This article was downloaded by: [Oulu University Library]On: 15 February 2014, At: 05:03Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH,UK

Laterality: Asymmetries of Body,Brain and CognitionPublication details, including instructions for authorsand subscription information:http://www.tandfonline.com/loi/plat20

Visual rightward spatial biasvaries as a function of ageFiia Takio a b , Mika Koivisto a b , Tuulikki Tuominen c ,Seppo J. Laukka c & Heikki Hämäläinen a ba Department of Psychology , University of Turku ,Turku , Finlandb Centre for Cognitive Neuroscience , University ofTurku , Turku , Finlandc Learning Research Laboratory (LearnLab) , Universityof Oulu , Oulu , FinlandPublished online: 13 Jan 2012.

To cite this article: Fiia Takio , Mika Koivisto , Tuulikki Tuominen , Seppo J. Laukka& Heikki Hämäläinen (2013) Visual rightward spatial bias varies as a functionof age, Laterality: Asymmetries of Body, Brain and Cognition, 18:1, 44-67, DOI:10.1080/1357650X.2011.628675

To link to this article: http://dx.doi.org/10.1080/1357650X.2011.628675

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all theinformation (the “Content”) contained in the publications on our platform.However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, orsuitability for any purpose of the Content. Any opinions and views expressedin this publication are the opinions and views of the authors, and are not theviews of or endorsed by Taylor & Francis. The accuracy of the Content shouldnot be relied upon and should be independently verified with primary sourcesof information. Taylor and Francis shall not be liable for any losses, actions,claims, proceedings, demands, costs, expenses, damages, and other liabilities

whatsoever or howsoever caused arising directly or indirectly in connectionwith, in relation to or arising out of the use of the Content.

This article may be used for research, teaching, and private study purposes.Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expresslyforbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Visual rightward spatial bias varies as a function of age

Fiia Takio1,2, Mika Koivisto1,2, Tuulikki Tuominen3,Seppo J. Laukka3, and Heikki Hamalainen1,2

1Department of Psychology, University of Turku, Turku, Finland2Centre for Cognitive Neuroscience, University of Turku, Turku,

Finland3Learning Research Laboratory (LearnLab), University of Oulu, Oulu,

Finland

Age-related changes in visual spatial biases in children, young adults, and olderadults were studied with unilateral and bilateral stimulus conditions in fast-pacedlinguistic and non-linguistic attention tasks. Only rightward spatial biases wereobserved. The incidence of the biases changed as a function of age: in childhoodand in old age the rightward spatial biases were more common than in youngadulthood. The present rightward spatial biases were similar to those observed inthe corresponding auditory spatial linguistic and non-linguistic attention tests(Takio, Koivisto, Laukka, & Hamalainen, 2011) and in the dichotic listeningforced-attention task (Takio et al., 2009). We suggest that the multimodal rightwardspatial bias observed under intensive attentional load is related to a right hemispacepreference and modulated by age-dependent changes in executive functions.

Keywords: Visuospatial bias; Executive functions; Age.

The cerebral hemispheres are asymmetrical both functionally and structu-

rally. The asymmetries change as a function of age beginning before birth

and continuing into old age (e.g., Boles, Barth, & Merrill, 2008; Dolcos,

Rice, & Cabeza, 2002; Everts et al., 2009; Hugdahl, 2003; Hugdahl et al.,

2009; McCartney & Hepper, 1999). The main focus of the present study was

Address correspondence to: Fiia Takio, Department of Behavioural Sciences and Philosophy,

University of Turku, 20014 Turku, Finland. E-mail: fiia.takio@utu.fi

This study was supported financially by the Nordic Centre of Excellence in Cognitive Control,

by the Finnish Cultural Foundation and by the National Doctoral Programme of Psychology in

Finland. MK was supported by the academy of Finland (project 125175). We thank Teemu Laine

for the programming and Ville Penttila, Mika Rekila, Faramosh Rashid, and Laura Jokiranta for

testing the participants. We also thank Jacqueline Valimaki and Paula Korhonen for providing

language help. Finally we thank all the participants for taking part in the study.

Laterality, 2013

Vol. 18, No. 1, 44�67, http://dx.doi.org/10.1080/1357650X.2011.628675

# 2013 Taylor & Francis

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

to investigate the age-related changes in hemispace asymmetries in visual

modality, as is expected on the bases of the asymmetry of attention

mechanisms (Corbetta, Patel, & Shulman, 2008; Corbetta & Shulman,

2002; Heilman, Bowers, Valenstein, & Watson, 1987; Kinsbourne, 1987;

Posner & Petersen, 1990) and of the recent findings of age-dependent

changes of asymmetry in auditory modality (Takio et al., 2009, 2011).

Functional asymmetries in visual and auditory modality are due to

perceptual biases of the two hemispheres in processing complex information

(e.g., Everts et al., 2009; Ivry & Robertson, 1998; Telkemeyer et al., 2009).

For example, in visual half-field presentation and in dichotic listening,

linguistic material is often better perceived and recognised from the right

than from the left visual field or ear (Hugdahl et al., 2009; Kimura, 1966,

1967; Takio et al., 2009; Voyer, 2001), presumably reflecting the left-

hemisphere’s dominance in language processing. Recently it has been

proposed that the asymmetrical hemispheric activation in many perceptual

asymmetry studies is associated with hemispheric lateralisation of spatial

attention mechanisms (e.g., Callaert et al., 2011; Takio et al., 2011). The

attention mechanisms are right-hemisphere lateralised, as suggested by

neglect and split-brain patient studies (Dobler, Manly, Verity, Woolrych, &

Robertson, 2003; Heilman et al., 1987; Kinsbourne, 1987; Laurent-Vannier,

Pradat-Diehl, Chevignard, Abada, & De Agostini, 2003; Proverbio, Zani,

Gazzaniga, & Mangun, 1994; Trauner, 2003), as well as by the studies on

healthy participants (Corbetta et al., 2008; Corbetta & Shulman, 2002;

Posner & Petersen, 1990). For example, Corbetta et al. (2000) in their event-

related fMRI study found that in healthy adults the activation in the right

temporoparietal cortical junction was stronger when the target occurred at

an unattended location than at an attended location. This was proposed to

indicate that the area involved in the processes of visual spatial reorienting is

right lateralised (see also Posner, 2008; Posner & Raichle, 1994). It has also

been suggested that the alerting system is right-hemisphere-lateralised in

healthy humans (for review see Callejas, Lupianez, Funes, & Tudela, 2005;

Posner & Petersen, 1990).

The functional imbalance between the two hemispheres after unilateral

neglect has evoked diverse theoretical models of hemispheric asymmetry in

attentional mechanisms. According to Kinsbourne’s model (e.g., Kins-

bourne, 1987), both hemispheres orient attention towards the contralateral

hemispace, but the left hemisphere has a stronger directional bias than the

right hemisphere. Heilman and colleagues (1987) proposed that the

attentional control of the two hemispheres is not equivalent; the right

hemisphere has bilateral spatial attentional control over the visual field so

that it can initiate orienting responses to stimuli in either hemispace, while

the left hemisphere’s attentional control is only contralateral. Thus,

VISUAL SPATIAL BIAS AND AGE 45

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

according to both views, attention is more strongly biased toward the right

hemispace.

It has been suggested that young adults are capable of modulating and

balancing the extent and the magnitude of the inherent asymmetries in

auditory modality with the help of executive functions; that is, with skills

necessary for high-level perceptual and cognitive goal-directed behaviour

such as attentional control and cognitive flexibility (e.g., Andersson &

Hugdahl, 1987; Hugdahl & Andersson, 1986; Hugdahl et al., 2009; Jurado &

Rosselli, 2007; Mondor & Bryden, 1991; Posner & Raichle, 1994; Takio et al.,

2009, 2011). For example, in bilateral dichotic stimulation with linguistic

stimuli a typical finding is a stimulus-driven right-ear advantage (REA),

reflecting left hemisphere’s dominance in language processing. Here adults

are capable of changing the REA into a left-ear advantage by directing

attention towards the left-ear stimuli, while children and older adults are

not able to do so (e.g., Hugdahl et al., 2009; Kimura, 1967; Takio et al.,

2009). Moreover, stronger rightward spatial biases have been observed in

childhood and in old age than in young adulthood in fast-paced linguistic

and non-linguistic auditory tests under sufficiently intensive attentional

load (Takio et al., 2011). It has been suggested that these age-related

changes in auditory rightward spatial bias result from early development

and late decline of executive functions (Hamalainen & Takio, 2010; Takio

et al., 2009, 2011; see also Anderson, Anderson, Northam, Jacobs, &

Catroppa, 2001; Jurado & Rosselli, 2007; Luciana, Conklin, Hooper, &

Yarger, 2005; Tsujimoto, 2008).

The purpose of the present study was to determine whether the rightward

spatial bias observed under sufficiently intensive attentional load in auditory

modality is a multimodal phenomenon that also occurs in visual tests

mimicking the fast-paced auditory linguistic and non-linguistic tests applied

in our previous study (Takio et al., 2011), and whether the visual hemispace

biases change as a function of age. As linguistic material is often better

perceived and recognised from the right than from the left visual field, spatial

biases for linguistic stimuli were expected to occur towards the right

hemispace. Since no unequivocal hemispheric advances have been docu-

mented in the processing of non-linguistic stimuli (such as dots), it was

assumed that if any spatial biases in the detection of non-linguistic visual

stimuli (such as dots) under attentional load were to be observed, the biases

would most probably result from hemispheric functional asymmetries in

other than linguistic mechanisms, for example, in the attentional mechan-

isms that are biased towards the right side. Moreover, based on our findings

from the auditory modality (Takio et al., 2009, 2011), we hypothesised that if

any hemispace biases were to be observed, they would be more intensive in

the child and the older adult participants than in the young adults. Two fast-

paced, attention-loading, linguistic and non-linguistic tests were applied for

46 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

children, young adults, and old adults. In these tests the observers had to

monitor the whole visual field while the stimuli were presented to the left

visual field (LVF), to the right visual field (RVF), or to both visual fields

bilaterally (BVF).

METHOD

Participants

A total of 190 Finnish-speaking participants were tested and divided into

five age groups (see Table 1). Since the development of language abilities has

been shown to influence 5�12-year-old children’s asymmetrical performance

in linguistic spatial attention tasks (e.g., Helland & Asbjørnsen, 2001; Takio

et al., 2009), and many important executive functions have been shown to

reach maturity around the ages of 8�10 years (e.g., Jurado & Rosselli, 2007),

children in children’s day-care aged up to 7 years and children in primary

school from age 7 years on were tested and divided into three age groups:

5�7-year-olds, 8�9-year-olds, and 10�11-year-olds. Furthermore, partici-

pants over 50 years of age have been reported to be unable to overcome the

inherent perceptual asymmetry with the executive control of attention (e.g.,

Hugdahl, 2003; Hugdahl, Carlsson, & Eichele, 2001; Jurado & Rosselli,

2007; Takio et al., 2011; Thomsen et al., 2004), and thus old participants

between 59 and 79 years of age were included in the study. All participants

volunteered and they were right-handed (Oldfield, 1971).

Adult participants gave their written informed consent to participate in

the study, and filled in a questionnaire asking about educational level,

mother tongue, profession, vision, hearing, previous or present neurological

and/or psychiatric disorder(s), dyslexia or brain damage, and possible

medication. Only healthy participants with normal or corrected vision

were included in the study. To assess the adult participants’ working memory

capacity, the numeric short-term memory of the adult participants was tested

with the Wechsler Memory Scale � Revised (Digit Span). To exclude the

possible interference of any depressive symptoms on the visual test results, a

brief Finnish modified version of the Geriatric depression scale was applied

(Yesavage et al., 1983). To screen the possible influence of mild cognitive

impairment (MCI) on the study (e.g., Karrasch, Sinerva, Gronholm, Rinne,

& Laine, 2005), the older adult age group was tested with the Wordlist

learning test and the Wordlist delayed recall in Finnish version of the

Consortium to Establish a Registry for Alzheimer’s Disease (CERAD).

Moreover, the adult participants were asked about possible drug or alcohol

misuse and the amount of sleep during the last 24 hours, in order to evaluate

their alertness at the beginning of the testing.

VISUAL SPATIAL BIAS AND AGE 47

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Before testing the child participants, written permission for the study was

requested from the heads of the children’s day-care centres and of the

comprehensive schools, the teachers and the primary caregivers. Only

healthy participants with normal or corrected vision were included in the

study. None of the children had suffered brain damage or had any untreated

visual, auditory, or neurological deficits during early childhood. Also,

children with dyslexia were not included in the study. The phonological

awareness of children under the age of 9 years was assessed with parts of the

Phonological Awareness Test (Poskiparta, Niemi, & Lepola, 1994; Silven,

TABLE 1The age groups and gender distributions in different subtasks

Subtask Age group N Females/males Mean age SD

Visual Go/No-Go spatial attention (VGSA)

2T, SOA1 �500�1500 ms

19�32 years 38 20/18 24.8 3.12

59�79 years 33 11/22 69.5 4.78

4T, SOA1 �500�1500 ms

19�32 years 39 21/18 24.7 3.14

59�79 years 33 11/22 69.5 4.78

2T, SOA2 �300�800 ms

5�7 years 29 16/13 6.4 0.66

8�9 years 42 20/22 9.1 0.49

10�11 years 24 13/11 10.8 0.32

19�32 years 39 21/18 24.7 3.17

59�79 years 33 12/22 69.5 4.78

4T, SOA2 �300�800 ms

5�7 years 29 16/13 6.4 0.66

8�9 years 42 20/22 9.1 0.49

10�11 years 24 13/11 10.8 0.32

19�32 years 39 21/18 24.7 3.14

59�79 years 34 12/22 69.2 5.04

Visual divided spatial attention (VDSA)

SOA �750 ms

5�7 years 29 16/13 6.4 0.66

8�9 years 42 20/22 9.1 0.49

10�11 years 29 14/15 10.8 0.31

19�32 years 50 30/20 24.6 3.02

59�79 years 40 18/22 69.0 4.82

The data from some of the participants had to be excluded due to either technical problems or

the participant’s inability or refusal to perform the test. Therefore the number of participants in the

different age groups varies between the tests.

48 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Poskiparta, Niemi, & Voeten, 2007): Rhyme task (Riimit), Alliteration task

(Alkusointu), and Phoneme-isolation task (Alkuaanne).

Tests

We used two different visual tests with unilateral and bilateral (left and right

visual fields) stimulation: a linguistic Visual Go/No-Go spatial attention test(VGSA) with pictures of animals or digits, and a non-linguistic Visual

divided spatial attention test (VDSA) with dots of light.

Visual Go/No-Go spatial attention test (VGSA)

Apparatus and stimulus material. Digits 1�9 were visually presented to

the adults and nine different animal drawings to the children with the

Presentation program via a projector (Ask C40 or XGA Hitachi ED-x3280,

Multimedia mobile LCD projector); they were projected into the left (LVF)

and/or right (RVF) visual field in light grey (61 cd/m2) on a dark grey

background (5 cd/m2). A single stimulus was projected 308 to the right and/

or the left from the fixation point (9 cd/m2) measured from the centre of the

fixation point to the nearest edge of the stimulus. The digits wereapproximately 48 high and 28 wide and the pictures of the animals were

approximately 88 high and 108 wide.

Procedure for adult participants. The VGSA test for adults consisted of

four subtasks, which varied according to their cognitive load. Each subtask

included 60 target trials and 180 non-target trials. The target digits were 3, 6,8, or 9, and the non-target digits were 1, 2, 4, 5, and 7. Each stimulus (digit)

was 200 ms in duration. In the 60 target trials 20 were presented in

randomised order unilaterally to the left (LVF), 20 to the right (RVF), and

20 bilaterally to both visual fields (BVF) with simultaneous onset. The side

of the targets was counterbalanced across the participants. The same digit

was never presented bilaterally and the fixation point was presented on the

screen throughout the whole test (see Figure 1A).

The subtasks varied either according to the duration of the stimulus-onsetasynchrony (SOA) time (500�1500 ms or 300�800 ms) and/or the number of

target digits (two targets or four targets). The SOA refers to the randomly

varying time interval between the onsets of two successive stimuli (see Figure

1b). Two of the subtasks had the same SOA (500�1500 ms�SOA1), but they

differed from each other in the number of targets that the participant was to

respond to: two target digits (one target digit to the left and the other to the

right) or four target digits (two target digits to the left and the other two to

the right). The duration of these two subtasks was approximately 4 minutes55 seconds. The two other subtasks also differed from each other in the

VISUAL SPATIAL BIAS AND AGE 49

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

number of targets (two target digits or four target digits), while the SOA was

300�800 ms (SOA2) in both subtasks. The duration of these two subtasks

was approximately 3 minutes. In all subtasks the participants’ task was to

fixate their eyes on the fixation point, to monitor the whole visual field, and

Figure 1. (A) An example of the stimulation sequence in the Visual Go/No-Go spatial attention

(VGSA) task for adults. (B). The stimulus-onset asynchrony (SOA) varied randomly between the

onsets of successive stimuli. The figure depicts the stimulus-response sequences and the time windows

for correct responses. For details of each subtask, see the text. Abbreviations: R = right side; L = left

side; SOA = stimulus-onset asynchrony time; T = target; nT = non-target. The relative sizes of the

stimuli and the distances between the fixation point and the stimuli in the picture do not correspond to

the test attributes applied in the actual test.

50 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

to respond unilaterally to the side where the unilateral target occurred, and

bilaterally to the bilaterally presented targets by pressing buttons on the

computer keyboard as rapidly and accurately as they could with the left and/

or right forefinger only when a target or targets were perceived. The left-

hand button for the LVF targets on the computer keyboard was the leftmost

Control button and the right-hand button for the RVF targets was therightmost Num enter button. In the instructions the order in which the

target digits were introduced to the participants was counterbalanced so that

half of the participants were given the LVF target digits first and the other

half the RVF target digits first. The adult participants always performed first

the two subtasks with the SOA1 (two targets, four targets) and then the two

subtasks with the SOA2 (two targets, four targets). The order of the subtasks

was based on piloting studies conducted in the Centre for Cognitive

Neuroscience, showing that if the order of the subtasks was the opposite,starting with the more difficult subtasks, the performance of old people in

particular was reduced dramatically throughout the test. Perhaps a too-

difficult subtask at the beginning of the testing prevents any learning of the

novel situation, and further reduces the person’s ability to perform even in

the easier subtasks.

The participants were seated 1 metre from the screen. A video camera

(Samsung Digital-Cam, VP-D351) was used to control the central fixation.

Central fixation was encouraged by presenting the stimuli randomly to thevisual fields (LVF and/or RVF), ensuring that the participants were unable to

anticipate the location of the stimulus, and thus were less likely to shift their

fixation from the central location. In addition, the participants were strongly

advised to fixate their eyes on the central fixation point to ensure optimal

performance in this particular test. The experimenter followed the partici-

pant’s central fixation in real time throughout the practice block and the

actual test and, if required, immediately reminded the participant verbally

about the central fixation. Before the actual tests the participants performeda practice block, which included 15 target trials and 45 non-target trials. The

actual test started once the participant and the experimenter were both

confident that the participant was able to perform the test and had

understood the instructions correctly.

Procedure for child participants. The visual tests mimicked our pre-

viously applied auditory tests (Takio et al., 2011), which included digits for

adults and names of animals for children. To ensure that the visual and

auditory tests would be analogical between the auditory and the visual

modality, the stimulus digits in VGSA for adults were changed to pictures of

animals in the children’s version (Figure 2). Children’s ability to stay focused

on cognitively demanding tasks for long periods of time is inferior to that ofadults. On the basis of the pilot studies in the laboratory of the Learning

VISUAL SPATIAL BIAS AND AGE 51

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Research Laboratory (LearnLab), University of Oulu, the VGSA test for

children was shortened to two subtasks. The targets were animal drawings of

‘‘cat’’, ‘‘dog’’, ‘‘sheep’’, and ‘‘rabbit’’, and the non-target drawings were of

‘‘pig’’, ‘‘goose’’, ‘‘cow’’, ‘‘rooster’’, and ‘‘horse’’. The stimulus-onset asyn-

chrony (SOA) varied randomly between 300 and 800 ms (�SOA2) and the

difficulty level varied as a function of the number of targets: two target

animals (one target to the left visual field and the other to the right visual

field) or four target animals (two targets to the left visual field and the other

two to the right visual field). The duration of these two subtasks was

approximately 3 minutes. The participants performed first the subtask that

included two targets and then the subtask that included four targets. All

other conditions corresponded to those in the VGSA test for adults.

To help the children stay focused on the task the experimenter told a

frame story (see Sanders, Stevens, Coch, & Neville, 2006). In the story the

participant was a zookeeper feeding only particular animals (targets) from

either left or right side (LVF or RVF). The participants were asked to fixate

their eyes on the fixation point, to monitor the whole visual field, and to

press the buttons (give food) on the computer keyboard as rapidly and

accurately as they could with the right and/or left forefinger only when they

perceived the targets. Since the performance of children, especially of young

ones, is rather sensitive to task- and stimulus-related factors (Ridderinkhof

& van der Stelt, 2000), all the child participants were first allowed to watch

the stimuli without responding and then carry out a practice block (for

details, see procedure for adult participants) before the actual test took place.

The actual test started after the participant and the experimenter were both

confident that the participant was able to perform the test and had

understood the instructions correctly.

Figure 2. An example of the non-target (rooster) and the target (rabbit) pictures of the animals

presented to child participants in the Visual Go/No-Go spatial attention test (VGSA).

52 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Visual divided spatial attention test (VDSA)

Apparatus and stimulus material. Dots of light (28; 63 cd/m2) were

presented with the Presentation program via a projector (XGA Hitachi ED-x3280, Multimedia mobile LCD projector or ASK C40) into the LVF and/or

RVF on a grey background (3 cd/m2). The dots were projected 308 to the

right and/or the left from the fixation point (9 cd/m2), measured from the

centre of the fixation point to the nearest edge of the stimulus.

Procedure. The VDSA test consisted of two subtasks that differed intheir stimulus-onset asynchrony (SOA), which was either 1500 ms or 750 ms.

In both subtasks, of a total of 150 stimuli, 50 were presented in randomised

order to the LVF, 50 to the RVF, and 50 bilaterally to both visual fields

(BVF) with simultaneous onset. Each stimulus was presented on the screen

for 20 ms. The fixation point was presented on the screen throughout the

whole test. The participants’ task was to fixate their eyes on the fixation

point, monitor the whole visual field, and to press the buttons on the

computer keyboard as rapidly and accurately as they could with their rightand/or left forefinger unilaterally to the side where the unilateral stimuli

occurred, and bilaterally to the bilaterally presented stimuli. The left-hand

button on the computer keyboard was the leftmost Control button and the

right-hand button was the rightmost Num enter button. For the details

about controlling for the central fixation, see the VGSA test for adults.

Before the actual tests the participants performed a practice block. The adult

participants and the 10�11-year-old children completed the subtask with the

SOA of 1500 ms first (duration approximately 3 minutes) and then thesubtask with the SOA of 750 ms (duration approximately 2 minutes 5

seconds). The 5�9-year-old participants accomplished only the subtask with

the SOA of 750 ms.

Data analysis

A unilateral response made to the right or the left visual field target/stimulus

was scored as a correct response when it occurred on the same side within150 and 1000 ms after the onset of the target/stimulus in the VGSA and the

VDSA tests. Simultaneous left and right responses were considered as a

correct bilateral response when they occurred in the VGSA within 150�1800

ms and in the VDSA within 150�1000 ms after the onset of a target/stimulus

(see Figure 1B). All these time windows were defined according to pilot

studies carried out in the laboratory of Centre for Cognitive Neuroscience,

University of Turku. The responses that were not made within the specified

time windows were recorded as false alarms in the VGSA test and as extraresponses in the VDSA test. The correct responses, the unilateral responses

VISUAL SPATIAL BIAS AND AGE 53

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

for bilateral stimuli/ targets, the false alarms (VGSA), and the extra

responses (VDSA) were converted into percentages. In addition, median

reaction times in correct unilateral responses were analysed.

The accuracy data from the VGSA test were analysed according to the

Signal detection theory (SDT) (Stanislaw & Todorov, 1999). When either

the correct response rate is 1.0 (100%) or the false alarm rate is zero, the

sensitivity (d’) and the decision criterion (c) values have an unlimited numeric

value and cannot be included in the SDT analysis. In order to overcome this

problem the estimates for d’ and c were converted according to Macmillan

and Creelman (2005): proportions of zero were converted to 1/(2N) and

proportions of one were converted to 1 � 1/(2N), with N referring to the

number of trials contributing to the proportion. In SDT the sensitivity (d’)

and decision criterion (c) values were calculated for the left and right side

separately by using all correct responses (i.e., hits) (for both unilateral and

bilateral targets) and all false alarms (for both unilateral and bilateral non-

targets).

First, to test whether the age groups were able to discriminate signals

(targets) from noise (non-targets) and how conservative was the decision

criterion (c) that each age group applied, the sensitivity values (d’) and the

decision criterion (c) values were compared with the test value zero with

One-Sample t-test for each age group separately.

The data from the VGSA test for children were statistically evaluated by a

general 2 (Target: 2 Targets, 4 Targets)�2 (Visual Field: LVF, RVF)�3

(Age group: 5�7; 8�9; 10�11)�2 (Gender: male, female) analysis of variance

(ANOVA). The data from the VGSA test for adults were statistically

evaluated by a general 2 (SOA: SOA1 [500�1500 ms], SOA2 [300�800

ms])�2 (Target: 2 Targets, 4 Targets)�2 (Visual Field: LVF, RVF)�2 (Age

group: 19�32; 59�79)�2 (Gender: male, female) analysis of variance

(ANOVA).

All participants performed the VDSA subtask with the SOA of 750 ms.

The data of the VDSA subtask with the SOA of 750 ms were statistically

evaluated by a general 5 (Age groups: 5�7, 8�9, 10�11, 19�32, 59�79)�2

(Gender: male, female)�3 (Visual Field: LVF, BVF, RVF) ANOVA. Since

three age groups (10�11-year-olds, 19�32-year-olds, and 59�79-year-olds)

also performed another subtask with the SOA of 1500 ms, we analysed these

data by a general 3 (Age groups: 10�11, 19�32, 59�79)�2 (Gender: male,

female) and 3 (Visual Field: LVF, BVF, RVF) ANOVA. Because the result

from the VDSA subtask with the SOA of 1500 ms did not change the

conclusions that could be drawn from the results of the subtask with the

SOA of 750 ms, and the only novel conclusion that could be drawn on

the basis of the results was that increasing presentation speed affected more

the 59�79-year-old adults’ performance than the performance of the young

54 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

adults or the 10�11-year-olds, we do not report the results from the VDSA

with the SOA of 1500 ms.

In all ANOVAs the significance levels were corrected with the Greenhouse-

Geisser correction when the degrees of freedom were higher than 1.

Significant interactions were followed up by ANOVAs and t-tests. Since the

data in some of the variables were not normally distributed, they were alsoanalysed with the Wilcoxon Signed Ranks non-parametric test. The results

from the non-parametric tests are reported only if they are in conflict with the

significance levels of the parametric and non-parametric tests. Finally, we do

not report the results of Gender because of large inconsistency in the results.

RESULTS

Visual Go/No-Go spatial attention test (VGSA) for children

Sensitivity values (d’). Figure 3A presents the sensitivity values (d’) for

LVF and RVF in the VGSA subtasks with the SOA2 with two targets (2T)and with four targets (4T) for each child age group. One-Sample t-test for

each age group separately showed that in all age groups the sensitivity

values (d’) differed significantly from the test value of zero (ps 5 .003): all

child groups were able to discriminate signals (targets) from noise (non-

targets) in both VGSA subtasks. The general ANOVA for d’ revealed that

increasing the number of targets from two to four decreased the ability to

discriminate the targets from the non-targets, F(1, 89)�16,71, p B.001,

hp2�.16. The performance of 5�7-year-olds was significantly inferior tothat of older children, F(2, 89)�14.05, p B.001, hp2�.24.

Decision criterion (c). Figure 3B presents the decision criterion (c)

values for LVF and RVF in the VGSA subtasks with the SOA2 with two

targets (2T) and with four targets (4T) for each child age group. One-Sample

t-test for each age group separately showed that in all age groups the decision

criterion (c) differed significantly from the test value of zero (psB.001), and

that all values of c were positive. In other words, the decision criteria in all

child age groups were reasonably conservative, and the participants had abias rather not to respond (correct rejection or miss) than to respond

(correct response or false alarm) in both VGSA subtasks. The general

ANOVA for c revealed that increasing the cognitive load lowered the

decision criterion, F(1, 89)�11.30, p�.001, hp2�.11, and the children

responded more readily to the RVF stimuli than to the LVF stimuli

regardless of whether the stimulus was a target or a non-target, F(1,

89)�12.11, p�.001, hp2�.12. Visual inspection of Figure 3B reveals that

the strength of the bias varies in different age groups and separate ANOVAsin each age group indeed showed that only the 5�7-year-old children,

VISUAL SPATIAL BIAS AND AGE 55

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Figure 3. Sensitivity values (d’), decision criterion (c) values, percentage of unilateral responses to bilateral targets, and reaction times (RTs) in milliseconds for the

left and the right side in the Visual Go/No-Go spatial attention test (VGSA) in the child age groups. The vertical bars represent the Standard Error of the Mean

(SEM).

56

TA

KIO

ET

AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

F(1, 27)�7.75, p�.010, hp2�.22, and the 8�9-year-old children, F(1,

40)�13.18, p�.001, hp2�.25, had a greater decision criterion (c) for the

LVF stimuli than for the RVF stimuli. In other words, only the children

between 5 and 9 years of age were biased towards the right visual field since

they responded more often towards the right side than towards the left side

irrespective of the presence or the absence of the target.

Unilateral responses to bilaterally presented targets. Figure 3C presents

the unilateral responses to bilaterally presented targets for LVF and RVF in

the VGSA subtasks with the SOA2 with two targets (2T) and with four

targets (4T) for each child age group. The ANOVA for unilateral responsesto the bilateral targets showed a significant main effect for Age group,

F(2, 89)�4.53, p�.013, hp2�.09: the 10�11-year-old children were

significantly better in detecting bilateral targets than their younger counter-

parts (ps 5 .024). The 5�7-year-old and the 8�9-year-old children equally

often made unilateral errors for bilateral targets. Further analyses for the

significant interaction between Age group and Target, F(2, 89)�3.70,

p�.029, hp2�.08, revealed that only the 8�9-year-olds made more

unilateral errors in the four-target subtask than in the two-target, subtask,F(1, 40)�5.13, p�.29, hp2�.11.

Reaction times (RTs). Figure 3D presents the reaction times (RTs) for

LVF and RVF in the VGSA subtasks with the SOA2 with two targets (2T)

and with four targets (4T) for each child age group. The general ANOVA for

reaction times showed a significant main effect for Age group, F(2,85)�7.52, p�.001, hp2�.15. The 5�7-year-olds had the slowest RTs,

which differed significantly from those of the older children (ps5.016).

There were no differences in RTs between the 8�9-year-olds and the 10�11-

year-olds.

Visual Go/No-Go spatial attention test (VGSA) for adults(digits)

Sensitivity values (d’). Figure 4A presents the sensitivity values (d’) forLVF and RVF in the VGSA subtasks with the SOA1 and the SOA2 with two

targets (2T) and with four targets (4T) for the two adult age groups. One-

Sample t-tests for each age group separately showed that the sensitivity

values (d’) differed significantly from the test value of zero (psB.001). Both

age groups were able to discriminate signals (targets) from noise (non-

targets) in all four VGSA subtasks. The general ANOVA for the sensitivity

values (d’) revealed that the 19�32-year-olds were significantly better in

discriminating the targets from the non-targets than the 59�79-year-olds,F(1, 67)�41.82, p B.001, hp2�.38. Decreasing the SOA, F(1, 67)�15.97,

VISUAL SPATIAL BIAS AND AGE 57

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

p B.001, hp2�.19, as well as increasing the number of the targets, F(1,

67)�34.23, pB.001, hp2�.34, decreased sensitivity. Further analyses of the

significant interaction between Target and SOA, F(1, 67)�6.90, pB.011,

hp2�.09, showed that at both SOA1 and SOA2, increasing the number of

targets from two to four decreased sensitivity*SOA1: F(1, 67)�33.33,

pB.001, hp2�.33; SOA2: F(1, 67)�20.36, pB.001, hp2�.23*but thechange was more radical at SOA1.

Decision criterion (c). Figure 4B presents the decision criterion (c)

values for LVF and RVF in the VGSA subtasks with SOA1 and SOA2 with

two targets (2T) and with four targets (4T) for the two adult age groups.

One-Sample t-tests for each age group separately showed that in both groupsthe decision criterion (c) differed significantly from the test value of zero

(psB.006) and that all values of c were positive: the decision criterion was

reasonably conservative and the participants had a bias rather not to

respond (correct rejection or miss) than to respond (correct response or false

alarm) in all four VGSA subtasks. In the general ANOVA for the decision

criterion (c), the 19�32-year-olds had significantly lower c values, F(1,

67)�15.64, p B.001, hp2�.19, than the older adult participants. The older

adults’ decision criterion was more conservative, and they were more biasedtowards not responding (miss or correct rejection) than the young adult

participants. Decreasing the SOA increased the decision criterion (c) F(1,

67)�34.88, pB.001, hp2�.34. Further analyses for significant interaction

between the SOA and Target, F(1, 67)�20.97, pB.001, hp2�.24, showed

that at SOA1, increasing the number of targets from two to four increased

the decision criterion (c), F(1, 67)�9.51, p�.003, hp2�.12, while at SOA2,

increasing the number of targets did not affect the decision criterion (c). In

other words, with the slower SOA, as the number of targets increased, theresponse criterion moved towards a more conservative direction. Such an

effect was not observed with the faster SOA.

Unilateral responses to bilaterally presented targets. Figure 4C presents

the unilateral responses to bilaterally presented targets for LVF and RVF in

the VGSA subtasks with SOA1 and SOA2 with two targets (2T) and withfour targets (4T) for the adult age groups. The general ANOVA for unilateral

responses to the bilateral targets showed that increasing the number of

targets that the participant needed to remember and detect from two to four

increased the unilateral errors for the bilateral targets, F(1, 65)�25.99,

pB.001, hp2�.29. The young adults were significantly better at detecting

bilateral targets than the older adults, F(1, 65)�33.20, pB.001, hp2�.34.

Further analyses for the significant interaction between the SOA and Target,

F(1, 65)�12.86, p�.001, hp2�.17, revealed that in both SOA1 and SOA2,increasing the number of targets increased the unilateral errors for bilateral

58 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

targets*SOA1: F(1, 67)�30.89, pB.001, hp2�.32; SOA2: F(1, 65)�5.79,

p�.019, hp2�.08*but the change was more radical at SOA1. More

unilateral responses to the bilateral targets were made to the right side than

to the left side, F(1, 65)�14.35, pB.001, hp2�.18. Further analyses for the

significant interaction between Age group and Visual Field, F(1, 65)�5.01,

p�.029, hp2�.07, showed that the main effects of Visual Field were

significant for both adult groups*19�32-year-olds: F(1, 34)�5.50, p�.025,

hp2�.14; 59�79-year-olds: F(1, 31)�9.00, p�.005, hp2�.23*but the

magnitude of the rightward bias was stronger for the older adults than for

the young adults. According to Wilcoxon Signed Ranks Test, young adults

made more unilateral responses to the right side than to the left side in both

VGSA subtasks with the SOA of 500-1500 ms (2 targets: Z��2.41,

p�.016; 4 targets: Z��2.00, p B.045), but there were no differences

between the left and right side in either of the VGSA subtasks with the SOA

of 300�800 ms. In the older adults the Wilcoxon Signed Ranks Test revealed

that the difference between the left and right unilateral responses to bilateral

targets was significant in all other subtasks except in VGSA with the SOA of

500�1500 ms with four targets: VGSA 500�1500 ms 2T (Z��2.95,

p�.003), VGSA 300�800 ms 2T (Z��2.79, p�.005) and VGSA 300�800 ms 4T (Z�2.18, p�.029). In other words the older adults more

frequently made right unilateral responses to bilateral targets than did the

young adults.

Reaction times (RTs). Figure 4D presents the reaction times (RTs) for

LVF and RVF in the VGSA subtasks with SOA1 and SOA2 with two targets

(2T) and with four targets (4T) for the adult age groups. The general

ANOVA for reaction times revealed that decreasing the SOA decreased the

reaction times, F(1, 66)�6.65, p�.012, hp2�.09, while increasing the

number of targets that the participant needed to remember and detect

increased the reaction times, F(1, 66)�94.83, pB.001, hp2�.59.

The correct responses to the RVF targets were significantly faster than the

responses to the LVF targets, F(1, 66)�17.62, pB.001, hp2�.21. The

analysis of the significant interaction between SOA and Age group, F(1,

66)�12.70, p�.001, hp2�.16, revealed that only the young adults’ reaction

times decreased when the SOA decreased, F(1, 35)�31.51, pB.001,

hp2�.47. Also, further analysis of the significant interaction between the

SOA and Target, F(1, 66)�8.44, p�.005, hp2�.11, showed that at both

SOA1 and SOA2, increasing the number of targets from two to four

decreased the reaction times, but the change was more radical at SOA1*SOA1: F(1, 66)�83.09, pB.001, hp2�.56; SOA2: F(1, 67)�44.04, pB.001,

hp2�.40.

VISUAL SPATIAL BIAS AND AGE 59

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Visual divided spatial attention subtask (VDSA)

Correct responses. Figure 5A presents the percentages of correctresponses made to the RVF, LVF, and BVF stimuli in the VDSA subtask

with the SOA of 750 ms for all age groups. The general ANOVA for the

correct responses in the VDSA with the SOA of 750 ms showed a significant

main effect for Age group, F(4, 179)�71.63, p B.001, hp2�.62, indicating

that all other age groups differed significantly from each other (ps 5 .042),

except the 10�11-year-olds and the 59�79-year-olds. The young adults made

the most and the 5�7-year-olds made the fewest correct responses. The main

effect for visual field, F(2, 358)�650.53, p B.001, hp2�.78, revealed that

fewest correct responses were made to the bilateral stimuli and the most

correct responses to the RVF stimuli (ps 5 .007). However, further analyses

Figure 4. Sensitivity values (d’), decision criterion (c) values, percentage of unilateral responses to

bilateral targets, and reaction times (RTs) in milliseconds for the left and the right side in the Visual

Go/No-Go spatial attention test (VGSA) in the adult age groups. The vertical bars represent the

Standard Error of the Mean (SEM).

60 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

of the significant interaction between the Visual Field and Age group, F(8,

358)�11,13, p B.001, hp2�.20, showed that, in all age groups, fewer

correct responses were made to the bilateral stimuli than to the unilateral

stimuli*5�7-year-olds: F(2, 54)�123.65, p B. 001, hp2�.82; 8�9-year-

olds: F(2, 80)�168.77, p B.001, hp2�.81; 10�11-year-olds: F(2,

52)�166.90, p B.001, hp2�.87; 19�32-year-olds: F(2, 96)�106.04,p B.001, hp2�.69; 59�79-year-olds: F(2, 76)�100.44, p B.001, hp2�.73.

In contrast to the other age groups, the 10�11-year-olds and the 59�79-year-

olds made most correct responses to the right unilateral stimuli (left vs. right

unilateral stimuli (ps 5 .007)), while in the other age groups there were no

significant differences between the correct responses to the left and right

unilateral stimuli.

Extra responses. Figure 5B presents the percentage of extra responses

made to the left and the right side in the VDSA subtask with the SOA of 750

ms for all age groups. The general ANOVA for the extra responses showed

that all age groups differed significantly from each other in the number of the

extra responses (ps 5 .011) and the 5�7-year-olds made the most and the

young adults the fewest extra responses, F(4, 180)�46.54, p B.001,

hp2�.51. More extra responses were made to the right than to the left

side, F(1, 180)�7.76, p�.006, hp2�.04. Visual inspection of Figure 3Breveals that this was not the case among all age groups. This finding was

confirmed with paired sample t-tests for each age group separately: only the

5�7-year-old children made significantly more extra responses to the right

side than to the left side, t(28)��2.20, p B.05.

Unilateral responses to bilateral stimuli. Figure 5C presents the percen-

tages of left and right unilateral responses to the bilateral stimuli in theVDSA subtask with the SOA of 750 ms for all age groups. The general

ANOVA for the unilateral responses to the bilateral stimuli showed a main

effect for Age group, F(4, 180)�33.65, p B.001, hp2�.43: all other

differences between the age groups were significant (ps 5 .023), except the

differences between the 5�7-year-olds and the 8�9-year-olds, between the 8�9-year-olds and the 10�11-year-olds, and between the 10�11-year-olds and

the 59�79-year-olds. The 19�32-year-old adults made the fewest, and the

children made the most unilateral responses to the bilateral stimuli. Moreunilateral responses to the bilateral stimuli were made to the right than to the

left side, F(1, 180)�19.10, p B.001, hp2�.10). In other words, the stimulus

in the LVF was missed more often than the stimulus in the RVF in the

bilateral stimulus condition.

Reaction times (RTs). Figure 5D presents the reaction times (RTs) forthe LVF and the RVF in the VDSA subtask with the SOA of 750 ms for all

VISUAL SPATIAL BIAS AND AGE 61

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Figure 5. Percentages of correct responses to left, right and bilateral stimuli, of extra responses, and of unilateral responses to bilateral stimuli, and reaction times

(RTs) in milliseconds for the left and the right side in the Visual divided spatial attention test (VDSA) with the SOA of 750 ms in all age groups. The vertical bars

represent the Standard Error of the Mean (SEM).

62

TA

KIO

ET

AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

age groups. The general ANOVA on RTs showed that the RTs to the right

were faster than the RTs to the left, F(1, 180)�6.93, p�.009, hp2�.04. The

significant main effect of Age group, F(4, 180)�55.11, p B.001, hp2�.55,

showed that the young adults’ RTs were the fastest and the two youngest

child groups’ RTs were the slowest (ps 5 .033). The RTs of the 5�7-year-olds

and 8�9-year-olds did not differ from each other, nor did the RTs of the

10�11-year-olds and the 59�79-year-old adults.

DISCUSSION

By applying fast-paced visual tasks, which put a sufficiently intensive load on

attention and working memory, we replicated the results of corresponding

auditory tasks (Takio et al., 2011) and demonstrated that solely rightward

spatial biases were observed for linguistic as well as for non-linguistic stimuli

in unilateral and/or bilateral presentation conditions. Furthermore, as

predicted, the incidence of the rightward spatial biases changed as a function

of age: they were more common in the children and in the older adult

participants than in the young adults.

With linguistic stimuli, all age groups were able to discriminate the targets

from the non-targets in both visual fields, and the decision criterion in all age

groups was reasonably conservative. Nevertheless, the children between the

ages of 5 and 9 years responded more often towards the right side than

towards the left side, irrespective of whether the right side stimulus was a

target or a non-target. In other words, their decision criterion was more lax

towards the right hemispace than towards the left hemispace. With non-

linguistic stimuli, the 5�7-year-olds responded more often towards the right

side than towards the left side, even irrespective of whether any stimulus was

presented on that side or not. The same kind of rightward biases as those

observed in the 5�7 and 8�9-year-old children were not observed in the

children between 10 and 11 years or in the adult participants. However, the

10�11-year-old children and the older adults detected the unilateral non-

verbal stimuli (dots) more often in the right than in the left visual field, thus

showing rightward spatial bias. When the dot was presented bilaterally, a

rightward spatial bias was observed in all age groups, whereas only the adult

participants showed a rightward spatial bias also for bilateral linguistic

(digit) stimuli. Interestingly, the older adults more frequently made right

unilateral responses to the bilateral linguistic targets than did the young

adults. Thus the cognitively more demanding bilateral stimulus condition

with linguistic stimuli induces stronger rightward bias in the older adult

participants than in the other participants. Moreover, increasing the

presentation speed (SOA) decreased the older adults’ performance more

than that of the other age groups.

VISUAL SPATIAL BIAS AND AGE 63

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

All our participants were right-handed and the possible motor right-hand

preference may partly explain the observed RTresults and perhaps some of the

rightward response bias in the 5�7-year-old and 8�9-year-old children (see

e.g., Goble & Brown, 2008). However, under intensive attentional load, the

stimuli in the right hemispace were also detected more accurately than the

stimuli in the left hemispace. This finding is consistent with the neuropsycho-

logical models proposing that attention is more strongly biased towards the

right hemispace (Heilman et al., 1987; Kinsbourne, 1987). Since the present

rightward spatial biases were independent of the stimulus type, we propose

that they were affected by the hemispheric asymmetry of attentional

mechanisms, producing right hemispace preference in healthy participants

in cognitively demanding tasks.A particular deficit called extinction can be observed in patients with right-

hemisphere damage during bilateral simultaneous stimulation: the patient

may be able to detect a single left-sided event in isolation, but in a bilateral

stimulus condition, the left-sided event is missed (for a review, see Driver &

Vuilleumier, 2001). Difficulties in becoming immediately aware of multiple

targets are also observed in normal healthy humans (for a review, see Driver &

Vuilleumier, 2001). Thus the spatial attentional bias appears when multiple

events compete for attention at the same time. The present findings on right-

side unilateral responses in bilateral stimulus conditions suggest that a mild

extinction-like phenomenon is present throughout the lifespan. Moreover, the

ability to distribute attention to multiple targets simultaneously decreases

especially in the course of ageing.

The present findings showed that the speed and efficiency of the

performance increased in childhood, were well developed in young adulthood,

and decreased again in old age (see also Ridderinkhof & van der Stelt, 2000;

Span, Ridderinkhof, & van der Molen, 2004). Similarly to what was observed

in the auditory tasks (Takio et al., 2011), in visual modality, the 5�7-year-olds’

performance level was inferior to that of older children, while the performance

level of 59�79-year-olds dropped occasionally to the same level as that of the

10�11-year-old children. The skills necessary for goal-directed behaviour

mature slowly during childhood, are well developed in adulthood and decline

as a function of ageing (Jurado & Rosselli, 2007; Luciana et al., 2005; Span

et al., 2004; Tsujimoto, 2008). Thus we propose that the present age-related

changes in the speed and efficiency of the performance and in the rightward

spatial bias are related to the development and decline of the executive control:

the inherent rightward spatial asymmetries are gradually balanced as the child

grows, are best controlled in young adulthood, and reappear as a function of

ageing. Strong asymmetries are not observed in young adults, with the

exception of mild asymmetries in specific bilateral stimulus conditions. Young

adults are probably better at overcoming the inherent rightward spatial biases

with the aid of their advanced executive functions (see Hugdahl et al., 2009;

64 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Posner, 2008; Posner & Raichle, 1994; Sætrevik & Specht, 2009). In childhood

the nature and the magnitude of the bias changed between the ages of 5 and 11

years. This indicates that, as the child develops, the more he/she is able to

inhibit responses that are not relevant for performing the tasks. The present

findings converge with the findings from our previous studies in auditory

modality (Takio et al., 2009, 2011) suggesting that some cognitive functions,

such as inhibition and ability to suppress task-irrelevant actions are relatively

well developed around the age of 10�11 years (for a review, see Hale, Bronik, &

Fry, 1997; Jurado & Rosselli, 2007). In old age the rightward spatial biases re-

emerge, especially in the more cognitively demanding bilateral stimulus

conditions. Perhaps in old age the asymmetrical bottom-up processes become

visible, especially in fast-paced perceptual tasks, due to the generalised slowing

of processing speed and the decline in executive functions.

In conclusion, the results showed that visual spatial biases occurred under

attentional load, they were solely towards the right side, and they changed as

a function of age. The age-related changes occurred presumably due to the

development and decline of executive functions. Since similar kinds of results

were also found in auditory modality (Takio et al., 2009, 2011), we propose

that the multimodal rightward spatial bias is related to the rightward

personal hemispace preference.

Manuscript received 28 March 2011

Revised manuscript received 20 July 2011

First published online 17 January 2012

REFERENCES

Anderson, V. A., Anderson, P., Northam, E., Jacobs, R., & Catroppa, C. (2001). Development of

executive functions through late childhood and adolescence in an Australian sample.

Developmental Neuropsychology, 20(1), 385�406.

Andersson, B., & Hugdahl, K. (1987). Effects of sex, age, and forced attention on dichotic listening

in children: A longitudinal study. Developmental Neuropsychology, 3(3/4), 191�206.

Boles, D. B., Barth, J. M., & Merrill, E. C. (2008). Asymmetry and performance: Toward a

neurodevelopmental theory. Brain and Cognition, 66, 124�139.

Callaert, D. V., Vercauteren, K., Peeters, R., Tam, R., Graham, S., Swinnen, S., et al. (2011).

Hemispheric asymmetries of motor versus nonmotor processes during (visuo)motor control.

Human Brain Mapping, 32(8), 1311�1329.

Callejas, A., Lupianez, J., Funes, M. J., & Tudela, P. (2005). Modulations among the alerting,

orienting and executive control networks. Experimental Brain Research, 167, 27�37.

Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M. P., & Shuman, G. L. (2000). Voluntary

orienting is dissociated from target detection in human posterior parietal cortex. Nature

Neuroscience, 3(3), 292�297.

Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain:

From environment to theory of mind. Neuron, 58, 306�324.

Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in

the brain. Nature Reviews. Neuroscience, 3, 201�215.

VISUAL SPATIAL BIAS AND AGE 65

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Dobler, V. B., Manly, T., Verity, C., Woolrych, J., & Robertson, I. H. (2003). Modulation of spatial

attention in a child with developmental unilateral neglect. Developmental Medicine & Child

Neurology, 45, 282�288.

Dolcos, F., Rice, H. J., & Cabeza, R. (2002). Hemispheric asymmetry and aging: Right hemisphere

decline or asymmetry reduction. Neuroscience and Biobehavioral Reviews, 26, 819�825.

Driver, J., & Vuilleumier, P. (2001). Perceptual awareness and its loss in unilateral neglect and

extinction. Cognition, 79, 39�88.

Everts, R., Lidzba, K., Wilke, M., Kiefer, C., Mordasini, M., Schroth, G., et al. (2009).

Strengthening of laterality of verbal and visuospatial functions during childhood and

adolescence. Human Brain Mapping, 30, 473�483.

Goble, D. J., & Brown, S. H. (2008). The biological and behavioural basis of upper limb

asymmetries in sensorimotor performance. Neuroscience and Biobehavioral Reviews, 32, 598�610.

Hale, S., Bronik, M. D., & Fry, A. F. (1997). Verbal and spatial working memory in school-age

children: Developmental differences in susceptibility to interference. Developmental Psychology,

33(2), 364�371.

Hamalainen, H., & Takio, F. (2010). Integrating auditory and visual asymmetry. In K. Hugdahl &

R. Westerhausen (Eds.), The two halves of the brain. Information processing in the cerebral

hemispheres (pp. 417�437). Cambridge, MA: MIT Press.

Heilman, K. M., Bowers, D., Valenstein, E., & Watson, R. T. (1987). Hemispace and hemispatial

neglect. In M. Jeannerod (Ed.), Neurophysiological and neuropsychological aspects of spatial

neglect (pp. 115�150). North-Holland: Elsevier Science Publishers BV.

Helland, T., & Asbjørnsen, A. (2001). Brain asymmetry for language in dyslexic children.

Laterality, 6(4), 289�301.

Hugdahl, K. (2003). Dichotic listening in the study of auditory laterality. In K. Hugdahl &

R. Davidson (Eds.), The asymmetrical brain (pp. 441�476). Cambridge, MA: MIT Press.

Hugdahl, K., & Andersson, L. (1986). The ‘‘forced-attention paradigm’’ in dichotic listening to

CV-syllables. A comparison between adults and children. Cortex, 22, 417�432.

Hugdahl, K., Carlsson, G., & Eichele, T. (2001). Age effects in dichotic listening to consonant-

vowel syllables: Interactions with attention. Developmental Neuropsychology, 20(1), 445�457.

Hugdahl, K., Westerhausen, R., Alho, K., Medvedev, S., Laine, M., & Hamalainen, H. (2009).

Cognition and neuroscience. Attention and cognitive control: Unfolding the dichotic listening

story. Scandinavian Journal of Psychology, 50, 11�22.

Ivry, R. B., & Robertson, L. C. (1998). The two sides of perception. Cambridge, MA: The MIT

Press.

Jurado, M. B., & Rosselli, M. (2007). The elusive nature of executive functions: A review of our

current understanding. Neuropsychology review, 17(3), 213�233.

Karrasch, M., Sinerva, E., Gronholm, P., Rinne, J., & Laine, M. (2005). CERAD test performances

in amnestic mild cognitive impairment and Alzheimer’s disease. Acta Neurologica Scandinavica,

11(3), 172�179.

Kimura, D. (1966). Dual functional asymmetry of the brain in visual perception. Neuropsychologia,

4, 275�285.

Kimura, D. (1967). Functional asymmetry of the brain in dichotic listening. Cortex, 3(2), 163�178.

Kinsbourne, 1987. Mechanisms of unilateral neglect. In M. Jeannerod, Neurophysiological and

neuropsychological aspects of spatial neglect (pp. 69�86). North-Holland: Elsevier Science

Publishers BV.

Laurent-Vannier, A., Pradat-Diehl, P., Chevignard, M., Abada, G., & De Agostini, M. (2003).

Spatial and motor neglect in children. Neurology, 60(2), 202�207.

Luciana, M., Conklin, H. M., Hooper, C. J., & Yarger, R. S. (2005). The development of nonverbal

working memory and executive control processes in adolescents. Child Development, 76, 697�712.

66 TAKIO ET AL.

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014

Macmillan, N. A., & Creelman, N. A. (2005). Detection theory. A user’s guide (2nd edition).

Cambridge, UK: Cambridge University Press.

McCartney, G., & Hepper, P. (1999). Development of lateralised behaviour in the human fetus from

12 to 27 weeks’ gestation. Developmental Medicine & Child Neurology, 41, 83�86.

Mondor, T. A., & Bryden, M. P. (1991). The influence of attention on the dichotic REA.

Neurospychologia, 29(12), 1179�1190.

Oldfield, R. C. (1971). The assessment and analysis of handedness. The Edinburgh inventory.

Neuropsychologia, 9, 97�113.

Poskiparta, E., Niemi, P., & Lepola, J. (1994). Diagnostiset testit 1: Lukeminen ja kirjoittaminen.

[Diagnostic Tests 1: Reading and Writing]. Finland: University of Turku.

Posner, M. I. (2008). Measuring alertness. Annals of the New York Academy of Sciences, 1129, 193�199.

Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of

Neuroscience, 13, 25�42.

Posner, M. I., & Raichle, M. E. (1994). Images of mind. New York: Scientific American Library.

Proverbio, A., Zani, A., Gazzaniga, M. S., & Mangun, G. R. (1994). ERP and RT signs of a

rightward bias for spatial orienting in split-brain patient. NeuroReport, 5, 2457�2461.

Ridderinkhof, K. R., & van der Stelt, O. (2000). Attention and selection in the growing child:

Views derived from developmental psychophysiology. Biological Psychology, 54, 55�106.

Sanders, L. D., Stevens, C., Coch, D., & Neville, H. J. (2006). Selective auditory attention in 3- to 5-

year-old children: An event-related potential study. Neuropsychologia, 44, 2126�2138.

Silven, M., Poskiparta, E., Niemi, P., & Voeten, M. (2007). Precursors of reading skill from infancy

to first grade in Finnish: Continuity and change in a highly inflected language. Journal of

Educational Psychology, 99, 516�531.

Span, M. M., Ridderinkhof, K. R., & van der Molen, M. W. (2004). Age-related changes in the

efficiency of cognitive processing across the life span. Acta Psychological, 117, 155�183.

Stanislaw, H., & Todorov, N. (1999). Calculation of signal detection theory measures. Behavior

Research Methods, Instruments. Computers, 31(1), 137�149.

Sætrevik, B., & Specht, K. (2009). Cognitive conflict and inhibition in primed dichotic listening.

Brain and Cognition, 71, 20�25.

Takio, F., Koivisto, M., Jokiranta, L., Rashid, F., Kallio, J., Tuominen, T., et al. (2009). The effect

of age on attentional modulation in dichotic listening. Developmental Neuropsychology, 34(3),

225�239.

Takio, F., Koivisto, M., Laukka, S. J., & Hamalainen, H. (2011). Auditory rightward spatial bias

varies as a function of age. Developmental Neuropsychology, 36(3), 1�21.

Telkemeyer, S., Rossi, S., Koch, S. P., Nierhaus, T., Steinbrink, J., Poeppel, D., et al. (2009).

Sensitivity of newborn auditory cortex to the temporal structure of sounds. The Journal of

Neuroscience, 29(47), 14726�14733.

Thomsen, T., Specht, K., Hammar, A., Nyttingnes, J., Ersland, L., & Hugdahl, K. (2004). Brain

localization of attentional control in different age groups by combining functional and

structural MRI. NeuroImage, 22(2), 912�919.

Trauner, D. A. (2003). Hemispatial neglect in young children with early unilateral brain damage.

Developmental Medicine & Child Neurology, 45, 160�166.

Tsujimoto, S. (2008). The prefrontal cortex: Functional neural development during early

childhood. The Neuroscientist, 14, 345�358.

Voyer, D. (2001). Reliability and magnitude of visual laterality effects: The influence of attention.

Laterality, 6(4), 315�336.

Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Ayden, M., & Von Leirer, O. (1983).

Development and validation of a geriatric depression scale: A preliminary report. Journal of

Psychiatric Research, 17(1), 37�49.

VISUAL SPATIAL BIAS AND AGE 67

Dow

nloa

ded

by [

Oul

u U

nive

rsity

Lib

rary

] at

05:

03 1

5 Fe

brua

ry 2

014