Effects of anxiety on memory storage and updating in young children

Laura Visu-Petra,1 Lavinia Cheie,1 Oana Benga,1 and Tracy Packiam Alloway2

International Journal of Behavioral Development 110 The Author(s) 2010 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0165025410368945 ijbd.sagepub.com

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 updating in a dual-task context, high-anxious children performed worse than low-anxious children on two verbal working memory tasks. Therefore, 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 (threatrelated) memory bias, another looking at memory for neutral information. 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 no evidence 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 anxiety 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, & Derakshan, 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 phonological loop provides temporary storage of verbal material, and the visuo-spatial sketchpad specializes in the maintenance and manipulation 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 measured by the resources involved in solving the task (e.g., time, mental 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 storage capacity 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 the active manipulation of 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 documented. 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

Developmental Psychology Lab, Department of Psychology, Babes -Bolyai University, Cluj-Napoca, Romania 2 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: laurapetra@psychology.ro

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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 threatinduced state anxiety (as opposed to the previously mentioned studies that targeted trait anxiety) has been related to a selective impairment in visual-spatial working memory (Shackman et al., 2006). An alternative theoretical account for the anxiety-related attentional 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/cognitive control. However, a divergent claim is that this impairment is most visible in conditions with low (perceptual) load, in which attentional resources are only partially occupied. This allows salient distractors 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 paradigm, the study shows that high trait-anxious individuals are slower to identify targets in the presence of incongruent distractors under conditions of low (but not high) perceptual load. The findings are explained by a processing style characteristic of trait anxiety (regardless of the type of information conveyed by the stimuli, i.e., threatening or not threatening), with difficulties in trial-to-trial alterations when attentional resources are not 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.

International Journal of Behavioral Development

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 performance (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 detrimental 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 effectiveness 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 detrimental effects of anxiety would be visible on the verbal, but not on the visual-spatial memory storage and updating tests.

Developmental research
In the context of early development, the relationship between anxiety, memory and learning has been under-investigated (see Visu-Petra, Ciairano, & Miclea, 2006, for a review). The few studies conducted with clinical populations (Gu nther, Holtkamp, Jolles, Herpertz-Dahlmann, & Konrad, 2004; Pine, Wasserman, & Workman, 1999; Toren et al., 2000; Vasa et al., 2007) and with nonclinical, 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) effectiveness, 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, Brogan, & Stevenson, 2005). In preschoolers, trait anxiety was a longitudinal 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 anxiety on spatial WM was found in preschoolers (Visu-Petra et al., 2010). Anxiety-related verbal, but not visual-spatial, WM impairments 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

Study 1
In the developmental literature, (state) anxiety and STM effectiveness 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 anxiety was a longitudinal predictor of a marginal impairment in performance 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 (memory 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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SD 13). Based on the median split of parental ratings of the childrens anxiety symptoms, all the children in our sample were classified as either low anxious (LA; N 59; mean Spence score 16.19, SD 5.82), or high anxious (HA; N 57; mean Spence score 37.78, SD 10.16). The difference between the two resulting groups in their trait anxiety scores (median value was 24, see the scale description below) was highly significant, F(1, 114) 198.96, p < .01, partial Z2 .63. The two anxiety groups did not significantly differ in age, F(1, 114) 1.98, n.s. (mean age for LA 61 months, SD 13; mean age for HA 64 months, SD 12). Parental informed consent was obtained prior to the testing and informed verbal consent from the child was requested before proceeding with the testing. From these 116 children, all completed the Word Span Task, 115 the Digit Span, 115 the Corsi Span, 112 the Object Span, and 105 the Color Span Task (see the description of measures below). Missing data was not used in the analyses.

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correctly recalled 3 two-word lists, 2 three-word lists and 1 four-word list, an aggregate span of 2 0.66 0.33 3 would be awarded. Processing efficiency was evaluated only for the verbal tasks (Word and Digit Span) for the lists correctly recalled by most children (LL2 and LL3). All responses were recorded on audiotape and analyzed using a speech waveform editor (CoolEditPro, Version 2.0) on a laptop. An index of efficiency was calculated by adding the preparatory intervals, word durations, and interword pauses to generate the total response time for LL2 and LL3 for each child (see Cowan et al., 2003; Visu-Petra et al., 2009).

Results
All of the following analyses reported in Study 1 were conducted with age in months as a covariate. We first investigated anxietyrelated impairments in performance effectiveness (i.e., memory accuracy, see Figure 1). A multivariate analysis of variance (MANCOVA) was conducted with the aggregate span scores from the five STM tasks (Digit, Word, Corsi, Object, and Color Span) as dependent variables and with Anxiety Group (HA and LA) as a betweensubject factor. The overall effect of Anxiety Group on the STM tasks was non-significant, Wilks lambda .91, F(5, 95) 1.84, n.s., suggesting that anxiety does not lead to a reuction in the effectiveness of STM performance. Total response time was considered a global index of processing efficiency in solving the verbal STM tasks. It was calculated as the sum (in seconds) of preparatory intervals, word durations and interword pauses for the LLs correctly recalled by all children (LL2 and LL3). A MANCOVA with Total response times for Word and Digit Span as dependent variables, and with Group (HA vs. LA) as a between-subjects factor was conducted. There was a main effect of Group on verbal STM Total response times, Wilks lambda .90, F(2, 102) 5.98, p .004, partial Z2 .11. Univariate ANOVAs showed that this effect was only significant in the case of Word Span, F(1, 106) 4.28, p .041, partial Z2 .04, and not of Digit Span, F(1, 106) .74, n.s. More specific, LA children (M 1.07, SD .19) were faster than HA children (M 1.15, SD .24) in correctly recalling the LL2 and LL3 items. In order to decompose this global temporal difference, we investigated the way anxiety impacts distinct segments of total response times (preparatory intervals, interword pauses, and word durations) for Word Span on LL2 and LL3, respectively (see Figure 2 for descriptives). These segments were entered as dependent variables in univariate analyses (with age as covariate). There was a main effect of Anxiety Group on preparatory intervals for LL2, F(1, 115) 6.13, p .015, partial Z2 .05; LA children (M .50, SD .13) were faster than HA children (M .56, SD .16) in preparing their initial responses on the Word Span test. There was also a tendency for HA children (M .15, SD .07) to have longer interword pauses on the same LL2 than LA (M .12, SD .25), though this was not significant when the effects of age were taken into account, F(1, 115) 2.84, p .09. As hypothesized, the findings revealed no effect of trait anxiety on performance effectiveness in the case of STM tasks. However, the preparatory intervals were longer for HA children in the case of their initial responses on the Word Span. Therefore, trait anxiety does not seem to impact memory recall when simple storage is involved. However, it can result in impairments of verbal processing efficiency, as high-anxious children take longer to prepare their answers.

Measures
The Spence Preschool Anxiety Scale (Spence, Rapee, McDonald, & Ingram, 2001) generates an overall measure of trait anxiety based on 28 anxiety items. It is assessed via parental report and contains five sub-scales, each tapping a specific aspect of child anxiety. The Romanian version of the test (Benga, T incas , & Visu-Petra, 2010) has good internal consistency (Cronbachs a . 87 for mother reports, and a .89 for father reports) and moderate testretest reliability (r .59). Two verbal STM tasks were administered: Word and Digit Span. The child hears a sequence of up to nine highly familiar twosyllable words/numbers, for the Word and Digit Span, respectively, and has to recall each sequence in the correct order. Three visual-spatial STM tasks were administered: Color, Object and Corsi Span. In the Color Span task we used nine cards (6.5 x 7 cm), each representing a circle of a certain color: red, yellow, blue, pink, grey, violet, brown, orange, and green. The cards in the object Span task were identical in size and represented familiar objects extracted from the Snodgrass colored, revised inventory (Rossion & Pourtois, 2004). In order to ensure color equivalence, only red stimuli were selected. For the Corsi Blocks Test, we used a 10 blue blocks display taken from the WAIS-R Neuropsychological Inventory (Kaplan, Fein, Morris, & Delis, 1991). The examiner used their index finger to point to the blocks at a rate of one block per second.

Procedure and scoring

The testing session lasted approximately 2030 minutes. The child had to reproduce gradually increasing series of presented elements (digits, words, images, locations) in the exact order as they had been presented by the examiner. Each task consisted of 9 items in 8 possible list lengths (LL). Each LL contained three trials of items for that particular length, beginning with a 2-items list (LL2). The child was presented with the three trials from each LL; after three consecutive wrong trials, testing was stopped. Following the procedure used by Cowan and collaborators (1994, 2003), an aggregate span was calculated to reflect performance across lists. This was taken to be a sensitive measure for performance effectiveness. After determining a base span as the highest LL at which all three trials were passed correctly, a score of 0.33 was added to this base span for every list of a higher length that was correctly recalled. For example, if a child

International Journal of Behavioral Development

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

Study 2
In 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 educational relevance of investigating memory updating in children with anxiety. No impact of anxiety on spatial WM was found in preschoolers (Visu-Petra et al., 2010).

Our second design involved a more extensive collection of verbal and visual-spatial tests from the Automated Working Memory Assessment battery (AWMA, Alloway, 2007), targeting younger children than those in previous studies. The aim was to test for potential anxiety-related working memory impairments in both effectiveness 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. Our hypothesis was that 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.

Visu-Petra et al.

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mental rotation and to subsequently recall the location of each ball by pointing to a picture with six compass points.

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 of the childrens anxiety symptoms (median was 26.5). The two resulting 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 Oddone-out task, 97 completed the Mr. X, Counting Recall and Backward Digit Recall tasks, and 91 the Listening Recall task.

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 correctly 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 efficiency 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 resources the child is investing in the primary (memory) task, the less he will perform on the secondary task.

Measures
The Colored Progressive Matrices test (CPM, Raven, 1986) with norms for the Romanian population (Dobrean, Rusu, Coms a, & Bala zsi, 2005) was used as an estimate of the childs general intelligence 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/dissimilar or false/true judgments for each of the to-be-remembered items). Three verbal WM measures were administered: Counting, Listening and Backward Digit Recall. In the Counting Recall test, the child was presented with a visual array of red circles and blue triangles; 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 three shapes, 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 displayed 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

Results
Figure 3 shows the mean memory scores (performance effectiveness) 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 nonverbal ability were included as covariates here and in all subsequent analyses. The results indicated a significant effect of Group on the WM 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: Backward 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 (M 5.51, SD 3.79 for Backward Digit Recall, and M 6.60, SD 5.70 for Listening Recall) had lower scores than LA (M 7.45, SD 3.49, and M 9.66, SD 3.03, for Backward Digit and Listening Recall, respectively). None of the two visual-spatial WM tasks was impacted by anxiety, F(1, 91) .02, n.s., for Odd-one-out, and F(1, 91) .59, n.s., for Mr. X. The analysis was repeated without controlling for nonverbal ability (Raven IQ), because this measure draws upon visual-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 nonsignificant, F(1, 91) .00, n.s., for Odd-one-out, and F(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, partial Z2 .21. Univariate ANOVAs showed that this effect was significant only for Listening Recall, F(1, 91) 20.71, p < .01,

International Journal of Behavioral Development

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

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, and M 22.18, SD 7.56 for LA). The findings revealed detrimental effects of trait anxiety on performance 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 discussion
To 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 visualspatial STM and WM measures. On these tests, performance effectiveness (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 children 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 updating measures, performance did not differ between the two anxiety groups. The main research questions revolved around the relationships between anxiety and performance index (efficiency vs. effectiveness), 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 necessarily 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 stronger 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 administered 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. effectiveness, 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 efficiency were calculated (the latter only for the verbal measures). While performance effectiveness was unaffected on all STM measures, processing efficiency was reduced in HA children on Word Span, as revealed by their longer preparatory intervals. In the second 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 performance 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 had a 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 individuals 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,

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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 cautionary 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 (Word Span). HA children took longer than their LA counterparts to prepare 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 processing 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 preparatory intervals and interword pauses (Cowan et al., 1998), in order to overcome anxiety-related interfering thoughts. However, the presence of this effect on the lower, but not on the higher list lengths could provide indirect evidence for the hypothesis of an anxietyrelated deficit under conditions of lower (in this case memory, not perceptual) load (Bishop, 2009), allowing the child to be more subjected 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 the working memory tasks did not allow us to further test this hypothesis 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 degree in HA children as they allocate more resources to the primary task. However, the detrimental effect of anxiety was only noted 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 requirement of a true/false judgment might 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 in effectiveness (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

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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 developmental period (Alloway, Gathercole, & Pickering, 2006). What are the potential mechanisms responsible for the detrimental effects of trait anxiety on the updating of neutral, not threatrelated elements? Different attentional and memory accounts for anxiety-related memory impairments have been proposed at different 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 performance effectiveness. Our data suggest that performance effectiveness is unimpaired in STM tasks and that efficiency is compromised only at the initial stages of recall (preparatory intervals for the first list length). An alternative would be that anxiety-induced worrisome thoughts interfere with the memory updating processes, compromising online rehearsal and maintenance of information. This proposal is supported by the selective impact of trait anxiety on WM, but not on STM measures. Neurobiological 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 retrievalinduced effects. High-anxious children have been shown to have less confidence in their answers and to underestimate (in anticipation) 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 the level 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 anxietyrelated attentional and memory effects being likely to affect different 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 compensatory 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 confluence of several remarkable progressions. Brain maturation, through processes of focalization and frontalization (Zelazo, Carlson, & Kesek, 2008), is accompanied by the development of executive functioning, 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

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behavioral evidences. In adults, a concurrent mediation of anxiety and memory by the ventromedial prefrontal cortex and medial temporal regions has been documented (Shu, Wu, Bao, & Leonard, 2003; Wall & Messier, 2000). There is similar evidence from pediatric neuroimaging data suggesting medial temporal lobe dysfunction in social phobia and other anxiety disorders (McClure et al., 2004; Thomas et al., 2001), which could underlie both memory deficits and anxiety disorders (Vasa et al., 2007). However, it is yet not documented whether such a neurobiological account could be valid in the case of non-clinical, high trait anxiety. An alternative, behavioral account has been described above, relying on attentional/ memory peculiarities in information processing in high-anxious children. The behavioral evidence suggests that very young children 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 testing, children with higher levels of trait anxiety have produced more attentional shifts towards internally or externally generated (evaluation) threat stimuli, resulting in encoding/maintenance/retrieval deficiencies. Unfortunately, there are few attempts to provide unitary 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, Hudson, & 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 limitation relates to the lack of a processing efficiency index in the WM tasks. It is for further research to investigate the presence of a comparable effect to the one noted in STM tasks in young children. 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 preschoolers, 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 measures. Further research should validate the effects of anxiety on processing efficiency measures in the WM tasks, and examine additional efficiency indexes complementary to the information provided 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 collection and to the children and kindergarten staff for their collaboration. Funding

International Journal of Behavioral Development

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
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