is evidence to suggest reduced overall weight and volume, increased ventricle growth, decreased length and number of neurons, and decreased myelination of axon bodies, with prefrontal cortices significantly more affected than any other region (for an extensive review see Raz and Rodrigue 2006). This may underlie many of the cognitive deficits seen in old age, such as processing speed, primary working memory, and reasoning (Cerella 1985; Verhaeghen and Salthouse 1997; Salthouse 2000; O’Sullivan et

2 al. 2001), as well as declines in attention and inhibition (Hasher and Zacks 1988; Hasher et al. 1991; Zeef et al. 1996; Fabiani 2012). Altered central nervous system processing and age- related changes to sensory organs may also underpin the decline in unisensory processing observed in older persons (Nusbaum 1999). In addition, reduced white matter connectivity with increasing age could underlie altered multisensory processing (Sullivan et al. 2001), whereby information received in the different sensory modalities (i.e. vision, touch and hearing) is brought together to create a more holistic percept of the environment (see Stein and Meredith 1993). Alterations to this process could lead to a less robust percept in older adults, and could impact on motor behaviours such as balance maintenance (Mahoney et al.

2014a; Stapleton et al. 2014) and limb coordination (e.g. Chaput and Proteau 1996).

Therefore, it is important to understand how ageing affects multisensory processing, and the implications for developing technology, therapeutic aids and interventions.

Multisensory processing is usually an efficient process, such that distinct sources of sensory information are perceived as a single multisensory event providing that they occur at approximately the same time and same location within our environment (known as the temporal and spatial rules, respectively; see Stein and Meredith 1993). This ensures a coherent representation of our surroundings, as well as our internal body state, and is pivotal to coordinating behaviour. For instance, the position and timing of arm and hand movements is reliant on an accurate 3-D representation of near body (peripersonal) space based on the interaction between visual, tactile and proprioceptive feedback (Maravita et al. 2003; Spence et al. 2004b; Holmes and Spence 2004; Sambo and Forster 2009). This has multiple purposes, such as ensuring accurate movements towards target objects and avoiding collisions with obstacles in the reach path, as well as protection from potentially threatening stimuli in near space (Holmes and Spence 2004; Brozzoli et al. 2010; Brozzoli et al. 2014; de Haan et al.

2014; de Vignemont and Iannetti 2014). Therefore, altered multisensory processing could

3 disrupt the representation of extrapersonal and peripersonal space (Fujii et al. 1995; Ghafouri and Lestienne 2000; Poliakoff et al. 2006a; Lepelley et al. 2010; Bloesch et al. 2013), leading to poorer upper-limb coordination in older adults (e.g. Chaput and Proteau 1996; Ketcham et al. 2002; Carmeli et al. 2003). The overall purpose of this study is to further our understanding of how ageing affects the spatial and temporal constraints on visuotactile interactions.

A common method for measuring the representation of visuotactile space is the crossmodal congruency task (CCT; Spence et al. 1998; Spence et al. 2004a). The original version of this task involves participants making speeded judgements regarding the elevation of tactile vibrations presented to either hand (upper vibration, index finger; lower vibration, thumb), whilst ignoring concurrent visual flashes presented next to the finger or thumb. The visual and tactile stimuli are presented at the same (congruent), or different (incongruent) elevations. Typically, younger participants show a congruency effect (CE), performing more rapidly and accurately in the congruent condition, and producing more errors and longer reaction times (RTs) in the incongruent condition. It is consistently reported that distractors presented close to the participant’s stimulated hand produce a greater effect than if they are presented near the opposite hand, i.e. visuotactile interactions (CEs) are spatially modulated

(see Maravita et al. 2003; Poole et al. 2015a). That is, visual information which occurs within the participant’s peripersonal space, surrounding the stimulated hand, is more likely to influence judgements of concurrent tactile stimulation.

Two previous studies investigating the spatial limits of visuotactile interactions in older adults have shown that interactions occur over greater distances, suggesting an expanded representation of visuotactile space with advancing age. Using the CCT, Poliakoff and colleagues (2006a) showed that older adults did not exhibit spatial modulation, instead showing significant visuotactile interactions irrespective of whether visual distractors were

4 presented close to the stimulated hand or by the unstimulated hand, in the contralateral hemispace. In a more recent RT study, Mahoney and colleagues (2014b) showed that older adults produced equivalent response times regardless of whether the two stimuli were presented in the same or opposite hemispace. However, in both studies, only two visual distractor locations were tested, near and far from the stimulated hand across hemispaces.

Therefore it is not known whether visuotactile space would also expand vertically within the same (ipsilateral) hemispace. Alternatively, the expanded representation of visuotactile space may occur horizontally across hemispaces exclusively. By understanding how visuotactile interactions might vary within and across hemispaces for older adults, it may be possible to develop new techniques for improving goal-directed movements.

To explore how visuotactile interactions vary across locations, we recently designed a modified unimanual version of the CCT in which visual distractors are presented at multiple locations; next to the participant’s stimulated hand, at an equivalent position in the contralateral hemispace, and 21cm and 42cm vertically from the participant’s stimulated hand within the same (ipsilateral) hemispace (Poole et al. 2015a). This modified design has been shown to effectively capture group differences in the representation of visuotactile space, where young adults with autism spectrum conditions showed an expanded representation of visuotactile space contralaterally (Poole et al. 2015b), whereas neurotypical younger adults only showed visuotactile interactions for distractors presented close to the stimulated hand

(Poole et al. 2015a; b). In the current investigation, we used this same experimental design with older adults. We predicted that distractors presented next to the stimulated hand would have a stronger influence on tactile judgements compared to distractors presented further away, although significant visuotactile interactions might be observed for disparate distractors for older adults (Poliakoff et al. 2006a; Mahoney et al. 2014b). If significant visuotactile interactions were observed for both the contralateral and the furthest ipsilateral

5 distractor positions (both separated from the tactile target by 42cm), this would imply that the expanded representation of visuotactile space spans regions both within and across hemispaces (i.e. vertically and horizontally). Conversely, if a significant visuotactile interaction was observed for the contralateral distractor, but not the furthest ipsilateral, this would imply an expansion of visuotactile space exclusively in the lower visual field and across hemifields (i.e. horizontally; as demonstrated by Poliakoff et al. 2006a). Studies have previously shown that spatial encoding is poorer for the transverse (left-right horizontally across hemispaces) plane for both younger and older adults, and older adults demonstrated worse spatial encoding for all planes (coronal, sagittal and transverse; Ghafouri and Lestienne

2000; Lepelley et al. 2010). In line with this, we predicted that the expanded representation of visuotactile space in older adults would be more evident horizontally across hemispaces, rather than within the same hemispace, since poorer spatial representation in this direction is exacerbated by ageing.

In addition to changes in spatial processing, the temporal processing of multisensory events has also been shown to vary with age. Older adults have been found to be poorer at determining the temporal order of audiovisual pairings (Virsu et al. 2003) and visuotactile pairings (Poliakoff et al. 2006b). That is, older adults required a greater temporal offset in order to tell which of two sensory modalities was presented first. Setti and colleagues (2011a) have also demonstrated that older adults show an increased susceptibility to the flash-beep illusion than younger adults. Specifically, when a single flash was presented with two beeps, older adults were more likely to report seeing two flashes, even when the visual and auditory inputs were separated by 270ms. Along with electrophysiological evidence (Golob et al.

2001; Setti et al. 2011b), these studies suggest that temporal modulation may also be reduced in older adults. Accordingly, temporally disparate sensory inputs may be processed as a

6 common multisensory event by older adults, which would otherwise be perceived as two distinct events by younger adults.

Overall, it appears that multisensory interactions occur across greater spatial and temporal discrepancies for older adults. Ultimately, this could lead to a less robust percept as irrelevant multisensory cues (i.e. spatially and temporally disparate) are more likely to interact

(Poliakoff et al. 2006a; Mozolic et al. 2012), which has been implicated in fall behaviour in older adults (Setti et al. 2011a; Stapleton et al. 2014; Setti et al. 2014; Merriman et al. 2015).

Interestingly, however, temporal and spatial modulation of multisensory interactions has previously been measured using distinct experimental paradigms and different participants.

Consequently, it is difficult to determine whether both of these processes might be affected for an individual, and thus might reflect a general age-related detriment to multisensory processing across a number of domains (Laurienti et al. 2006; Peiffer et al. 2007; Mahoney et al. 2011). To explore this issue, we manipulated both the spatial location and temporal offset of visual distractors in the current study. The temporal modulation of visuotactile interactions was investigated by manipulating the temporal discrepancy between the target vibration and distractor light (Shore et al. 2006), while always presenting the distractor at a single spatial location next to the stimulated hand. Importantly, the task demands remain the same for both spatial and temporal manipulations, thus it is possible to determine how both spatial and temporal domains are affected for individual participants. Given evidence suggesting a larger temporal binding window in older adults, it was expected that visuotactile interactions would extend to later temporal asynchronies between the target and distractor (Poliakoff et al.

2006b; Diederich et al. 2008; Setti et al. 2011a; Setti et al. 2011b).

The design of the current study also allows us to rule out a number of alternative explanations for altered visuotactile processing in older adults. First, spatial modulation may not have been captured in previous studies due to the positioning of the near and far distractors. In the study

7 by Mahoney and colleagues (2014b), the near ipsilateral visual distractor may not have been within peripersonal space of the stimulated hand (i.e. separated by 49°), which may have reduced the potential to observe spatial modulation between distractor locations. Therefore we used a near distractor location as close as possible to the stimulated hand, so that interactions for distant distractors could be measured relative to when visual and tactile stimuli were spatially aligned. In the study by Poliakoff and colleagues (2006b), the distant visual distractor was presented by the unstimulated hand; thus the contralateral visual distractor may have been incorporated into the peripersonal space surrounding the unstimulated hand, which could have influenced tactile judgements (Poole et al. 2015a). The fact that our modified version of the CCT is a unimanual task means that we can be confident that visuotactile interactions for more distant distractors (42cm away) could not be attributed to proximity to the unstimulated hand.

Second, it is possible that ageing might affect how clearly visual distractors at the different locations can be perceived, and thus may have a differential influence on tactile judgements.

Therefore, we include an additional visual only condition at the end of the experiment to check whether there was a significant difference between distractor locations.

Third, there may be some variability in unisensory tactile performance both within (Poole et al. 2015a) and between different age (or clinical; Poole et al. 2015b) groups. If a participant reaches ceiling or floor performance in a single sensory modality, introducing a different sensory modality may have no effect (Holmes 2009a; Holmes 2009b). In turn, this could mask age-related differences in multisensory processing. Therefore, our modified task includes a threshold procedure prior to the main experiment which is designed to equate unisensory tactile performance across all individuals. In previous studies using the CCT, the elevation judgement is suprathreshold and error rate is low. As such, the CE is typically observed in RTs, and not always in error data (Spence and Walton 2005). Thus, by presenting

8 the experimental stimuli at the participant’s approximate threshold level, a higher error rate is produced, and so multisensory interactions can be reliably measured through error rate alone.

It may be advantageous to analyse error data in older adults rather than RTs, since older adults exhibit more within- and between- participant variability in motor tasks (Fozard et al.

1994; Shammi et al. 1998; MacDonald et al. 2006).

Finally, it is possible that age-related enhancements in multisensory interactions could be due to a general age-related decline in attention and inhibition (Hasher and Zacks 1988; Hasher et al. 1991; Zeef et al. 1996; Fabiani 2012). Indeed, a general decline in inhibition might mean that older adults are less able to suppress the processing of distractors, irrespective of spatial and temporal discrepancies. Alternatively, reduced capacity to sustain attention might more generally affect older adults’ ability to stay focused on the task. To test these possibilities, we compared performance on the modified CCT to measures of attention using the Sustained

Attention to Response Task (SART; Robertson et al. 1997) and to measures of inhibition using the Stroop task (MacLeod 1991). If there is no relationship between these measures this would suggest that ageing produces a specific detriment to multisensory processing, such as selective attention for a particular sensory modality.

Method

Participants

Thirty older adults (16 female; mean age = 73.2 ± 6.1 years) were recruited via local community groups, newspapers and webpages. All participants were screened for dementia using the Addenbrooke’s Cognitive Examination – Revised (ACE-R; mean score = 95.0 ±

4.5) and depression using the Geriatric Depression Scale – Short Form (GDS – SF; mean score = .7 ± .8). All participants demonstrated better than 6/12 (20/40) monocular visual acuity for both eyes (with or without correction) as assessed by the Snellen letter chart,

9 indicating good acuity for all participants (Falkenstein et al. 2008; Kaiser 2009). Hand dominance was assessed using the Edinburgh Handedness Inventory (EHI; Oldfield 1971; right handed, n = 27). The risk of having a fall was assessed using the Berg Balance Scale

(BBS; Berg 1989), with all participants deemed as at low risk (BBS score > 40/56; average score = 53.5 ± .4 SEM). Participants received a small monetary reimbursement for taking part in this study. The study was approved by the University of Manchester Research Ethics

Committee in accordance with the Declaration of Helsinki, and written informed consent was obtained before participation.

Stimuli and apparatus

Participants sat at a desk in a dimly lit room and were instructed to focus on a central fixation point, consisting of a white cross (19mm) on a computer monitor, displayed approximately at eye level and 45cm from the participant. A mirror was angled above the participant that allowed the experimenter to ensure that central fixation was maintained.

A bone conductor (Oticon Limited, B/C 2-PIN, 100Ω, Hamilton, UK) was embedded within a 70 x 70 x 70mm foam cube. Participants held the cube between the thumb and forefinger of their dominant hand such that only the pad of the index finger was in contact with the bone conductor. The participant’s index finger was attached to the bone conductor using double- sided adhesive tape. The bone conductor was driven by sound files (white noise, ~66dB SPL) from a PC through a Tacamp amplifier (Dancer Design, St. Helens UK) and was perceived as a tactile vibration. Six 10mm red LEDs, were affixed in symmetrical locations around the monitor. The LEDs were visible through 10mm holes in a black cardboard shield which surrounded the monitor. Each light was 29cm from the fixation cross (~33° viewing angle): one light positioned above the bone conductor, one light 21cm above the conductor offset at an angle of 10˚, and one light 42cm directly above the bone conductor. Three lights were

10 fixed in symmetrical positions on the opposite side of the monitor, allowing equivalent positioning for left handed participants (Fig. 1a).

White noise was played through headphones throughout the experiment to prevent the participant from hearing sounds emitted by the bone conductor (~75dB SPL). Throughout the experiment, the participant’s dominant foot rested with their heel and toe each depressing a foot pedal. Responses were recorded by them lifting their heel or toe.

Threshold procedure

Participants received two successive tactile stimuli in a two-interval forced choice (2-IFC) procedure; a constant (single) vibration and two separate (double) 80ms vibrations separated by a 0-200ms gap. Participants were instructed to indicate which interval contained the double vibration by using the foot pedals; a toe lift if presented in the first interval, a heel lift if presented in the second interval. An adaptive staircase procedure (PEST; Taylor and

Creelman 1967) was used to reduce the temporal offset between double vibrations until participants were able to distinguish single from double vibrations on 75% (±10%) of trials.

This temporal offset (ms) was taken as an individual’s tactile threshold and was used in the main experimental procedures (for further details, see Poole et al. 2015a).

Experimental Procedure

Participants were asked to make speeded responses following each target vibration, responding by lifting their toe in response to single vibrations, and heel in response to double vibrations. Throughout the experimental procedure, vibrations were presented at the previously determined threshold level for that participant. The task included both baseline

(unisensory tactile) trials and trials with task irrelevant distracting LED light flashes, which were either congruent (e.g. single vibration, single light flash) or incongruent (e.g. single vibration, double light flash; Fig. 1b). Participants were explicitly instructed to ignore the

11 light flashes as much as possible. A central fixation cross remained onscreen throughout the session.

In each trial, a larger, silver version of the cross (24mm) appeared for 750ms to warn participants that the trial was about to commence. The white cross then reappeared 750ms before the onset of the target stimulus and remained onscreen while the stimulus was delivered. Distracting light flashes were presented close in time to the target (see below). For single flashes the LED was illuminated for 80ms, while double flashes comprised two single

80ms flashes separated by 120ms. Trials ended when participants made a response, followed by an inter-trial interval of 1500ms (see Fig. 1c for typical trial design). Both accuracy and speed were emphasised prior to conducting trials.

Participants completed three practice blocks before the main procedure to familiarise them with the task and ensure that the threshold procedure had worked effectively.

For the temporal manipulation, the distractor lights were always presented by the participant’s stimulated hand. There were 9 conditions: distractors (congruent, incongruent) x

SOA (-30ms, 100ms, 200ms and 400ms; Fig. 1c), plus baseline (unisensory tactile). Note that distractors are typically presented 30ms prior to the target stimulus (−30ms), rather than as objectively simultaneous (0ms), as this produces the greatest CE in studies of the CCT (see

Spence et al. 2004a). For the spatial manipulation, the distractor lights were always presented at -30ms SOA. There were 9 conditions: distractors (congruent, incongruent) x position (0cm,

21cm, 42cm, 42cm on the opposite side, referred to herein as 42cm_opp; Fig. 1a) plus baseline trials. For both spatial and temporal manipulations, distractor and baseline unisensory trials were intermixed. Each manipulation consisted of four experimental blocks of 90 trials, in which each condition was presented 10 times in a randomised order, with half of these trials being single vibrations and half double. This gave 360 trials per manipulation

(720 in total), with 40 trials in each condition. An enforced break was included after each

12 block and both manipulations (plus the threshold procedure) were completed in a single two hour session.

At the end of the testing session, participants performed a light only control condition consisting of 40 trials in which no vibrations were presented and participants were instead instructed to report the number of light flashes, presented from the 4 different locations (5 single flashes and 5 double flashes per position). This task was conducted to confirm that participants were able to discriminate the single/double lights (i.e. they were suprathreshold) across all spatial locations. Participants performed this task under the same conditions as the main procedure with their dominant hand holding the foam cube. Participants were also instructed to maintain their gaze on the central fixation throughout so that lights were detected in the periphery.

[Figure 1. about here]

13 Sustained attention to response task (SART)

All participants completed the SART (Robertson et al. 1997) as a general measure of sustained attention over a prolonged period. Participants were instructed to press a single button in response to numbers presented on screen in rapid succession. The number stimuli, from 1 to 9, varied in font size: 48, 72, 94, 100 and 120 points. Participants were told to withhold a response if number ‘3’ was presented. Numbers were presented in a pseudo- randomised sequence that followed set rules: no more than two targets of the same number or size were presented in succession; targets of a particular size and number was presented no more than once per 45 trials; the presentation of five sizes of each target were never in ascending (small-large) or descending (large-small) order; there were never more than two target numbers in ascending (1 to 9) or descending (9 to 1) order; the target number preceding a '3' was never used more than three times. Participants were instructed to respond as quickly and accurately as possible. Commission errors (i.e. incorrectly pressing on ‘3’) were measured and converted into correct no-go accuracy (%).

Stroop task

Participants also completed the Stroop test (MacLeod 1991) as a measure of inhibition capabilities. Participants were presented with 3 cards. Card 1 required participants to name 50 colour patches (red, blue, green) as quickly and accurately as possible. Card 2 required participants to read aloud 50 colour words (red, blue, green) presented in black print as quickly as possible. Card 3 (classic Stroop test) required participants to name the colour of the ink of 50 colour words (red, blue, green) which were always incongruent (e.g. the word

“RED”, written in blue ink). Participants were instructed to perform this task as quickly and accurately as possible. Completion time (seconds) for each card was used to calculate an interference score:

14 Data analysis

Results analysis for the spatial and temporal manipulations were considered separately.

Unforced error analysis

Trials where responses were less than 150ms (anticipatory) or longer than 2000ms (late) were initially removed from analysis. These errors were likely caused by lapses in attention, anticipation of the target, or foot pedal errors, and were thus determined as ‘unforced errors’.

The overall unforced error rate was low for both spatial (1.40%) and temporal (1.65%) manipulations, and so no further analysis was conducted.

Forced error analysis

Of the remaining data, errors induced by the experimental design (i.e. ‘forced errors’) were calculated for each condition. Although error rate was the main focus, mean RTs have also been included for completeness (Table 1). Participants whose unisensory baseline performance fell outside 60-90% accuracy on the main procedure (for spatial and temporal manipulations separately) were not included in the analysis, since this would signify that performance had not been successfully constrained. For the remaining participants, Pearson’s correlation analysis was conducted between average threshold scores and unisensory baseline performance. If task difficulty was correctly set for these individuals then there should be no relationship between these measures, and so there was equal opportunity for visual distractors to influence tactile processing for each participant.

A 2 x 4 (Congruency x Condition; 4 positions/SOAs) repeated measures ANOVA was used to compare error rates across conditions. Pairwise comparisons were used to analyse main effects. Significant interactions were analysed by first calculating the CE (i.e. incongruent

15 error rate – congruent error rate) for each participant in each condition (position/SOA), before comparing the mean CE in each condition to zero using one-sample t-tests, and comparing the mean CE between conditions using paired-samples t-tests. Baseline performance was compared to congruent/incongruent conditions by subtracting each participant’s baseline error rate from congruent and incongruent error rates at each position/SOA. One-sample t- tests were conducted on the mean difference to determine whether congruent/incongruent light flashes had caused significant facilitation/interference of responses at each position/SOA. Paired-samples t-tests were then performed on the mean difference between each position/SOA for congruent and incongruent conditions separately.

Bonferroni corrections were applied where appropriate. Greenhouse-Geisser corrections were applied if the assumption of sphericity was violated.

Results

[Table 1. about here]

Spatial manipulation

Baseline unisensory performance was successfully constrained for 26 participants (mean baseline accuracy = 76.9% ± 1.9 SEM). The average threshold for detecting double tactile vibrations was 39.5ms ± 2.7 (SEM) and ranged from 24 to 85ms. Pearson’s correlations between tactile thresholds and baseline scores were not significant [r = .189, n = 26, p = .

354], suggesting that task difficulty had been set at approximately the correct level for each participant.

16 The repeated measures ANOVA revealed a main effect of position [F (1.723, 60.055) =

20.045, p < .001, η2 = .445]. Pairwise comparisons revealed that the percentage of errors produced by the distractor positioned at 0cm (28.6%) was significantly greater than those at

21cm (26.9%) (p = .002), and 42cm (24.8%) (p = .001), but was not significantly different to the 42cm_opp distractor (26.8%) (p > .05). There was no significant difference in error rate between distractor positions 21cm and 42cm (p > .05), but the error rate for the 42cm_opp distractor position was significantly greater than both 21cm and 42cm distractor positions

(both p < .001) (Fig. 2a). There was also a main effect of congruency [F (1, 25) = 4.780, p = .

038, η2 = .161] showing that more errors were produced for incongruent (32.2%) than congruent (21.4%) distractors (i.e. a positive CE). The crucial position x congruency interaction was also significant [F (2.402, 60.055) = 4.990, p = .007, η2 = .166] (Fig. 2b).

One-sample t-tests showed significant CEs for distractors positioned at 0cm, 21cm and

42cm_opp, but not for the 42cm distractor (Table 2). Paired samples t-tests revealed that CEs were significantly greater for distractors at 42cm_opp compared to 42cm [t (25) = 3.045, p = .

005) and borderline significantly greater for 0cm compared to 42cm [t (25) = 2.840, p = .009;

Bonferroni correction p < .008], indicating that some spatial modulation had occurred. There were no other significant differences in CEs between distractor positions (all p > .008).

Comparing baseline performance to all conditions showed no significant facilitation/interference effects for congruent distractors (all p > .006, Bonferroni correction), however significant interference effects were observed for incongruent distractors at 0cm,

21cm and 42cm_opp positions, but not for the distractor placed at 42cm within the same hemispace (Table 3, Fig. 2c). Paired samples t-tests between congruent conditions at each position showed no significant differences (all p > .008, Bonferroni correction). Conversely, interference effects for incongruent distractors at 0cm were significantly greater than at 42cm

[t (25) = 3.327, p = .003], and significantly greater for incongruent distractors at 42cm_opp

17 than at 42cm distractors [t (25) = 2.936, p = .007]. There were no other significant differences in interference effects between distractor positions (all p > .008, Bonferroni correction).

Temporal manipulation

Baseline unisensory performance was successfully constrained for 26 participants (mean baseline accuracy = 77.6% ± 1.5 SEM). The average threshold for detecting double tactile vibrations was 39.7ms ± 2.9 (SEM) and ranged from 22 to 90ms. Pearson’s correlations between tactile thresholds and baseline scores were not significant [r = -.213, n = 26, p = .

296], suggesting that task difficulty had been set at approximately the correct level for each participant.

The repeated measures ANOVA revealed a main effect of SOA [F (3, 75) = 3.058, p = .033,

η2 = .109]. Pairwise comparisons indicated a significantly greater number of errors for distractors following the -30ms SOA (28.3%) compared to the 400ms SOA (23.5%) only (p

= .018). There were no other significant differences in error rate between SOAs (all p > .05).

There was also a main effect of congruency [F (1, 25) = 4.807, p = .038, η2 = .161], indicating an overall higher error rate in incongruent (26.7%) compared to congruent (23.6%) conditions (Fig. 2d). The crucial SOA x congruency interaction was also significant [F (3,

75) = 7.319, p < .001, η2 = .226]. One-sample t-tests revealed significant CEs for distractors at the -30ms SOA and approaching significance at the 100ms SOA, but not for any other

SOA (Table 2). Paired samples t-tests also showed that CEs at the -30ms SOA were significantly greater than at the 400ms SOA [t (25) = 3.079, p = .005] and borderline significantly greater compared to the 200ms SOA [t (25) = 2.848, p = .009; Bonferroni correction p < .008], indicating that temporal modulation had occurred (Fig. 2e). There were no other significant differences in CEs between SOAs (all p > .008, Bonferroni correction).

Comparing baseline performance to all conditions showed no significant difference between baseline and congruent conditions at any SOA (all p > .006, Bonferroni correction), however

18 significant interference effects were observed for incongruent distractors at -30ms SOA only

(Table 3). Paired samples t-tests between congruent conditions at each SOA showed no significant differences (all p > .008, Bonferroni correction). However, there were significantly greater interference effects for incongruent distractors at the -30ms SOA compared to 200ms [t (25) = 3.684, p = .001] and 400ms [t (25) = 3.236, p = .003] SOAs

(Fig. 2f). There were no other significant differences in interference effects between distractor SOAs (all p > .008, Bonferroni correction).

[Table 2. about here]

[Table 3. about here]

19 [Figure 2. about here]

Light only control condition

For participants who were included in the spatial manipulation analysis (n = 26), the overall accuracy for detecting single/double light flashes was high (mean accuracy = 87.9% ± 2.6,

SEM). A repeated measures ANOVA revealed a main effect of light position [F (3, 75) =

3.542, p = .019, η2 = .124], with reduced accuracy when lights were presented at 42cm_opp

(83.5%) compared to 21cm (91.4%) (p = .043). Other light positions did not significantly differ (all p > .05).

20 Correlation analysis between CEs

To determine whether the magnitude of visuotactile interactions for spatially and temporally coincident stimuli (0cm and -30ms) was related to the magnitude of interactions for spatially and temporally disparate stimuli, Pearson’s correlations were conducted between the coincident CE (0cm and -30ms) and each distractor position (21cm, 42cm and 42cm_opp) and SOA (100ms, 200ms and 400ms) separately.

For the participants included in both spatial and temporal analyses (n = 23), there was a very strong correlation between CEs for the 0cm and -30ms condition [r = .804, n = 23, p < .001]

(Fig. 3a). This is to be expected, since these conditions are identical across the two different manipulations (spatial and temporal). As such, these conditions were averaged and then compared to CEs for the remaining distractor positions (21cm, 42cm and 42cm_opp) and distractor SOAs (100ms, 200ms and 400ms) separately. Strong correlations were observed between CEs for the averaged 0cm/-30ms distractor condition and the 21cm distractor position [r = .584, n = 23, p = .003] (Fig. 3b) and the 42cm_opp distractor position [r = .627, n = 23, p < .001] (Fig. 3d), but not the ipsilateral 42cm distractor [r = .178, n = 23, p = .001].

This demonstrates that the magnitude of visuotactile interactions for spatially coincident stimuli (0cm) was related to the magnitude of visuotactile interactions for the contralateral distractor (42cm_opp) and the distractor immediately above the hand (21cm), i.e. the positions where a significant CE was observed (Fig. 3c). There were no significant correlations between CEs for the averaged 0cm/-30ms distractor condition and any SOA (all p > 0.05).

Since there was a strong CE observed for the 42cm_opp distractor, further exploratory correlations were performed between the CE for this position and the remaining SOAs

(100ms, 200ms and 400ms) to determine whether there was a relationship between the magnitude of visuotactile interactions at this position and other temporal offsets. A

21 significant positive correlation was observed for the 400ms SOA [r = .445, n = 23, p = .033] and approaching significance for the 200ms SOA [r = .371, n = 23, p = .082], but not for the

100ms SOA [r = .248, n = 23, p = .254]. This analysis was also repeated for the smaller CE observed for the 21cm distractor, but no correlations were observed (all p > .05).

[Figure 3. about here]

Stroop and SART scores and CEs

Given the large visuotactile interaction for the 42cm_opp distractor, hierarchical regression analyses were performed with the CE for the 42cm_opp distractor as the dependent variable

(Table. 4; n = 26). In model 1 (unadjusted model), neither SART no-go accuracy (mean =

75.23% ± 18.9 SD) nor Stroop interference scores (mean = 50.10 ± 17.7 SD) were significant predictors of CEs at this location (both p > .05). Additional covariates were entered in a stepwise manner. In model 2, age and gender were added as independent variables. In step 3, tactile threshold (ms) was added as an independent variable. SART and Stroop scores were still not significant predictors of CEs at the 42cm_opp location, even when accounting for these covariates (all p > .05).

22 [Table 4. about here]

Discussion

The aim of the current experiment was to use a modified version of the CCT to further explore how the spatial and temporal modulation of visuotactile interactions is affected in older adults. Extending previous studies, the current methodology allowed multiple visual distractor locations to be used. Furthermore, unisensory tactile performance was constrained at the individual level so that task difficulty could be equated across participants. The results indicated that spatial and temporal modulation of visuotactile interactions did occur, although the degree of spatial modulation was reduced for older adults, compared to previous findings in young participants (Poole et al. 2015a). These findings are unlikely to be due to alterations in the general ability to sustain attention (SART) or to inhibit processing (Stroop task), since distractor effects were not significantly predicted by these measures, despite considerable between participant variability.

First focusing on the spatial findings, it has been observed previously that the visual distractor positioned 21cm vertically from the stimulated hand (ipsilateral hemispace) did not produce a significant CE with younger participants (Poole et al. 2015a). However, the authors predicted that there might be some distraction from this location since the stimulus was positioned within peripersonal space (~30cm; Lloyd 2007). In line with this, the current

23 findings show a significant CE for older adults for the 21cm distractor and the size of this effect correlated positively with the spatially coincident (0cm) distractor (Fig. 3b). It is possible that a general enhancement in visuotactile processing by the older adults meant that interactions were stronger at the 21cm location, despite the spatial separation between the target and distractor (Mahoney et al. 2011).

For the more disparate spatial distractors (42cm vertically, and 42cm contralaterally), these were positioned beyond the normal limits of peripersonal space (Lloyd 2007). Thus, significant CEs at these locations would suggest an expanded representation of visuotactile space. For younger adults, visuotactile interactions were observed for spatially coincident

(0cm CE = ~20%) distractors, but not the more disparate distractors (42cm_opp CE = ~7%;

Poole et al. 2015a), which is the typical pattern seen in the original version of the CCT (e.g.

Maravita et al. 2003), and also supported by electrophysiological evidence (Sambo and

Forster 2009). In the current study, CEs for the 42cm_opp distractor (42cm_opp CE = ~15%) were comparable to when distractors were spatially coincident (0cm CE = ~13%) for older adults, similar to previous research using the original version of the CCT (Poliakoff et al.

2006a). In other words, older adults were more affected than young adults by visual distractors which are presented in an equivalent position to the tactile target, but in the contralateral hemispace. This could suggest an expanded representation of visuotactile space for older adults (Poliakoff et al. 2006a; Mahoney et al. 2014b). Nevertheless, the older group showed a reduction in the effect of visual distractors displaced by 42cm vertically within the ipsilateral hemispace, suggesting it is not simply absolute distance between the tactile target and visual distractor which determines whether visuotactile interactions take place for older adults. That is, it is not a general expansion of peripersonal hand space within and across hemispaces (Mahoney et al. 2014b). Rather, the spatial location of the distractor appears to cause this effect, with the contralateral distractor in the lower visual field influencing tactile

24 judgements i.e. a specific horizontal expansion of peripersonal hand space into the contralateral hemispace. Note that these findings are unlikely to be due to the older adults’ ability to discriminate single versus double lights at the 42cm ipsilateral and 42cm_opp

(contralateral) distractor locations, since performance did not differ between these locations in the light only control condition (i.e. there was equal potential for interference from these locations), plus overall accuracy was high.

In the present experiment, ipsilateral distractors were presented vertically from the stimulated hand, thus controlling for visual depth. Therefore it is possible that differences in processing and attention between the upper and lower visual fields could explain the differences between the two 42cm and 42cm_opp spatial distractors. This concept has been widely explored previously, although not in the context of ageing, demonstrating a lower visual field advantage for tasks performed in near (peripersonal) space and visuomotor coordination, compared to an upper visual field advantage for tasks performed in far (extrapersonal) space

(Previc 1990; Christman 1993; Christman and Niebauer 1997; Previc 1998). In the current task, all stimuli were presented in near space. Therefore, visual distractors in the lower visual fields (i.e. 0cm and 42cm_opp) may have received preferential processing and thus had a greater effect on tactile judgements. In addition, there is also evidence to suggest a bias in visuospatial attention towards the left hemispace in lower visual field tasks (Rubens 1985;

Christman and Niebauer 1997; Hagenbeek and Van Strien 2002; Thomas and Elias 2011).

Since the majority of participants in the experiment were right handed (n = 27), the contralateral distractor was within the lower-left visual hemispace, and thus could produce a strong distraction effect. This could be tested with a distractor placed in the opposite, upper visual hemispace. This would also enable a more general hemifield effect to be ruled out, that is, a visual stimulus placed within any region of the contralateral visual hemispace might produce a visuotactile interaction.

25 What remains unclear, however, is why older adults were influenced by both lower visual distractors, whilst younger adults were influenced by the lower distractor presented adjacent to the hand only (Poole et al. 2015a). Within the current experimental setup, the location of the contralateral distractor differs along the left-right (transverse) plane from the location of the stimulated hand, whilst the location of the elevated distractors differs on the coronal plane. Therefore, if there are difficulties with spatial representation along the transverse plane specifically, which are also exacerbated by ageing (Ghafouri and Lestienne 2000; Lepelley et al. 2010), then the location of the 42cm_opp distractor may appear closer or less distinct from the stimulated hand and thus interfere more with tactile judgements for older adults, but less so for younger.

Another difference between the upper and lower visual distractors is that the lower locations were both closer to (and equidistant from) the body/trunk, while the upper locations were more distant. Indeed, recent evidence suggests that attentional reference frames for peripersonal space shift from hand/action-centred to body/trunk-centred with increasing age

(Bloesch et al. 2013). Therefore, it could be argued that a more body-centred attentional reference frame with increasing age produced the visuotactile interactions observed for both lower visual field distractors, as opposed to the upper visual field distractor which may have been positioned beyond the limits of peripersonal trunk space. It may be possible to tease apart these hand-centred and body-centred accounts by manipulating the location of the stimulated hand.

There are several possible reasons why older adults show this altered representation of visuotactile space, irrespective of whether it is hand or body centred. Previous studies have shown enhanced multisensory processing of spatially and temporally coincident cues for older adults, which could serve as a compensatory strategy to counteract decline in unisensory (Laurienti et al. 2006; Mahoney et al. 2011) and/or motor function (Stern et al.

26 2005; Mahoney et al. 2014a; Mahoney et al. 2015). Likewise, multisensory processing could occur over greater distances as a compensatory strategy for poorer arm and hand coordination in older adults (Ketcham et al. 2002; Carmeli et al. 2003). This is supported by the fact that older adults who showed increased visuotactile interactions for spatially coincident stimuli

(0cm) also showed increased visuotactile interactions for the contralateral distractor

(42cm_opp; Fig. 3), suggesting that a general increase in multisensory processing is associated with increased processing of multisensory stimuli over a larger area. Having an expanded representation of peripersonal space could allow better identification of sensory events in near space, and thus could enable more efficient goal-directed reach movements and/or body protection from collisions (see de Vignemont and Iannetti 2014).

Alternatively, it has been proposed that decreased selective attention for a sensory modality

(as opposed to a general ability to sustain attention) could mean that older adults are less able to inhibit multisensory interactions (Poliakoff et al. 2006a; b; Peiffer et al. 2007; Setti et al.

2011a; Mozolic et al. 2012) (although see counter arguments from Hugenschmidt et al.

2009a; Hugenschmidt et al. 2009b). Indeed, Poole and colleagues (2015b) suggest a similar explanation for expanded visuotactile space in young adults with autism spectrum conditions.

Additionally, there is evidence to suggest that older adults bias their attention towards visual inputs (Sundermier et al. 1996; Simoneau et al. 1999; Newell et al. 2011; Barrett et al. 2013).

As such, older adults might be less capable of inhibiting visual stimuli within near space, which could distract from other sensory inputs (e.g. proprioceptive) which are essential for coordinating action (Rosenbaum et al. 2001; Gosselin-Kessiby et al. 2008; 2009). To examine these possibilities, it would be useful to compare visuotactile interactions with measures of goal-directed reaching in older adults. This also raises the question as to whether reduced spatial modulation in older adults is specific to visuotactile interactions, or whether it also occurs for other sensory modalities.

27 Interestingly, some previous studies have observed no spatial modulation between visual and tactile stimuli presented to the lower visual field in younger adults (Girard et al 2011; Girard et al 2013). It has been proposed that spatial modulation only occurs under certain conditions, such as when task requirements require more explicit processing of the spatial position of the targets, rather than simple RT tasks (cf. Mahoney et al. 2014b). In this instance, higher-order cognitive or attentional processes brought about by the task demands might have a top-down influence on multisensory interactions (for review see Spence 2013).

Although our modified method does not include an explicit spatial judgement, the task required participants to make a demanding discrimination which may require more attentional orienting towards the stimulated hand (Poole et al. 2015a). The critical finding is that for this particular task, older adults do not show spatial modulation, whereas younger adults do.

Turning to the temporal findings, visuotactile interactions were temporally modulated for older adults, in keeping with the temporal rule of multisensory processing (Meredith et al.

1987). A similar pattern was obtained for younger adults (Poole et al. 2015a), whereby significant congruency effects extended up to a 100ms SOA, but were diminished thereafter, supporting the notion that visuotactile interactions can last up to several hundred milliseconds

(Shore et al. 2006). For the 200 and 400ms SOA distractors, it is likely that the visual stimulus fell outside of the “temporal window” to interact with the tactile target, and so had less influence on the tactile judgements (see Colonius and Diederich 2004; Diederich et al.

2008). Indeed, the decision making process for the tactile judgement may have already been completed prior to the presentation of the distractor (especially by the 400ms SOA). These findings are inconsistent with previous observations of multisensory interactions over larger temporal discrepancies for older adults (Virsu et al. 2003; Poliakoff et al. 2006b; Diederich et al. 2008; Setti et al. 2011a; b). Using the flash-beep illusion, the results of Setti and

28 colleagues (2011a) suggested that the temporal binding window extends up to 150-190ms in older adults and 70ms in younger. Given that the temporal increments in current experiment were large (100ms and 200ms), more subtle changes in temporal processing may have been missed.1

On the other hand, temporal modulation may have been intact in the current group of participants. Indeed, previous studies have implicated poorer temporal processing of multisensory stimuli in fall behaviour (Setti et al. 2011a; Stapleton et al. 2014), whereas the current participants were all deemed as having a low fall risk. Furthermore, a recent study suggests that younger and healthy older adults do not differ in their ability to distinguish temporally discrepant audiovisual stimuli (Fiacconi et al. 2013). The authors point out that studies measuring the temporal limits of multisensory interactions produce variable results, even when using similar age groups and assessing similar multisensory (audiovisual) interactions. They suggest that inconsistency in the methods could explain these between study differences. As highlighted previously, although the current method might be insensitive to detecting age-related differences, the near significant CE for the 100ms SOA suggest some age-related change in temporal modulation was captured, or at least for some older adults. Moreover, the significant positive correlation between the visuotactile interactions for the contralateral distractor and later SOAs (400ms and close to significant for

200ms) implies that those who have an expanded representation of visuotactile space also have expanded temporal window in which visuotactile interactions can occur. This could demonstrate a fundamental enhancement in multisensory processing with increasing age,

1 Note that the temporally coincident distractor was presented at an SOA of -30ms, since this time point has been found to produce a judgment of simultaneity in younger adults (Spence et al. 2004;

Poole et al. 2015a). However, it is difficult to fully interpret temporal coincidence in ageing since this has not been fully mapped out for older adults.

29 across both spatial and temporal domains. Future experiments could explore the interaction between spatial and temporal processing in older adults in greater detail (cf. Stevenson et al.

2012).

To summarise, the current findings suggest that spatial processing of visuotactile interactions is altered in older adults, while more subtle effects may occur for temporal processing. The overall pattern of temporal modulation for older adults was the same as for younger participants, but the correlational analyses suggest that some individuals may be more affected by spatially and temporally discrepant distractors. Altered visuotactile interactions may underlie some of the difficulties with goal-directed movements for older adults, and thus it may be possible to develop technology or therapeutic strategies to assist older persons in their daily functioning. For example, Lee, Poliakoff and Spence (2009) have shown that older adults benefit more from a combination of visual, tactile and auditory feedback when using touch screen devices. Mahoney and colleagues (2014b) also suggest that expanded spatial processing could be capitalised on to develop “multisensory cross-walk stimulators” to assist with crossing the road. Likewise, it may be possible to provide more sensory cues in near space to guide goal-directed reaching actions. Alternatively, improving selective attention to a sensory modality could prevent irrelevant sensory events from disrupting perception and action. For example, Setti and colleagues (2014) implemented a training programme to improve audiovisual temporal order judgements, which also reduced older adults’ susceptibility to the flash-beep illusion, which could be used to improve balance in fall prone older adults. In a similar way, it may be possible to train older adults to reduce their representation of visuotactile space and/or the temporal window in which visuotactile interactions may occur.

30 Conclusion

A modified version of the CCT was used to assess spatial and temporal modulation of visuotactile interactions in older adults. Temporal modulation appears to be less affected by increasing age, with visuotactile interactions only occurring when presented as subjectively simultaneous. In contrast, the pattern of spatial modulation in older adults differed from that seen in younger adults, with interactions being seen for visual distractors far from the stimulated hand and in the lower visual field. As such, the representation of near visuotactile peripersonal space appears to be expanded for older adults. Whilst this could be attributed to poorer selective attention to the tactile modality, this expanded spatial processing may reflect a compensatory mechanism for poorer control of reaching movements. However, further research is required to determine the mechanisms underlying this reduced spatial modulation of visuotactile interactions for older adults, whether it is a general multisensory effect which applies to other sensory modalities, and how it relates to the coordination of arm and hand movements.

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40 Table 1 Mean reaction times (ms, ±SEM) for each condition in each task. Outliers from each participant’s data, for each condition, were removed via the non-recursive procedure as described by van Selst and Jolicoeur (1994). This accounted for 1.8% and 2.0% of the data in the spatial and temporal tasks, respectively. Note that no temporal or spatial modulation was observed for reaction time measures (all p > .05).

Spatial task (n = 26) Position Baseline 0cm 21cm 42cm 42cm_opp 749 736 746 753 (22.3) congruent 763 (26.1) RT (ms) (20.0) (19.8) (24.3) 763 762 761 incongruent 778 (26.9) (26.4) (27.1) (22.0) Temporal task (n = 26) SOA Baseline -30ms 100ms 200ms 400ms 743 767 749 746 (20.2) congruent 735 (20.5) RT (ms) (23.5) (20.8) (20.0) 758 755 750 incongruent 738 (21.5) (24.2) (23.7) (22.1)

41 Table 2 One-sample t-test statistics to determine significant congruency effects for both spatial and temporal tasks. Asterisks denote significant congruency effects (Bonferroni correction, p < .0125). Effect sizes (Cohen’s d) below 0.20 is considered small, 0.50 medium, and 0.80 large.

Position t (25) p d SOA t (25) p d 0cm 3.88 .001* 0.99 -30ms 3.11 .005* 0.85 21cm 4.24 <.001* 0.80 100ms 2.63 .015 0.46 42cm 2.52 .019 0.35 200ms -0.33 .747 0.06 42cm_opp 4.55 <.001* 0.95 400ms -0.76 .454 0.08

42 Table 3 One-sample t-test statistics to determine significant interference effects for incongruent visual

distractors, for both spatial and temporal tasks. Asterisks denote significant interference effects (Bonferroni correction, p < .

006). Effect sizes (Cohen’s d) below 0.20 is considered small, 0.50 medium, and 0.80 large.

Position t (25) p d SOA t (25) p d 0cm 4.12 <.001* 0.86 -30ms 4.56 <.001* 1.08 21cm 4.20 <.001* 0.73 100ms -2.15 .042 0.48 42cm 1.99 .058 0.35 200ms -0.44 .663 0.09 42cm_opp 3.50 .002* 0.73 400ms -0.72 .479 0.14

Table 4. Summary of linear regression model for predicting congruency effects (i.e. visuotactile interactions) at

the 42cm_opp distractor location.

Mode Coefficients l Unstandardized Standardize t p 95.0% coefficients d Confidence

43 coefficients interval for B B Std. Beta Lower Upper Error bound bound 1 SART – no-go accuracy 0.16 0.16 0.20 1.00 0.32 -0.17 0.49 9 Stroop – interference 0.21 0.17 0.25 1.23 0.23 -0.14 0.56 score 0 2 SART – no-go accuracy 0.16 0.17 0.20 0.94 0.35 -0.19 0.51 6 Stroop – interference 0.20 0.18 0.24 1.11 0.27 -0.18 0.58 score 9 Age 0.28 0.55 0.11 0.50 0.62 -0.86 1.42 0 Gender -0.01 6.70 0.00 0.00 0.99 -13.94 13.93 9 3 SART – no-go accuracy 0.13 0.16 0.17 0.83 0.41 -0.20 0.46 8 Stroop – interference 0.24 0.17 0.28 1.39 0.18 -0.12 0.60 score 1 Age 0.40 0.52 0.16 0.76 0.45 -0.69 1.48 5 Gender -3.34 6.55 -0.11 - 0.61 -17.01 10.33 0.51 6 Tactile threshold 0.42 0.22 0.39 1.91 0.07 -0.04 0.88 1

Figure 1

44

42cm

29cm + 21cm

42cm 0cm _opp

Bone conductor

Figure 2.

Figure 3.

45 46