Effects of anxiety on children

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Effects of anxiety on memory storage andupdating in young children

Laura Visu-Petra,1

Lavinia Cheie,1

Oana Benga,1

andTracy Packiam Alloway2

Abstract

The relationship between trait anxiety and memory functioning in young children was investigated. Two studies were conducted, using

tasks tapping verbal and visual-spatial short-term memory (Study 1) and working memory (Study 2) in preschoolers. On the verbal storage

tasks, there was a detrimental effect of anxiety on processing efficiency (duration of preparatory intervals) on Word Span. Performance

effectiveness (memory span) did not differ between high-anxious and low-anxious children. In the second study, evaluating memory updat-

ing in a dual-task context, high-anxious children performed worse than low-anxious children on two verbal working memory tasks. There-

fore, when simple verbal storage is required, high-anxious children show only efficiency deficits; when executive demands are higher (i.e.,

verbal updating) both accuracy and efficiency are impaired. However, on the visual-spatial storage and updating measures, performance did

not differ between the two anxiety groups. The results are discussed in the context of the attentional control theory (Eysenck, Derakshan,Santos, & Calvo, 2007).

Keywords

anxiety, attentional control theory, preschoolers, short-term memory, updating, working memory

To date, the relationship between trait anxiety and general memory

functioning has been a controversial issue. Two lines of research

have been pursued: one investigating a content-specific (threat-

related) memory bias, another looking at memory for neutral infor-

mation. In the first case, clinical/high trait anxiety was found to

have a mixed (both facilitative and detrimental) impact on memory

for threat-related information, although several studies found noevidence for a memory bias specific to anxiety disorders (see

Mathews, Mackintosh, & Fulcher, 1997; Miu & Visu-Petra,

2009; Pine, 2007, for reviews).

A second line of research focused on the link between trait anxi-

ety and memory for emotionally neutral (i.e., non-threat-related)

stimuli in adult populations. There is evidence of anxiety-related

memory deficits for neutral stimuli when a high (executive) load

is imposed by task demands. Higher loads can be imposed by

increasing processing demands (Eysenck, 1985; Ashcraft & Kirk,

2001) or by using loading paradigms (Eysenck, Payne, & Derak-

shan, 2005; MacLeod & Donnellan, 1993; Derakshan & Eysenck,

1998). The attentional control theory (ACT; Eysenck, Derakshan,

Santos, & Calvo, 2007; Derakshan & Eysenck, 2009), an extension

of the processing efficiency theory (PET, Eysenck & Calvo, 1992),

describes the detrimental impact of anxiety on memory in light of

the central executive component in Baddeleys working memory

(WM) model (1986). The central executive is a domain-general

component responsible for the control of attention and processing

that is involved in a range of regulatory functions including the

retrieval of information from long-term memory (Baddeley,

Emslie, Kolodny, & Duncan, 1998). The temporary storage of

information is mediated by two domain-specific stores: the phono-

logical loop provides temporary storage of verbal material, and the

visuo-spatial sketchpad specializes in the maintenance and manip-

ulation of visual and spatial representations (see Baddeley & Logie,

1999, for a review).

Within the PET framework, it has been established that there is a

greater effect of anxiety on processing efficiency, commonly mea-

sured by the resources involved in solving the task (e.g., time, men-

tal effort), rather than on performance effectiveness, measured by

performance accuracy (Eysenck & Calvo, 1992).

According to the newer ACT, anxiety-related worrisome thoughts

create cognitive interference, affecting WM processing and storagecapacity by generating the need for auxiliary processes and strategies

to be activated. This interference affects the updating, inhibition, and

shifting functions of the central executive (Ansari, Derakshan, &

Richards, 2008; Derakshan, Ansari, Shoker, Hansard, & Eysenck,

2009; Derakshan & Eysenck, 2009). Memory updating in particular,

involves more than simple retention, relying on attentional control

in theactivemanipulationof representations(Miyake et al.,2000),and

so it is particularly susceptible to anxiety-related interference.

Additionally, a selective impairment of anxiety on verbal, but

not on visual-spatial memory tasks (Elliman, Green, Rogers, &

Finch, 1997; Ikeda, Iwanaga, & Seiwa, 1996) has been documen-

ted. This selective deficit is thought to be a consequence of inner

worrisome thoughts disrupting the functioning of the phonological

loop (Eysenck et al., 2007; Rapee, 1993). The detrimental effect of

1 Developmental Psychology Lab, Department of Psychology, Babes-Bolyai

University, Cluj-Napoca, Romania2 Centre for Memory and Learning over the Lifespan, Department of

Psychology, Stirling University, UK

Corresponding author:

Laura Visu-Petra, 37 Republicii Street, Developmental Psychology Lab,

Department of Psychology, Babes-Bolyai University, Cluj-Napoca, CJ

400015, Romania.

Email: [email protected]

International Journal of

Behavioral Development

110

The Author(s) 2010

Reprints and permissions:

sagepub.co.uk/journalsPermissions.nav

DOI: 10.1177/0165025410368945

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negative ruminations on phonological aspects of working memory

has been revealed in other contexts, such as solving mathematical

problems under stereotype threat (e.g., Beilock, Rydell, &

McConnell, 2007). However, it should be noted here that threat-

induced state anxiety (as opposed to the previously mentioned stud-

ies that targeted trait anxiety) has been related to a selective impair-

ment in visual-spatial working memory (Shackman et al., 2006).

An alternative theoretical account for the anxiety-related atten-tional biases for neutral information has recently been put forward

by Bishop (2009). The study supports the ACT prediction that trait

anxiety (even when controlling for current levels of state anxiety)

is characterized by impaired (in terms of efficiency) attentional/cog-

nitive control. However, a divergent claim is that this impairment is

most visiblein conditionswith low (perceptual)load, in which atten-

tional resources are only partially occupied. This allows salient dis-

tractors to compete for further processing, thus eliciting increased

demands for attentional control. In conditions with high (perceptual)

load, the processing requirements of the primary task terminate the

processing of distractors at an early stage, before their involvement

in response selection/working memory. Using a visual search para-

digm, the study shows that high trait-anxious individuals are slower

to identify targets in the presence of incongruent distractors underconditions of low (but not high) perceptual load. The findings are

explained by a processing stylecharacteristicof traitanxiety (regard-

less of thetype of information conveyed by the stimuli, i.e., threaten-

ing or not threatening), with difficulties in trial-to-trial alterations

when attentional resources arenot fully occupied by the task at hand.

This contrasts with the ACT claim that anxiety-related deficits

emerge as the task becomes more executively demanding.

Developmental research

In the context of early development, the relationship between

anxiety, memory and learning has been under-investigated (seeVisu-Petra, Ciairano, & Miclea, 2006, for a review). The few stud-

ies conducted with clinical populations (Gunther, Holtkamp, Jolles,

Herpertz-Dahlmann, & Konrad, 2004; Pine, Wasserman, & Work-

man, 1999; Toren et al., 2000; Vasa et al., 2007) and with non-

clinical, high-anxious children (Hadwin, Brogan & Stevenson,

2005; Owens, Stevenson, Norgate, & Hadwin, 2008; Visu-Petra,

Miclea, Cheie, & Benga, 2009; Visu-Petra, T incas, Cheie, &

Benga, 2010) have found mixed evidence of impaired memory for

neutral information. For example, no concurrent relationship was

found between state anxiety and short-term memory (STM) effec-

tiveness, although high-anxious school-age children reported

increased mental effort (reduced efficiency) in solving the Digit

Span task when compared to low-anxious children (Hadwin, Bro-

gan, & Stevenson, 2005). In preschoolers, trait anxiety was a long-itudinal predictor of a marginal impairment in performance

effectiveness on the same Digit Span (Visu-Petra et al., 2009) and

of processing efficiency (duration of preparatory intervals and

interword pauses) on Word and Nonword Span. No impact of anxi-

ety on spatial WM was found in preschoolers (Visu-Petra et al.,

2010). Anxiety-related verbal, but not visual-spatial, WM impair-

ments were found in 910-year-olds with high state anxiety in terms

of processing efficiency (total response time; Hadwin, Brogan, &

Stevenson, 2005), and in 1112-year-olds with high trait anxiety

in terms of processing effectiveness (Owens et al., 2008).

The educational implications of investigating this relationship

are paramount, especially when considering the variety of learning

and academic difficulties associated with childhood anxiety

(Phillips, Pitcher, Worsham, & Miller, 1980; Rabian & Silverman,

2000; Woodward & Fergusson, 2001). Moreover, recent research

on school-age children (1112 years) established that verbal WM

accuracy was a mediator between trait anxiety and academic perfor-

mance (Owens et al., 2008).

Current study

The aim of the present study was to investigate early precursors

of anxiety-related memory impairments for neutral information

by focusing on an under-investigated developmental period

(37 years). There were several issues of interest. The first issue

was whether the same pattern observed in adults of greater

anxiety-related impairments in processing efficiency (response

time), as compared to effectiveness (accuracy), would be evidenced

in this young age group as well.

Next, we also addressed the issue of whether the potential detri-

mental effect of anxiety on performance effectiveness would be

evidenced in both STM tasks (Study 1) and WM tasks (Study 2).

In line with the ACT, we would expect that trait anxiety would only

impact the executive demanding WM tasks, and not the STM tasks,

which require simple storage of information.

Finally, we were interested in whether anxiety would negatively

impact performance on verbal tasks compared to visual-spatial

ones. This issue relates to the particular underlying structure of

working memory early in development, as young children rely

more on executive resources when performing visuo-spatial tasks

(Alloway, Gathercole, & Pickering, 2006).

To summarize, we hypothesized that: (1) performance effective-

ness on the memory storage tasks would not be affected by anxiety;

(2) processing efficiency on both the memory storage and updating

tasks would be negatively affected by anxiety; and (3) the detrimen-

tal effects of anxiety would be visible on the verbal, but not on the

visual-spatial memory storage and updating tests.

Study 1

In the developmental literature, (state) anxiety and STM effective-

ness were found to be unrelated, although high-anxious school-age

children reported reduced efficiency (increased mental effort) in

solving the Digit Span task when compared to low-anxious children

(Hadwin, Brogan, & Stevenson, 2005). In preschoolers, trait anxi-

ety was a longitudinal predictor of a marginal impairment in perfor-

mance effectiveness on the Digit Span task (Visu-Petra et al., 2009)

and of processing efficiency (duration of preparatory intervals and

interword pauses) on Word and Nonword Span tasks.

The first study evaluated both performance effectiveness (mem-

ory span) and processing efficiency (total response time) on verbal

and visual-spatial STM tasks. Our hypotheses were that at this low

level of executive demands, trait anxiety would not impact

performance effectiveness. However, some impairment might be

noted at the level of processing efficiency of verbal, but not

visual-spatial, STM.

Method

Participants

Our sample consisted of 116 preschoolers (50 girls) with an age

range between 3.1 years and 7.4 years (mean age 62 months,

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Study 2In the developmental literature, anxiety-related verbal (but not

visual-spatial) WM impairments were found in 910-year-olds with

high state anxiety (Hadwin, Brogan, & Stevenson, 2005) in terms of

processing efficiency (total response time), and in 1112-year-olds

with high trait anxiety (Owens et al., 2008) in terms of performance

effectiveness. The latter study used the AWMA (Alloway, 2007)

and found that verbal WM significantly mediated the relationship

between trait anxiety and academic performance, revealing the edu-

cational relevance of investigating memory updating in children

with anxiety. No impact of anxiety on spatial WM was found in pre-

schoolers (Visu-Petra et al., 2010).

Oursecond designinvolved a more extensivecollection of verbaland visual-spatial tests from the Automated Working Memory

Assessment battery (AWMA, Alloway, 2007), targeting younger

children than those in previous studies. Theaim wasto test forpoten-

tial anxiety-related working memory impairments in both effective-

ness and efficiency measures. An indirect index of precision

(childrens accuracy on the secondary task) was taken to represent

a potential measure of efficiency, as the AWMA does not record

response time. Ourhypothesis wasthat at this high level of executive

load imposed by the memory-updating demands of the tasks, both

performance effectiveness and processing efficiency would be

affected by higher levels of trait anxiety. This effect would only be

visible on the verbal, and not on the visual-spatial WM tasks.

Figure 2. Mean response times (performance efficiency) for the HA and LA groups on Word span, for list lengths (LLs) of 2 and 3 words.

Figure 1. Mean memory span (performance effectiveness) for the HA and LA groups on the verbal and visual-spatial STM tasks.



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Method

Participants

In the second study, 98 preschoolers (45 girls) were tested, with an

age range between 4.6 years and 7.4 years (mean age 68 months,

SD 9). The children were classified as LA (N 49; mean Spence

score 16.12,SD 6.16), or HA (N 49; mean Spence score

38.85,SD 9.41), based on the median split of parental ratings ofthe childrens anxiety symptoms (median was 26.5). The two result-

ing groups differed in the Spence score,F(1, 96) 200.03,p < .01,

partial Z2 .67, but did not differ in age, F(1, 96) 1.70, n.s.

(mean age for LA 67 months, SD 9, and mean age for HA

69 months, SD 9) or intelligence, F(1, 96) .34, n.s. (mean

IQ for LA 97.57, SD 9.23, and mean IQ for HA 96.32,

SD 11.62), measured with the Raven Colored Progressive

Matrices test (Raven, 1986). All 98 children completed the Odd-

one-out task, 97 completed the Mr. X, Counting Recall and Back-

ward Digit Recall tasks, and 91 the Listening Recall task.

MeasuresThe Colored Progressive Matrices test (CPM, Raven, 1986) with

norms for the Romanian population (Dobrean, Rusu, Comsa, &

Balazsi, 2005) was used as an estimate of the childs general intel-

ligence level. During its unfolding, a booklet with 36 items is

shown to the child; the total number of correct responses generated

the IQ score.

We used the Romanian version of AWMA (Visu-Petra, 2008), a

standardized battery for the assessment of verbal and visual-spatial

WM in children (ages 411). All tests (except Backward Digit

Span) contained a primary memory task (the child had to update

memory representations in order to remember an increasingly long

sequence of items) and a secondary processing task (similar/dissim-

ilar or false/true judgments for each of the to-be-remembereditems).

Threeverbal WMmeasures were administered: Counting, Lis-

tening and Backward Digit Recall. In the Counting Recall test, the

child was presented with a visual array of red circles and blue tri-

angles; he/she was required to count the number of circles in an

array and to recall the totals from gradually increasing numbers

of arrays. In the Listening Recall task, the child was presented with

a series of short sentences, judged the veracity of each sentence in

turn by responding yes/no, and then recalled the final word of

each sentence in sequence. In the Backward Digit Recall, the child

was asked to recall a gradually increasing sequence of spoken digits

in the reverse order.

Two visual-spatial WM tasks were administered: Odd-one-out

and Mr. X. The Odd-one-out task presented the child with threeshapes, each in a box, displayed in a row. He/she was required to

point the odd-one-out shape in each row. Subsequent arrays with

increasing number of such rows appeared. Each array was dis-

played on the computer for 2 seconds. At the end of each trial

(array), the child recalled the location of each previously identified

odd-one-out shape, in the correct order, by tapping on a row with

three empty boxes. In the Mr. X task two fictitious cartoon figures,

presented as Mr. X, were displayed. The child was first asked to

identify whether Mr. X with the blue hat is holding the ball in the

same hand as Mr. X with the yellow hat or not (the secondary task

required a mental rotation). With increasing task difficulty, more

Mr. Xs appear on each trial and the child is required to perform the

mental rotation and to subsequently recall the location of each ball

by pointing to a picture with six compass points.

Procedure and scoring

All WM tasks were administered individually using a laptop, in one

session lasting on average 30 minutes. The AWMA test trials were

presented as a series of blocks, each block consisting of six trials.According to the move on rule, once the child responded cor-

rectly to the first four trials within a block of trials, the program

automatically proceeded to the next block and credited the tasks

that were not administered. If three errors were made within a block

of trials, the test administration stopped.

Two indices were analyzed for each task: (1) a memory score

(performance effectiveness): the total number of recalled items

from the primary memory task; (2) precision scores: performance

accuracy on the secondary task. The AWMA does not record

response times, which would offer a comparable processing effi-

ciency index to Study 1. However, as processing efficiency is

defined by the resources involved in solving a task, we considered

that the precision score on the secondary task would provide an

indirect measure of processing efficiency, i.e., the more resourcesthe child is investing in the primary (memory) task, the less he will

perform on the secondary task.

Results

Figure 3 shows the mean memory scores (performance effective-

ness) for the HA and LA groups on the verbal and visual-spatial

WM tasks. We conducted a MANCOVA with the memory scores

from the five WM tasks as dependent variables and with Anxiety

Group (HA and LA) as a between-subject factor. Age and nonver-

bal ability were included as covariates here and in all subsequent

analyses. The results indicated a significant effect of Group on theWM tests, Wilks lambda .83, F(5, 83) 5.61, p < .01, partial

Z2

.25. Univariate ANOVAs showed that the differences

between anxiety groups were significant for the verbal tasks: Back-

ward Digit Recall, F(1, 91) 9.6, p .003, partial Z2 .10 and

Listening Recall, F(1, 91) 10.76, p < .01, partial Z2 .15, but

not Counting Recall, F(1, 91) .81, n.s. On both tasks, HA

(M5.51, SD 3.79 for Backward Digit Recall, andM 6.60,

SD 5.70 for Listening Recall) had lower scores than LA (M

7.45,SD 3.49, andM 9.66,SD 3.03, for Backward Digit and

Listening Recall, respectively).

None of the two visual-spatial WM tasks was impacted by anxi-

ety,F(1, 91) .02,n.s., for Odd-one-out, andF(1, 91) .59,n.s.,

for Mr. X. The analysis was repeated without controlling for non-

verbal ability (Raven IQ), because this measure draws uponvisual-spatial resources, and by treating it as a covariate we might

have partialled out some of the variance we were interested

in. However, the effect of Anxiety Group remained non-

significant, F(1, 91) .00, n.s., for Odd-one-out, andF(1, 91)

1.39, n.s., for Mr. X.

Childrens precision on the secondary task was considered an

indirect measure of processing efficiency. A MANCOVA with

WM processing scores as dependent variables and Group (HA vs.

LA) as a between-subjects variable revealed a main effect of group

on WM processing scores, Wilks lambda .78,F(4, 84) 5.74,p

< .01, partialZ2 .21. Univariate ANOVAs showed that this effect

was significant only for Listening Recall,F(1, 91) 20.71,p< .01,

Visu-Petra et al. 5


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partial Z2 .19 (similar results were obtained when IQ was

removed from the analyses). Again, HA had lower scores than

LA (M 13.63, SD 10.51 for HA, andM 22.18, SD 7.56

for LA).

The findings revealed detrimental effects of trait anxiety on per-

formance accuracy in the case of two verbal WM tasks. Processing

efficiency, as measured by processing accuracy on the secondary

task, was also affected in one verbal WM task. This pattern mirrors

that reported in adult data: anxiety affects only verbal WM, but not

visual-spatial WM performance in preschool children.

General discussionTo our knowledge, the present study provides the first investigation

of anxiety-related memory storage and updating impairments in a

very young age group (37 years). Based on parental reports of the

childs trait anxiety level, preschool children were classified as high

or low trait-anxious. Children were tested with verbal and visual-

spatial STM and WM measures. On these tests, performance effec-

tiveness (accuracy) and processing efficiency (resources used to

solve a primary task, such as response times study 1, and accuracy

on a secondary task study 2), were computed. Results revealed

that when simple verbal storage was required, high-anxious chil-

dren showed only efficiency deficits; when executive demands

were higher (i.e., verbal updating) both efficiency and accuracy

were impaired. However, on the visual-spatial storage and updatingmeasures, performance did not differ between the two anxiety

groups.

The main research questions revolved around the relationships

between anxiety and performance index (efficiency vs. effective-

ness), executive load (STM vs. WM), and stimulus modality (verbal

vs. visual-spatial). First, we tried to replicate the classical

efficiency-effectiveness distinction in a younger sample. The aim

was to reveal that although performance effectiveness is not neces-

sarily impaired by anxiety, processing efficiency can be altered by

higher trait anxiety levels. Two more anxiety-related interactions

were postulated. Anxiety was predicted to have a stronger impact

upon the executive demanding WM tests, than on the simple

storage demanding STM tests. Second, anxiety would have a stron-

ger impact upon the verbal, than upon the visual-spatial memory

measures. It would have been ideal to test all three interactions

within a single design. However, the STM and WM tests were not

equivalent, and the (more difficult) WM tests could only be admi-

nistered to older children. Therefore, two studies were conducted,

testing memory storage and updating, respectively. Within each

study, we looked at the impact of anxiety on efficiency vs. effec-

tiveness, and on verbal vs. visual-spatial measures.

In the first study, five verbal and visual-spatial STM tasks were

used, and indexes of performance effectiveness and processing effi-

ciency were calculated (the latter only for the verbal measures).

While performance effectiveness was unaffected on all STM mea-

sures, processing efficiency was reduced in HA children on Word

Span, as revealed by their longer preparatory intervals. In the sec-

ond study, five verbal and visual-spatial WM tasks from the

AWMA battery were used, and performance effectiveness, as well

as an indirect measure of efficiency, were assessed. Trait anxiety

had a negative impact upon performance effectiveness on two of

the three verbal WM measures and upon the indirect measure of

processing efficiency on one of these two verbal tasks. No

anxiety-related impairment in visual-spatial STM or WM perfor-

mance was evidenced.

Several implications regarding the impact of anxiety on memory

storage and updating in very young children emerge from these

findings. First, looking at performance effectiveness, anxiety hada detrimental impact only on executive demanding WM tasks, and

not on STM tests. This pattern is in line with previous findings from

studies with adults (see Eysenck et al., 2007, for a review) and older

children (Hadwin, Brogan, & Stevenson, 2005, but see Visu-Petra

et al., 2009, for longitudinal evidence of the predictive role of trait

anxiety on Digit Span accuracy). According to ACT, anxious indi-

viduals should show impaired performance in dual-task situations

in which the concurrent demands of the two tasks on the central

executive are high (Derakshan & Eysenck, 2009). In simple recall

tasks with little executive demands, they would compensate for the

adverse effects of anxiety on processing efficiency by activating

additional processing resources (Eysenck et al., 2007). Indeed,

Figure 3. Mean memory span (performance effectiveness) for the HA and LA groups on the verbal and visual-spatial WM tasks.



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there was an impact of trait anxiety on the storage-plus-processing

WM tasks, but not on the storage-only STM tasks. However, a cau-

tionary note should be re-stated: the STM and WM tasks cannot be

directly contrasted, as they are not equivalent (the storage demands

of the WM tasks are not identical to the ones on the STM task).

Our second hypothesis regarding the detrimental impact of trait

anxiety on processing efficiency could only be tested in the first

study, and was confirmed in the case of verbal STM tasks (WordSpan). HA children took longer than their LA counterparts to pre-

pare their initial responses and tended to have longer interword

pauses during the same LL2 responses. This pattern is in line with

previous findings of an anxiety-related STM impairment in pro-

cessing efficiency, translated as increased reported mental effort

on a digit span task (Hadwin, Brogan, & Stevenson, 2005), or as

longer preparatory intervals on word and nonword recall

(Visu-Petra et al., 2009). Such an effect could be explained by HA

childrens need to mobilize additional resources in order to perform

the memory scanning operations that take place during the prepara-

tory intervals and interword pauses (Cowan et al., 1998), in order to

overcome anxiety-related interfering thoughts. However, the pres-

ence of this effect on the lower, but not on the higher list lengths

could provide indirect evidence for the hypothesis of an anxiety-related deficit under conditions of lower (in this case memory, not

perceptual) load (Bishop, 2009), allowing the child to be more sub-

jected to distractors (interfering thoughts) than in conditions with

higher load, which generate a more task-focused performance.

Unfortunately, the lack of an efficiency (response time) index on

theworking memorytasksdid notallowus to further test this hypoth-

esis across different list lengths in the updating context. However,

anxiety-related impairments on the secondary task from the WM

tests were hypothesized. We used an indirect measure of processing

efficiency, the childs precision in solving the concurrent (simple,

almost automatic) task, hypothesizing that it would be impaired to

a greater degreein HA children as they allocate more resourcesto the

primary task. However, the detrimental effect of anxiety was onlynoted on the precision index from Listening Span, a task which

required the child to listen and to decide on the veracity of a series

of sentences as a secondary task (the primary memory task being

to remember the last word from each sentence). Indeed, this require-

mentof a true/falsejudgmentmight have imposed greater processing

demands than simple same/different or odd-one-out judgments

required by the visual-spatial tasks, or the by now automatic

counting demand imposed by the secondary verbal task from

Counting Recall. Therefore, it might have been subject to greater

interference from anxiety-related intruding thoughts.

Finally, we evaluated the verbal vs. visual-spatial nature of the

anxiety-related memory impairments. The two studies were

consistent in revealing an impairment in efficiency (on the Word

Span STM task and on the Listening Recall WM task) and ineffectiveness (on the Backward Digit Recall and Listening Recall

WM tasks) on the verbal tasks. There were no anxiety-related

impairments on the visual-spatial STM and WM tasks (actually

HA outperformed LA participants on the Corsi Blocks Test). This

extends previous findings of a selective anxiety-related verbal

impairment from adult (Elliman et al., 1997; Ikeda, Iwanaga, &

Seiwa, 1996) and developmental research (Hadwin, Brogan, &

Stevenson, 2005; Toren et al., 2000). This could be explained by the

effect of anxiety-related inner thoughts on the phonological loop,

rather than on the visual-spatial sketchpad. This selective verbal

effect is revealed in a sensitive period (37 years), in which the

fractionation of the WM system into verbal and visual-spatial

components is still developing (Tsujimoto, Kuwajima, &

Sawaguchi, 2007). It appears that the developmentally specific

executive-demanding nature of the visual-spatial tasks did not

differentially affect high- and low- anxious preschoolers. Even

at this early age, the interference of worrisome thoughts appears

to primarily affect verbal, not visual-spatial measures, although

the latter might be more executive-demanding during this devel-

opmental period (Alloway, Gathercole, & Pickering, 2006).What are the potential mechanisms responsible for the detrimen-

tal effects of trait anxiety on the updating of neutral, not threat-

related elements? Different attentional and memory accounts for

anxiety-related memory impairments have been proposed at differ-

ent stages of information processing. An encoding explanation

would suggest that subjects with higher levels of trait anxiety do not

attend sufficiently to the presented stimuli and do not encode them

efficiently (Visu-Petra et al., 2009). However, this effect should be

present across different list lengths and should primarily affect per-

formance effectiveness. Our data suggest that performance effec-

tiveness is unimpaired in STM tasks and that efficiency is

compromised only at the initial stages of recall (preparatory inter-

vals for the first list length). An alternative would be that

anxiety-induced worrisome thoughts interfere with the memoryupdating processes, compromising online rehearsal and mainte-

nance of information. This proposal is supported by the selective

impact of trait anxiety on WM, but not on STM measures. Neuro-

biological research has pinpointed both the underpinnings of the

link between anxiety and higher-level executive performance

(Derakshan & Eysenck, 2009; Fales et al., 2008; Pine & Monk,

2008). Finally, a third possible account would rely on retrieval-

induced effects. High-anxious children have been shown to have

less confidence in their answers and to underestimate (in anticipa-

tion) the accuracy of their cognitive performance (Kendall &

Chansky, 2001; Spence, Donovan, & Brechman-Toussaint, 1999).

This would explain their longer preparatory intervals, but this effect

should appear across tasks and not be directly influenced by thelevel of task complexity. Unfortunately, the lack of response timing

measures in the second study does not allow a direct comparison to

test for the presence of anticipatory anxiety effects on WM tasks.

The three proposals are not mutually exclusive; distinct anxiety-

related attentional and memory effects being likely to affect differ-

ent stages of information-processing (Pine, 2007). However, it is

clear that although encoding explanations are appealing, they

alone cannot account for the variety of memory effects (and com-

pensatory strategies) related to childhood anxiety (Daleiden, 1998).

From a developmental perspective, the age groups investigated

(37 years in Study 1, and 4.57 years in Study 2) are at the conflu-

ence of several remarkable progressions. Brain maturation, through

processes of focalization and frontalization (Zelazo, Carlson,

& Kesek, 2008), is accompanied by the development of executivefunctioning, in general, and of memory functioning, in particular.

The underlying cognitive structure for working memory appears

to be in place in children as young as 4 years, consisting of a

domain-general working memory factor, and two domain-specific

(verbal and visual-spatial) storage factors (Alloway, Gathercole,

& Pickering, 2006). This structure is consistent across childhood

and adolescence, although memory capacity per se shows steady

improvements in accuracy. How do increased levels of anxiety

relate to the ongoing memory development in this very young age

group? Identifying adult-like anxiety-related updating biases for

non-emotional information suggests a developmental continuity

model, supported by (the few existing) neurobiological and/or

Visu-Petra et al. 7


8/10

behavioral evidences. In adults, a concurrent mediation of anxiety

and memory by the ventromedial prefrontal cortex and medial tem-

poral regions has been documented (Shu, Wu, Bao, & Leonard,

2003; Wall & Messier, 2000). There is similar evidence from pedia-

tric neuroimaging data suggesting medial temporal lobe dysfunc-

tion in social phobia and other anxiety disorders (McClure et al.,

2004; Thomas et al., 2001), which could underlie both memory def-

icits and anxiety disorders (Vasa et al., 2007). However, it is yet notdocumented whether such a neurobiological account could be valid

in the case of non-clinical, high trait anxiety. An alternative, beha-

vioral account has been described above, relying on attentional/

memory peculiarities in information processing in high-anxious

children. The behavioral evidence suggests that very young chil-

dren in non-clinical samples (2.56.5 years) experience a variety

of worries (Spence et al., 2001), and that the tendency to worry

excessively is relatively stable across childhood years (Weems,

2008). It is plausible to consider that, in the stressful context of test-

ing, children with higher levels of trait anxiety have produced more

attentional shifts towards internally or externally generated (evalua-

tion) threat stimuli, resulting in encoding/maintenance/retrieval

deficiencies. Unfortunately, there are few attempts to provide uni-

tary frameworks for cognitive functioning in childhood anxiety,which could bring together both neurobiological and behavioral

evidences in an information-processing perspective (but see Pine,

2007, for such an attempt).

Among the limitations of the present study, important aspects

would be our reliance on parental reports of trait anxiety and the

lack of a self-reported measure of state anxiety. However, it has

been shown that it is difficult to reliably assess state anxiety using

self-reports in children until 7 or 8 years of age (Schniering, Hud-

son, & Rapee, 2000) and that there is a high degree of congruence

between trait and state anxiety in potentially stressful situations,

like cognitive testing (Lau, Eley, & Stevenson, 2006). Another lim-

itation relates to the lack of a processing efficiency index in the

WM tasks. It is for further research to investigate the presence ofa comparable effect to the one noted in STM tasks in young chil-

dren. Based on ACT findings, it is presumable that such an effect

would be even stronger than effectiveness impairments if response

time on verbal WM tasks were evaluated.

To conclude, we return to our main research questions. In pre-

schoolers, the results of our investigation have supported the ACT

predictions of anxiety-related impairments: (1) on the accuracy of

updating (WM tests), and not of simple memory storage (STM

tests); (2) on processing efficiency indexes from the STM tasks

(although response timing is not usually assessed when measuring

memory span); and (3) on verbal, but not on visual-spatial mea-

sures. Further research should validate the effects of anxiety on pro-

cessing efficiency measures in the WM tasks, and examine

additional efficiency indexes complementary to the informationprovided by response times, such as subjective mental effort, or

(in)sensitivity to reward (Eysenck & Calvo, 1992). Based on such

a complex information processing perspective, these results would

help elaborate prevention programs targeting memory functioning

in young children with high anxiety levels (see Daleiden and Vasey,

1997, for a similar proposal).

Acknowledgments

The authors are grateful to Irina Bulai for her help with the data col-

lection and to the children and kindergarten staff for their

collaboration.

Funding

This work was partially supported by the National University

Research Council (PN-II-RU-PD-2009/427 Grant awarded to the

first author) and by the Sectorial Operational Programme for

Human Resources Development (Invest in people POSDRU/6/

1.5/S/4 Grant awarded to the second author).

References

Alloway, T.P. (2007). Automated Working Memory Assessment

(AWMA). London: Pearson Assessment.

Alloway, T.P., Gathercole, S.E., & Pickering, S.J. (2006). Verbal and

visuo-spatial short-term and working memory in children: Are they

separable?Child Development, 77, 16981716.

Ansari, T.L., Derakshan, N., & Richards, A. (2008). Effects of anxiety

on task-switching: Evidence from the mixed antisaccade task.Cog-

nitive, Affective, and Behavioural Neuroscience, 8, 229238.

Ashcraft, M.H., & Kirk, E.P. (2001). The relationships among working

memory, math anxiety and performance. Journal of Experimental

Psychology: General, 2, 224237.

Baddeley, A.D. (1986). Working memory. Oxford: Oxford University

Press.Baddeley, A.D., Emslie, H., Kolodny, J., & Duncan, J. (1998). Random

generation and the executive control of working memory. Quarterly

Journal of Experimental Psychology: Human Experimental Psy-

chology, 51A, 819852.

Baddeley, A.D., & Logie, R.H. (1999). Working memory: The multiple

component model. In A. Miyake & P. Shah (Eds.), Models of work-

ing memory. New York: Cambridge University Press.

Beilock, S.L., Rydell, R.J., & McConnell, A.R. (2007). Stereotype

threat and working memory: Mechanisms, alleviation, and

spill over. Journal of Experimental Psychology: General, 136,

256276.

Benga, O., T incas, I. & Visu-Petra, L. (2010). Investigating the struc-

ture of anxiety symptoms among Romanian preschoolers using theSpence Preschool Anxiety Scales. Cognition, Brain, Behavior. An

Interdisciplinary Journal,14, 159182.

Bishop, S.J. (2009). Trait anxiety and impoverished prefrontal control

of attention. Nature Neuroscience, 12, 9298.

Cowan, N., Keller, T., Hulme, C., Roodenrys, S., McDougall, S., &

Rack, J. (1994). Verbal memory span in children: Speech timing

clues to the mechanisms underlying age and word length effects.

Journal of Memory and Language, 33, 234250.

Cowan, N., Towse, J.N., Hamilton, Z., Saults, J.S., Elliott, E.M., Lacey,

J.F., Moreno, M.V., & Hitch, G.J. (2003). Childrens working-

memory processes: A response-timing analysis. Journal of Experi-

mental Psychology: General, 132, 113132.

Cowan, N., Wood, N.L., Wood, P.K., Keller, T.A., Nugent, L.D., &

Keller, C.V. (1998). Two separate verbal processing rates contribut-ing to short-term memory span. Journal of Experimental Psycho-

logy: General, 127, 141160.

Daleiden, E.L. (1998). Childhood anxiety and memory functioning:

A comparison of systemic and processing accounts. Journal of

Experimental Child Psychology, 68, 216235.

Daleiden, E.L., & Vasey, M.W. (1997). An information-processing per-

spective on childhood anxiety. Clinical Psychology Review, 17,

407429.

Derakshan, N.,Ansari,T.L., Shoker, L.,Hansard, M.E., & Eysenck,M.W.

(2009). Anxiety, inhibition, efficiency, and effectiveness: An

investigation using the antisaccade task. Experimental Psychology,

56, 4855.



9/10

Derakshan, N., & Eysenck, M.W. (1998). Working memory capacity in

high trait-anxious and repressor groups.Cognition and Emotion,12,

697713.

Derakshan, N., & Eysenck, M.W. (2009). Anxiety, processing

efficiency, and cognitive performance: New developments from

attentional control theory. European Psychologist,14(2), 168176.

Dobrean, A., Rusu, C., Comsa, M., & Balazsi, R. (2005). Standardi-

zarea pe populatia Romaniei a testului Matrici Progresive RavenColor Forma Paralel. In J. Raven, J.C. Raven, & J.H. Court (Eds.),

Manual Raven: Sectiunea 2, Matrici Progresive Color. Cluj-

Napoca: Editura ASCR.

Elliman, N.A., Green, M.W., Rogers, P.J., & Finch, G.M. (1997). Pro-

cessing efficiency theory and the working memory system: Impair-

ments associated with subclinical anxiety. Personality and

Individual Differences, 23, 3135.

Eysenck, M.W. (1985). Anxiety and cognitive-task performance. Per-

sonality and Individual Differences, 6, 57586.

Eysenck, M.W., & Calvo, M.G. (1992) Anxiety and performance: The

Processing Efficiency Theory.Cognition and Emotion, 6, 409434.

Eysenck, M.W., Derakshan, N., Santos, R., & Calvo, M.G. (2007).

Anxiety and cognitive performance: The attentional control theory.

Emotion, 7, 336353.Eysenck, M.W., Payne, S., & Derakshan, N. (2005). Trait anxiety,

visuospatial processing, and working memory. Cognition and Emo-

tion, 19(8), 12141228.

Fales, C.L., Barch, D.M., Burgess, G.C., Schaefer, A., Mennin, D.S.,

Gray, J.R., & Braver, T.S. (2008). Anxiety and cognitive efficiency:

Differential modulation of transient and sustained neural activity

during a working memory task. Cognitive, Affective & Behavioral

Neuroscience, 8, 239253.

Gunther, T., Holtkamp, K., Jolles, J., Herpertz-Dahlmann, B., &

Konrad, K. (2004). Verbal memory and aspects of attentional con-

trol in children and adolescents with anxiety disorders or depressive

disorders. Journal of Affective Disorders, 82, 265269.

Hadwin, J., Brogan, J., & Stevenson, J. (2005). State anxiety and work-

ing memory in children: A test of processing efficiency theory. Edu-

cational Psychology, 25(4), 379393.

Ikeda, M., Iwanaga, M., & Seiwa, H. (1996). Test anxiety and working

memory system. Perceptual and Motor Skills, 82, 12231231.

Kaplan, E., Fein, D., Morris, R., & Delis, D. (1991).WAIS-R-NI man-

ual. San Antonio, TX: Psychological Corporation.

Kendall, P.C., & Chansky, T.E. (1991). Considering cognition

in anxiety-disordered children. Journal of Anxiety Disorders, 5,

167185.

Lau, J.Y.F., Eley, T.C., & Stevenson, J. (2006). Examining the state

trait anxiety relationship: A behavioural genetic approach. Journal

of Abnormal Child Psychology, 34, 1927.

MacLeod, C., & Donnellan, A.M. (1993). Individual differences in

anxiety and the restriction of working memory capacity.Personalityand Individual Differences, 15, 163173.

Mathews, A., Mackintosh, B., & Fulcher, E.P. (1997). Cognitive biases

in anxiety and attention to threat. Trends in Cognitive Sciences,

1, 340345.

McClure, E.B., Monk, C.S., Nelson, E.E., Zarahn, E., Leibenluft, E.,

Bilder, R.M., Charney, D.S., Ernst, M., & Pine, D.S. (2004).

A developmental examination of gender differences in brain

engagement during evaluation of threat. Biological Psychiatry,

55, 10471055.

Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter,

A., & Wager, T.D. (2000). The unity and diversity of executive

functions and their contributions to complex frontal lobe tasks:

A latent variable analysis. Cognitive Psychology, 41, 49100.

Miu, A.C., & Visu-Petra, L. (2009). Anxiety disorders in children and

adults: A cognitive, neurophysiological and genetic characteriza-

tion. In R. Carlstedt (Ed.),Handbook of integrative clinical psychol-

ogy, psychiatry and behavioral medicine: Perspectives, practices

and research(pp. 309351), New York: Springer.

Owens, M., Stevenson, J., Norgate, R., & Hadwin, J.A. (2008).Working memory partially mediates the relationship between trait

anxiety and academic performance. Anxiety, Stress, & Coping, 21,

417430.

Phillips, B.N., Pitcher, G.D., Worsham, M.E., & Miller, S.C. (1980).

Test anxiety and the school environment. In I.G. Sarason (Ed.), Test

anxiety: Theory, research, and applications(pp. 327346). Hills-

dale, NJ: Lawrence Erlbaum.

Pine, D.S. (2007). Research review: a neuroscience framework for

pediatric anxiety disorders. Journal of Child Psychology and Psy-

chiatry, 48, 631648.

Pine, D.S., & Monk, C.S. (2008). The development and cognitive neu-

roscience of anxiety. In C. Nelson & M. Luciana (Eds.),Handbook

of developmental cognitive neuroscience (pp. 755771). Cam-

bridge, MA: MIT Press.Pine, D.S., Wasserman, G.A., & Workman, S.B. (1999). Memory and

anxiety in prepubertal boys at risk for delinquency. Journal of the

American Academy of Child and Adolescent Psychiatry, 38,

10241031.

Rabian, B., & Silverman, W.K.(2000).Anxietydisorders.In M. Hersen &

R.T. Ammerman (Eds.), Advanced abnormal child psychology (pp.

271289). London: Lawrence Erlbaum Associates.

Rapee, R.M. (1993). The utilization of working memory by worry.

Behavior Research and Therapy, 31, 617620.

Raven, J. (1986). Fostering competence. In T. Burgess (Ed.),Education

for capability. London: NFER-Nelson.

Rossion, B., & Pourtois, G. (2004). Revisiting Snodgrass and Vander-

warts object set: The role of surface detail in basic-level object rec-

ognition. Perception, 33, 217236.

Schniering, C., Hudson, J.L., & Rapee, R.M. (2000) Issues in the

assessment and diagnosis of anxiety disorders in children and ado-

lescents.Clinical Psychology Review, 20, 453478.

Shackman, A.J., Sarinopoulos, I., Maxwell, J.S., Pizzagalli, D.A.,

Lavric, A., & Davidson, R.J. (2006). Anxiety selectively disrupts

visuospatial working memory. Emotion, 6, 4061.

Shu, S.Y., Wu, Y.M., Bao, X.M., & Leonard, B. (2003). Interactions

among memory-related centers in the brain. Journal of Neu-

roscience Research, 71, 609616.

Spence, S.H., Donovan, C., & Brechman-Toussaint, M. (1999).

Social skills, social outcomes, and cognitive features of child-

hood social phobia. Journal of Abnormal Psychology, 108,

211221.Spence, S.H., Rapee, R., McDonald, C., & Ingram, M. (2001). The

structure of anxiety symptoms among preschoolers. Behavior

Research and Therapy, 39, 12931316.

Thomas, K.M., Drevets, W.C., Dahl, R.E., Ryan, N.D., Birmaher, B.,

Eccard, C.H., Axelson, D., Whalen, P.J., & Casey, B.J. (2001).

Amygdala response to fearful faces in anxious and depressed chil-

dren. Archives General Psychiatry, 58(11), 10571063.

Toren, P., Sadeh, M., Wolmer, L., Eldar, S., Koren, S., Weizman, R., &

Laor, N. (2000). Neurocognitive correlates of anxiety disorders in

children: A preliminary report. Journal of Anxiety Disorders, 14,

239247.

Visu-Petra et al. 9


10/10

Tsujimoto, S., Kuwajima, M., & Sawaguchi, T. (2007). Developmental

fractionation of working memory and response inhibition during

childhood. Experimental Psychology, 54(1), 3037.

Vasa, R.A., Roberson-Nay, R., Klein, R.G., Mannuzza, S., Moulton,

J.L., Guardino, M., Merikangas, A., & Pine, D.S. (2007). Memory

deficits in children with and at risk for anxiety disorders.Depression

and Anxiety, 24, 8594.

Visu-Petra, L. (2008).The Multidimensional Development of ExecutiveFunctioning: A Neuropsychological Approach. Cluj-Napoca:

ASCR Printing House.

Visu-Petra, L., Ciairano, S., & Miclea, M. (2006). Neurocognitive cor-

relates of child anxiety: a review of working memory research. Cog-

nition, Brain, Behavior, 4, 517541.

Visu-Petra, L., Miclea, M., Cheie, L., & Benga, O. (2009). Processing

efficiency in preschoolers memory span: A longitudinal investiga-

tion of individual differences related to age and anxiety. Journal of

Experimental Child Psychology, 103, 3049.

Visu-Petra, I. T incas, L. Cheie, & O. Benga (2010) Anxiety and visual-

spatial memory updating in young children: An investigation using

emotional facial expressions. In N. Derakshan, & M. Eysenck

(Eds.), Cognition and emotion: Emotional states, attention, and

working memory. 24(2), 223240.

Wall, P. M., & Messier, C. (2000) Concurrent modulation of anxiety

and memory.Behavioral Brain Research, 109, 229241.

Weems, C.F. (2008). Developmental trajectories of childhood anxiety:Identifying continuity and change in anxious emotion. Developmen-

tal Review, 28, 488502.

Woodward,L.J., & Fergusson, D.M.(2001). Lifecourse outcomes of young

people with anxiety disorders in adolescence.Journal of the American

Academy of Child and Adolescent Psychiatry,40, 10861093.

Zelazo, P.D., Carlson, S. M., & Kesek, A. (2008). The development of

executive function in childhood. In C. Nelson & M. Luciana (Eds.),

Handbook of developmental cognitive neuroscience (2nd ed.,

pp. 553574). Cambridge, MA: MIT Press.


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