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The effects of background white noise on memory performance in inattentive school children

The effects of background white noise on memory performance in inattentive school children Background: Noise is typically conceived of as being detrimental for cognitive performance; however, a recent computational model based on the concepts of stochastic resonance and dopamine related internal noise postulates that a moderate amount of auditive noise benefit individuals in hypodopaminergic states. On the basis of this model we predicted that inattentive children would be enhanced by adding background white noise while attentive children’s performance would deteriorate. Methods: Fifty-one secondary school pupils carried out an episodic verbal free recall test in two noise conditions. In the high noise condition, verb-noun sentences were presented during auditory background noise (white noise, 78 dB), and in the low noise condition sentences were presented without noise. Results: Exposure to background noise improved performance for inattentive children and worsened performance for attentive children and eliminated episodic memory differences between attentive and inattentive school children. Conclusions: Consistent with the model, our data show that cognitive performance can be moderated by external background white noise stimulation in a non-clinical group of inattentive participants. This finding needs replicating in a larger sample using more noise levels but if replicated has great practical applications by offering a non-invasive way to improve school results in children with attentional problems. Background children with attention deficits. Under certain circum- It has long been known that cognitive processing is stances children with attentional problems (including easily disturbed by incompatible environmental stimu- those with ADHD) benefit from, rather than being lation which distracts attention from tasks [1]. This distracted by, background task-irrelevant noise pre- effect is believed to stem from competition for atten- sented concurrently with a target task. For instance, tional resources between the distracting and the target Stansfeld et al. [9] found that under certain conditions stimuli. Such negative distractor effects hold across a road traffic noise can improve performance on episodic wide variety of tasks and stimuli as well as in different memory tasks in children at risk for attentional pro- participant populations [2-6]. For some populations blems and academic under-achievement. Research data the effects are predicted to be especially strong. For from our group demonstrated that adding background instance, individuals with attentional problems such as white noise to the environment enhanced memory per- attention deficit/hyperactivity disorder (ADHD) are formance of children with ADHD [10]; although in generally acknowledged to be more vulnerable to every day situations optimal levels of white noise will distraction than normal control children [7,8]. vary from one individual to another. At the same time there are reports of contradictory Why these paradoxical effects should occur is not well findings where certain types of task irrelevant noise understood. Most accounts in the past, for example the actually improve the performance of children. Surpris- optimal stimulation theory by Zentall and Zentall [11] ingly, this effect may also be most pronounced in and later models of cognitive energetic and motivational processes [12], have focused on the role of background * Correspondence: goran@ling.su.se stimulation as a generator of increased arousal which Department of Linguistics, Stockholm University, Sweden counteracts boredom. A recent computational model has Full list of author information is available at the end of the article © 2010 Söderlund et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 2 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 attempted to explain these positive effects of background differences are linked to attention ability and neuro- noise on performance in a different way [13]. This model transmission in the brain in such way that inattentive combines two factors: It explains (i) how noise enhances persons need more external noise for a proper cognitive attention and performance in general by the concept of functioning. In the model dopamine is the crucial neu- stochastic resonance (SR) and (ii) whythere areindivi- rotransmitter. This is because it modulates the neural dual differences in the way noise affects the brain by a cell’s responses to the environment and determines the model of individual differences in dopamine. probability that it will fire following the presentation of a stimulus [23]. Alterations in dopamine function are Stochastic Resonance - how noise strengthens the signal related to individual differences in attention [24,25], SR or noise-improved signaling is a well-established phe- cognition [26] and motivated behavior [27,28]. Dopa- nomenon across a range of experimental settings; SR mine release has both tonic (background levels) and exists in any threshold-based system with noise that phasic (response to specific environmental events) com- requires a threshold to be passed before a signal is regis- ponents regulated by different brain regions [29,30]. tered. SR can be observed in nature in any non-linear Tonic dopamine levels are suggested to modulate the dynamic system, which is not working at its optimum phasic reactivity; a low tonic level increases stimulus level, in particular SR has been found in the nervous dependent phasic release, and the opposite, a high tonic system. The simplest examples of an SR-related benefit level suppresses phasic release [31]. Low tonic levels canbeseen in thedetection of sensorysignals.Whena cause neural instability associated with cognitive symp- weak signal (e.g. a tone stimulus) is presented below the toms such as failure to sustain attention [32]. The hypo- hearing threshold it becomes detectable when random or dopaminergic state in ADHD is distinguished by low white noise is added to the signal. In essence, this tonic dopamine levels leading to excessive reactivity to account proposes that the additional variability provided environmental stimulation [33,34]. If the firing probabil- by the noise interacts with the weak signal pushing it ity or gain parameter is low, neurons will fire at random above the detection threshold, see review in [14]. For yielding poor cognitive performance. If the gain para- instance, SR has been found in several modalities; audi- meter is high there will be cognitive stability and thus tion [15], vision [16], and touch [17] where stochastic high performance. This responsiveness of neurons is noise improves sensory discriminability. Recently SR has modulated via dopamine that enhances the differentia- been shown to work across modalities, for example when tion between efferent firing and afferent external stimu- auditory noise improves visual signal detection [18]. lation. It has been shown recently that neural noise Most SR studies have used perception tasks, requiring related to dopamine tone is an integral part of inter- the detection of weak peripheral sensory inputs. Few neuronal communication and that a sufficient level of studies have examined how noise influences cognitive noise may be necessary for normal function in the performance. Recent empirical evidence suggests that SR nervous system [21,35], through the process of SR. That can also improve central processing and cognitive perfor- is, there exists both external noise - outside of the ner- mance. For example, SR has been found in cognitive vous system - and neural noise (related to dopamine tasks where auditory noise improved the speed of arith- tone) inside the system. metic computations [19] and recall on visual memory The moderate brain arousal model (MBA) [13], upon tasks [20]. Thus, adding noise to the input of the infor- which the current study is based, is a neurocomputa- mation processing system can increase its signal-to-noise tional model that relies on classic conditions for output. SR is usually quantified by plotting detection, or stochastic resonance and the modulating properties of cognitive performance, as a function of noise intensity. dopamine-related gain and neural noise in determining This relationship follows an inverted U-curve function, neural responsivity. It suggests that the hypodopaminer- where performance peaks at a moderate noise level. That gic brain need higher input noise to function to its full is, moderate noise is beneficial for performance whereas potential. Thus the model suggests that external white too little, or too much, noise attenuates performance. For noise could compensate for behavioral dysfunction con- extensive reviews on the influence of noise on the nected to conditions caused by impaired dopamine trans- nervous system the reader is referred to recent reviews mission. Accordingly, ADHD children or low attentive [14,21]. Also detrimental effects of noise on the nervous children more generally have a low gain parameter owing system and in particular on speech processing are to low levels of baseline dopamine neuron firing. Neuro- reported in a recent review [22]. computationally the MBA model shows that more exter- nal environmental noise is required for optimal Individual differences in the SR effect performance in cognitive tasks for such low gain “indivi- The novel aspect of the proposed framework is that the duals” compared to high gain “individuals”. Accordingly, SR phenomena differs between individuals and these external noise, it is predicted by the model” will Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 3 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 compensate for reduced neural background activity in (WCST). In another study on healthy controls by Mattay ADHD. That is to say that increased levels of external et al. [42] dextroamphetamine was found to increase auditive noise can activate internal noise and restore the N-back working memory performance in group with low activity level. Further, given the inverted U function that baseline working-memory capacity, whereas the perfor- operates in relation to noise and performance in SR, the mance worsened in a group with high baseline perfor- MBA model also predicts that levels of background noise mance [42]. Dextroamphetamine also had differential that might be beneficial for ADHD children would be effects on the BOLD fMRI response on these groups. detrimental for those with normal attention. Crucially, These findings have been corroborated in a study using a the beneficial effects are not specific to ADHD (Figure 1): spatial working memory task where stimulant medication they are also found in dopamine-related neurodegenera- only improved memory performance in healthy indivi- tive disorders such as: akinesia [36], Parkinson’s disease duals with low baseline working memory capacity [43]. [37] and in aging [38]. These effects have been modeled This was also mirrored by increased cerebral blood flow in terms of age dependent dopamine loss [39]. in dorsolateral prefrontal cortex and posterior parietal In this paper we investigate, for the first time, how cortex. Taken together these studies indicate that dopa- noise influences cognitive performance in a normal, non- mine function influences performance and brain activity clinical, group of children that differ from each other in differently also in groups consisting of healthy controls their attentional abilities. Recent evidence suggests that depending on tasks that are linked to attention and work- dopamine plays a role in attention also in non-clinical ing memory (e.g., WCST, N-back, spatial working mem- groups. When a visual orienting task was used to study a ory). This body of data is consistent with the view that normal group of children, it was found that those chil- ADHD and related attentional problems is best concep- dren who were homozygous for alleles influencing dopa- tualized as a continuum rather than a discrete category mine transportation displayed inattention on left-hand and that ADHD symptoms are distributed in populations sided stimuli, whereas those who were heterozygotes did [44]. The syndrome of ADHD represents a transition of not [40]. The response to amphetamine has also been degree rather than of a kind and diagnostic thresholds found to be influenced by genetic factors; it depends on are therefore somewhat arbitrary resting on general and the functional polymorphisms of the Catechol O-methyl- cultural norms about behavior and development [45]. transerase (COMT) gene in a normal population of In addition, a comparison of the extreme points in a nor- humans. Mattay et al. [41] found that amphetamine mal distribution shows the same heritability patterns as a enhanced prefrontal efficiency measured by fMRI for the comparison between ADHD and control [46]. This, in val/val (high DA metabolism) genotype, whereas met/ turn, suggests that non-clinical persons with low and met (low DA metabolism), had no such effect on low to high attention may show similar effect from noise as medium workload, and decreased efficiency on high ADHD and control persons do. workload tasks. Furthermore, preservations errors were In this paper, we study inattentive and normally atten- decreased by amphetamine in the val/val, but not the tive children’s episodic memory in a verb-noun sentence met/met groups, in a Wisconsin Card Sorting Test recall task under two conditions varying in terms of the Figure 1 Individual difference in SR curves. Note. Performance on cognitive tests (y-axis) is optimal for moderate noise levels (x-axis), and attenuated for both too low and too high noise levels. More noise is required for optimal performance in inattentive or low performing children compared to attentive or high performing children. Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 4 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 levels of background auditive white noise. Our predic- sentences in each list. Each sentence consisted of a tion is that in the low noise condition the inattentive unique verb and a unique noun (e.g., “roll the ball”)in children will perform less well than attentive children Norwegian. The sentences were placed in random order. while in the high noise condition these differences List-order (1-8) and condition-order (no noise vs. noise) should diminish as the addition of white noise benefits were counterbalanced and noise was present on every the inattentive but not the normally attentive children. second list. All to-be-remembered sentences were recorded on a CD. A new item was read every 9th sec- Methods ond. The sentences were read in both the low noise and Participants the high noise condition. The equivalent continuous Fifty-one secondary school pupils (25 boys and 26 girls) sound level of the white noise was 78 and the speech between 11-12 years (M = 11.7) participated in the signal was 86 dB; thus the signal-to-noise ratio was study. The group consisted of children from two school 8 dB. The signal was sufficiently strong so that all parti- classes, year seven (86% of children participated). Parti- cipants could perceive the content of the words in both cipants where divided into two groups after their atten- conditions without error (i.e., the tests were a cognitive tion abilities were assessed by teachers using a seven memory test and not a perceptual test). The two noise point Likert scale. The assessment scale is the same as levels were chosen to correspond to levels that have that used in the longitudinal research program Indivi- been found in earlier studies to affect cognition in an dual Development and Adaptation [47]. Participants arithmetic’s test for a normal population [19] and work- that scored high (6 or 7 - severe problems in the class ing memory performance in patients with Alzheimer’s room) on inattention where assigned to the inattentive disease [4]. Recordings were made in a sound studio. group. This group consisted of 10 participants, 6 of them also scored high on hyperactivity as evaluated by Procedure the teachers. The comparison group comprised the The testing was conducted at the child’s school, following remaining 41 children thatscored5or loweratthe permission from parents and children. The University scale, and were assessed as average- or highly attentive. College of Sogndal, Norway and the regional ethic board None of the inattentive group had an ADHD diagnosis in Stockholm approved the study. The participants were and none were treated with medication. Achievements tested individually in a room during the school day. The and scholastic skills (3 point scale) and reading ability test lasted for about 45 minutes including the presenta- (7 point scale) used in [47] were also rated by their tea- tion of instructions. Before starting the experiment chers. Children’s school achievement was assessed in proper, two practice sentences were presented. The time terms of whether their school performance was at the taken to present each list was approximately 1 minute level expected for this age group. General cognitive skills and 40 seconds. The to-be-remembered sentences were and reasoning ability were assessed using the Raven’s presented concurrent with continuous white noise during progressive matrices test [48]. The Raven’s test assesses the encoding phase in the high noise condition and in learning and problem solving ability and correlates silence in the low noise condition. Noise conditions highly with the g-factor in IQ tests. Forward and back- changed after every sentence list in outbalanced order. ward digit span measuring short-term and working No noise was presented during retrieval. Directly after memory respectively were assessed. Table 1 shows the presentation of the last item in a list, participants results from these tests for the high and low attentive performed a free recall test in which they spoke out loud groups as well as other background characteristics of as many sentences as possible, in any order. these groups. The groups were well matched on school performance and general cognitive ability - the inatten- Results tive group had less developed reading skills. Recall performance A 2 × 2 mixed ANOVA was conducted with one Design between-subject factor, Group (normal attention vs inat- We used a 2 × 2 design, where noise levels (low versus tentive) and one within-subjects factor, encoding condi- high) was the within participant manipulation and the tion (low noise vs high noise). We choose the standard between group variable was teacher rated classroom scoring procedure in the action memory literature attention level (normal versus inattentive). [10,49], where strict scoring is used for the nouns (exact matches were required) and lenient scoring is used for Materials verbs (where non-exact matches are scored as correct). All participants undertook a verbal episodic recall test. This is because nouns are typically recalled somewhat The to-be-remembered (TBR) items consisted of 96 sen- more easily than verbs [50]. There where no main effects tences divided into 8 separate lists with 12 verb-noun of noise (F(49,1) = .01, p =.94)orgroup (F(49,1) = .30, Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 5 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 Table 1 Participant characteristics and cognitive test scores Cognitive and behavioral measures Attentive group Inattentive group Attentive vs. Inattentive N= 41 N=10 (20 boys, 21 girls) (5 boys, 5 girls) Mean SD Range Mean SD Range t-test score Inattention 2.8 (1.6) 1 - 7 6.2 (0.4) 1 - 7 t(49) = 6.67*** (1 = low, 7 = high) Hyperactivity 2.5 (1.6) 1 - 7 4.9 (2.0) 1 - 7 t(49) = 4.11*** (1 = low, 7 = high) School performance 2.3 (0.7) 1 - 3 2.1 (0.7) 1 - 3 t(49) = 0.94 (1 = below, 2 = average, 3 = above) Reading skill 5.0 (2.0) 1 - 7 3.5 (1.7) 1 - 7 t(49) = 2.38* (1 = low, 7 = high) Raven score 41.2 (8.6) 16 - 55 37.3 (10.6) 19 - 53 t(49) = 1.09 Digits forward 23.1 (9.1) 4 - 42 15.0 (6.6) 4 - 23 t(49) = 3.22** Digits backwards 14.9 (6.9) 2 - 34 13.2 (4.2) 7 - 18 t(49) = 0.97 Note: * p < .05, ** p < .01, *** p < .001. p = .59). Both groups performed at the same level overall group (M = .46 vs. .41). Inattentive children performed across the two conditions. However, the interaction better in the high rather than the low noise condition between noise and group was significant (F(49,1) = 9.96, (t(9) = 1.84, p = .05 one-tailed). The opposite was p = .003, eta = .17) (Figure 2). This interaction was the case for the normally attentive group (t(40) = -3.46, further explored with planned simple contrasts for the p = .001). Using attention (score 1-7) and noise-effect within subjects factors, using paired sample t-tests. Con- (noise - no noise) as variables a Spearman rank-order sistent with the hypothesis the addition of white noise correlation revealed positive correlation between atten- enhanced performance for the inattentive group (M = .39 tion and noise (r = .378, N = 51, p = .006; a medium vs..44),and impaired performance for the attentive effect size according to Cohen’sd). Thehigherscore on Figure 2 Recall performance as a function of noise and attention; inattentive vs. attentive children (teachers judgments: attentive N = 41; inattentive: N = 10). Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 6 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 inattention the larger was the positive effect of noise and auditive white noise may have its effects either at a per- vice versa, attentive children performed worse in pre- ceptual or neuro-psychological level or may operate a sence of noise. neuro-chemical level directly altering levels of dopamine As reported above the two groups differed with respect release [13,51]. Animal models of dopamine function or to reading skills, as judged by teachers; with the inatten- pharmacological probes to manipulate tonic and phasic tive group having inferior reading skills compared to the dopamine are called for to investigate these effects. attentive group. However, when reading ability was Stimulant medication (e.g. methylphenidate) also added as a covariate to the main analysis the original improves cognitive performance in children with ADHD interaction effect, although diminished, persisted (F(48,1) [52,53]. This medication increases dopamine levels by = 7.13, p = .010). Reading level was independently related blocking the dopamine transporter [54]. Low performing to performance (F(6,1) = 1.46, p = .213). A Spearman’s healthy controls also benefit from increased dopamine rank order correlation revealed negative correlation transmission, which is manifested in improved cognitive between reader skills and positive effect of noise (r = performance and increased prefrontal cortical activity .335, N = 51, p = .016), a positive correlation between [43]. Our data show that auditory white noise may exert attention and reading ability (r = .498, N = 51, p < .001) potentially similar effects on cognition as medication and finally, a high positive correlation between teacher through the phenomenon of stochastic resonance (SR). ratings of inattention and hyperactivity (r =.789,N=51, White noise is characterized by randomness and so p < .001). However, there was no correlation between introduces variability in the nervous system [14]. hyperactivity and noise-effect (r = .141, N = 51, p = .323). A poorly tuned neural system benefit from additional white noise. In fact, the stochastic resonance theory pre- Discussion dicts that noise that is applied to the signal as an input We have proposed a framework for understanding indi- to a neural cell, improves the signaling efficiency of the vidual difference in the facilitative effects of auditive output of that cell, where the non-linearity in the firing white noise on performance. As predicted the results threshold of the neural cells is the key to improvement show different effects of noise in attentive and inatten- of the signal to noise ratio [14,55]. tive children selected from the normal population. Despite the fact that it appears that noise and methyl- There was significant improvement in performance for phenidate both improve cognitive performance, the under- the children rated as inattentive by their teachers, and a lying mechanism that is the basis of these phenomena are significant decline in performance for those rated as likely to be different. According to the model theoretically attentive as noise levels were increased. Furthermore speaking the difference between these phenomena is clear. these effects seem independent of other factors mea- Methylphenidate changes the strength (but not the varia- sured in the study - attentional ability seems to be a key bility) of the input, which is typically modeled by the gain marker of this effect. Even if inattention and hyperactiv- parameter in abstract neural networks [23]. In contrast, ity are strongly correlated, no correlation between noise changes the variability of the input (but per defini- hyperactivity and a positive noise effect was found, this tion does not influence the strength) of the input. How- suggests that in this study inattention is the key factor ever, despite these clear differences in the underlying level, to explain noise improvement. These results are similar the behavioral outcome may be similar, and the two to those previously reported with ADHD patients [10]. mechanisms interact in a complex way, making it difficult Here we discuss theoretical and practical implications of to distinguish the phenomena at the behavioral level [56]. these findings. Furthermore, direct evidence of difference between these From a theoretical point of view the findings are con- levels is emerging. Pålsson and Söderlund et al. (Noise sistent with the suggestion that the neural noise level benefit in pre-pulse inhibition of the acoustic startle reflex, associated with dopamine tone in inattentive children is submitted) studied the effect of methylphenidate, dopa- sub-optimal, see also [13] and that noise may enhance mine and noise on the startle response in a rat model of performance through the phenomenon of stochastic ADHD. They found that both control and ADHD strains resonance (SR). According to the model developed here, (SHR) benefited from noise; however, this effect was also noise in the environment yields an input to the percep- found in dopamine lesioned rats, suggesting that dopa- tual system, which can either compensate for low noise mine is not a necessary requirement for the stochastic in the neural system leading to an output consisting of resonance phenomenon to occur. improved cognitive performance, or, depending on pre- Another theoretical interpretation of the data is that existing levels of neural noise, can add too much to an noise in a general way increase arousal that makes the already well functioning system. The specific neuro- subject more alert, and less drowsy. The optimal stimu- biological and neuro-chemical mechanisms responsible lation model states that hyperactivity is as a homeostatic for these effects need further research. For instance, response to underarousal in order to achieve an optimal Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 7 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 arousal level [11]. However, this model does not make around 100 dB [62-64]. In later experiments by Broad- any explicit predictions about the selective effects of bent and colleagues, (memory recall of unrelated words) external stimulation whereas in the current study inat- lower noise levels (80-85 dB) were used; results showed tentive persons benefited from extra stimulation and no effects of noise on memory when exposed during the attentive children did not. In the cognitive energetic encoding phase but deteriorating results if exposed dur- model state factors like arousal, activation and effort are ing the recall phase [65,66]. More recently, episodic taken into account to explain shortcomings in ADHD memory has been found to be particularly vulnerable to patients [57]. According to this model state factors can speech noise, whereas traffic noise showed no effect [2]. be moderated by event rate (inter-stimulus-intervals, Results from the present study would indicate that the ISI) and workload in cognitive tasks both under- and effects of external noise would have look quite different over arousal can be produced. Recent research has in many of these studies if participants had been divided shown that stimulant medication (methylphenidate) and into attentive and inattentive or young and elderly, that shortened event rate can produce the same effect in a is high and low gain participants (tentatively high/low Go-Nogotask[58].Fromour pointofviewthe term dopamine groups). Selective effects of noise can easily arousal is poorly defined in the literature, and could be get hidden in group-means if some participants improve interpreted in terms of wakefulness or in term of neural and others are impaired. Our data may encourage noise arousal. To fully investigate the arousal-noise hypothesis researchers to reanalyze their experiments dividing par- an experiment would have to be designed where physio- ticipants by individual differences in attention and per- logical arousal is explicitly manipulated and measured. formance. Preliminary data from our lab, on an ADHD We arguethatthatproposedframework,including the rat model provide further support for the benefits of dopaminergic influence on stochastic resonance, pro- adding white noise. The Spontaneous hypertensive rat vides a more elaborated view both at the neural and at (SHR)showedimprovedsensorimotorgatingbyshow- the behavioral level. To account for the current data an ing more a pronounced pre-pulse inhibition of the star- arousal view would have to argue for a selective lower tle reflex when exposed to white noise as compared to arousal for the inattentive children. Finally, our experi- control strains, even though control rats also increased ence is that the subjects in our experiment are fully their inhibition in noise conditions (Pålsson, Söderlund aroused, the testing conditions at hand are very stimu- et al., Noise benefit in pre-pulse inhibition of the acous- lating, and subjects are very motivated to perform well. tic startle reflex, submitted). By highlighting the role of individual differences in the Reading disability is a common co-morbidity in ADHD. facilitative effects of auditive noise the current study Consistent with these findings, our data show lower read- refines our understanding of SR. SR exhibits an inverted ing skill for the inattentive group. Reading disability is also U-curve function, where performance peaks at a moder- linked with reduced short-term verbal memory that ate noise level. However, this is an oversimplification, as requires phonetic coding of material, but not necessarily there is no absolute sense in which a moderate noise with executive functions or long-term memory [67,68]. level is optimal. An “optimal” noise level for one indivi- This is also consistent with our data that show a lower dual could be either too high, or too low amount of performance in the digits forward task that measures noise for another individual. These complex interactions short-term memory, but no deficits for digits backward between noise and performance may account for some task that is related to working memory capacity. The of the contradictory findings in the previous literature. MBA model accounts for these findings because the digits For example, earlier research on noise in normal popu- backward task is a more demanding task leading to higher lations has shown both enhancing and diminishing brain arousal and thus good performance for inattentive effects of auditory white noise on cognition in non- children, whereas the less demanding digit forwards task clinical groups (90 dB) on simpler, short-term memory does not sufficiently arouse the brain for the low attention tasks like anagrams, whereas speech noise was detrimen- children [13]. Additionally, the positive correlation tal [59]. These noise effects also interacted with other between reading ability and noise enhancement suggests variables such as gender and time of the day [60], which that white noise may enhance awareness. This is consis- makes these results equivocal. No effect of white noise tent with the idea that dyslexia is caused by phonological was found in digit span recall in two experiments, deficits [69], however, a further investigation of phonologic whereas speech noise had a detrimental effect [4,5]. awareness is outside the scoop of the present study. However, noise improvement was found in a simple addition task in selected groups, elderly and young par- Limitations ticipants [61] and among elderly and Alzheimer patients Thecurrent studyhas anumberoflimitations.First, [4]. In Broadbent’s early research negative effects of ratings of academic attainment and reading were based noise have been found using high (excessive) noise levels on single item non-validated scales. Second, only two Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 8 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 Author details noise levels were investigated. It would be interesting to 1 2 Department of Linguistics, Stockholm University, Sweden. Linné University, include different levels so that the entire stochastic reso- 3 4 Växjö, Sweden. Sogn and Fjordane University College, Norway. University nance curve can be mapped out. One prediction from of Southampton, Dept. of Psychology, UK. Department of Experimental Clinical and Health Psychology, Ghent University, Belgium. our model is that in attentive group, a subset of partici- pants will benefit from noise when levels are individually Authors’ contributions adjusted. Furthermore, it would be of interest to investi- GS planned and designed the experiment, performed the statistical analysis and drafted the manuscript. SS have been involved in drafting and revision gate if the SR effect is dependent on task difficulty. of the manuscript. LML was responsible for the data collection. ESB have Third, only one test of cognitive ability was tested. been involved in revising the manuscript critically for important intellectual Future research may study whether the effects found content. All authors read and approved the final manuscript. here generalizestoother taskssuchasexecutive and Competing interests inhibitory functions. This is of particular importance The authors G. Söderlund, S. Sikström and, J-M. Loftesnes declare that they while investigating the possibility of noise, as an inter- have no competing interest. Financial disclosures and conflicts of interest statement E. Sonuga-Barke: vention in ADHD. A final limitation of the present Recent speaker board: Shire, UCB Pharma study is that the experiment was not designed to study Current & recent consultancy: UCB Pharma, Shire differential effects of noise on study and recall. The Current & recent research support: Janssen Cilag, Shire, Qbtech, Flynn Pharma experiment manipulates noise at encoding, but not at Advisory Board: Shire, Flynn Pharma, UCB Pharma, Astra Zeneca retrieval, so the effects of noise seen can only be attribu- Conference support: Shire ted to the conditions at encoding. To what extent noise Received: 2 March 2010 Accepted: 29 September 2010 presented at recall influences performance cannot be Published: 29 September 2010 determined by the experiment. However, the MBA pre- dicts that the conditions where noise is beneficial during References encoding should also be beneficial for performance dur- 1. Broadbent DE: The effects of noise on behaviour. Elmsford, NY, US: Pergamon Press, Inc 1958. ing retrieval. At same time it may be difficult to directly 2. Boman E, Enmarker I, Hygge S: Strength of noise effects on memory as a compare encoding and retrieval conditions, because the function of noise source and age. 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Papageorgiou C, Giannakakis GA, Nikita KS, Anagnostopoulos D, Papadimitriou GN, Rabavilas A: Abnormal auditory ERP N100 in children with dyslexia: comparison with their control siblings. Behav Brain Funct 2009, 5:26. doi:10.1186/1744-9081-6-55 Cite this article as: Söderlund et al.: The effects of background white noise on memory performance in inattentive school children. Behavioral and Brain Functions 2010 6:55. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral and Brain Functions Springer Journals

The effects of background white noise on memory performance in inattentive school children

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Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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Abstract

Background: Noise is typically conceived of as being detrimental for cognitive performance; however, a recent computational model based on the concepts of stochastic resonance and dopamine related internal noise postulates that a moderate amount of auditive noise benefit individuals in hypodopaminergic states. On the basis of this model we predicted that inattentive children would be enhanced by adding background white noise while attentive children’s performance would deteriorate. Methods: Fifty-one secondary school pupils carried out an episodic verbal free recall test in two noise conditions. In the high noise condition, verb-noun sentences were presented during auditory background noise (white noise, 78 dB), and in the low noise condition sentences were presented without noise. Results: Exposure to background noise improved performance for inattentive children and worsened performance for attentive children and eliminated episodic memory differences between attentive and inattentive school children. Conclusions: Consistent with the model, our data show that cognitive performance can be moderated by external background white noise stimulation in a non-clinical group of inattentive participants. This finding needs replicating in a larger sample using more noise levels but if replicated has great practical applications by offering a non-invasive way to improve school results in children with attentional problems. Background children with attention deficits. Under certain circum- It has long been known that cognitive processing is stances children with attentional problems (including easily disturbed by incompatible environmental stimu- those with ADHD) benefit from, rather than being lation which distracts attention from tasks [1]. This distracted by, background task-irrelevant noise pre- effect is believed to stem from competition for atten- sented concurrently with a target task. For instance, tional resources between the distracting and the target Stansfeld et al. [9] found that under certain conditions stimuli. Such negative distractor effects hold across a road traffic noise can improve performance on episodic wide variety of tasks and stimuli as well as in different memory tasks in children at risk for attentional pro- participant populations [2-6]. For some populations blems and academic under-achievement. Research data the effects are predicted to be especially strong. For from our group demonstrated that adding background instance, individuals with attentional problems such as white noise to the environment enhanced memory per- attention deficit/hyperactivity disorder (ADHD) are formance of children with ADHD [10]; although in generally acknowledged to be more vulnerable to every day situations optimal levels of white noise will distraction than normal control children [7,8]. vary from one individual to another. At the same time there are reports of contradictory Why these paradoxical effects should occur is not well findings where certain types of task irrelevant noise understood. Most accounts in the past, for example the actually improve the performance of children. Surpris- optimal stimulation theory by Zentall and Zentall [11] ingly, this effect may also be most pronounced in and later models of cognitive energetic and motivational processes [12], have focused on the role of background * Correspondence: goran@ling.su.se stimulation as a generator of increased arousal which Department of Linguistics, Stockholm University, Sweden counteracts boredom. A recent computational model has Full list of author information is available at the end of the article © 2010 Söderlund et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 2 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 attempted to explain these positive effects of background differences are linked to attention ability and neuro- noise on performance in a different way [13]. This model transmission in the brain in such way that inattentive combines two factors: It explains (i) how noise enhances persons need more external noise for a proper cognitive attention and performance in general by the concept of functioning. In the model dopamine is the crucial neu- stochastic resonance (SR) and (ii) whythere areindivi- rotransmitter. This is because it modulates the neural dual differences in the way noise affects the brain by a cell’s responses to the environment and determines the model of individual differences in dopamine. probability that it will fire following the presentation of a stimulus [23]. Alterations in dopamine function are Stochastic Resonance - how noise strengthens the signal related to individual differences in attention [24,25], SR or noise-improved signaling is a well-established phe- cognition [26] and motivated behavior [27,28]. Dopa- nomenon across a range of experimental settings; SR mine release has both tonic (background levels) and exists in any threshold-based system with noise that phasic (response to specific environmental events) com- requires a threshold to be passed before a signal is regis- ponents regulated by different brain regions [29,30]. tered. SR can be observed in nature in any non-linear Tonic dopamine levels are suggested to modulate the dynamic system, which is not working at its optimum phasic reactivity; a low tonic level increases stimulus level, in particular SR has been found in the nervous dependent phasic release, and the opposite, a high tonic system. The simplest examples of an SR-related benefit level suppresses phasic release [31]. Low tonic levels canbeseen in thedetection of sensorysignals.Whena cause neural instability associated with cognitive symp- weak signal (e.g. a tone stimulus) is presented below the toms such as failure to sustain attention [32]. The hypo- hearing threshold it becomes detectable when random or dopaminergic state in ADHD is distinguished by low white noise is added to the signal. In essence, this tonic dopamine levels leading to excessive reactivity to account proposes that the additional variability provided environmental stimulation [33,34]. If the firing probabil- by the noise interacts with the weak signal pushing it ity or gain parameter is low, neurons will fire at random above the detection threshold, see review in [14]. For yielding poor cognitive performance. If the gain para- instance, SR has been found in several modalities; audi- meter is high there will be cognitive stability and thus tion [15], vision [16], and touch [17] where stochastic high performance. This responsiveness of neurons is noise improves sensory discriminability. Recently SR has modulated via dopamine that enhances the differentia- been shown to work across modalities, for example when tion between efferent firing and afferent external stimu- auditory noise improves visual signal detection [18]. lation. It has been shown recently that neural noise Most SR studies have used perception tasks, requiring related to dopamine tone is an integral part of inter- the detection of weak peripheral sensory inputs. Few neuronal communication and that a sufficient level of studies have examined how noise influences cognitive noise may be necessary for normal function in the performance. Recent empirical evidence suggests that SR nervous system [21,35], through the process of SR. That can also improve central processing and cognitive perfor- is, there exists both external noise - outside of the ner- mance. For example, SR has been found in cognitive vous system - and neural noise (related to dopamine tasks where auditory noise improved the speed of arith- tone) inside the system. metic computations [19] and recall on visual memory The moderate brain arousal model (MBA) [13], upon tasks [20]. Thus, adding noise to the input of the infor- which the current study is based, is a neurocomputa- mation processing system can increase its signal-to-noise tional model that relies on classic conditions for output. SR is usually quantified by plotting detection, or stochastic resonance and the modulating properties of cognitive performance, as a function of noise intensity. dopamine-related gain and neural noise in determining This relationship follows an inverted U-curve function, neural responsivity. It suggests that the hypodopaminer- where performance peaks at a moderate noise level. That gic brain need higher input noise to function to its full is, moderate noise is beneficial for performance whereas potential. Thus the model suggests that external white too little, or too much, noise attenuates performance. For noise could compensate for behavioral dysfunction con- extensive reviews on the influence of noise on the nected to conditions caused by impaired dopamine trans- nervous system the reader is referred to recent reviews mission. Accordingly, ADHD children or low attentive [14,21]. Also detrimental effects of noise on the nervous children more generally have a low gain parameter owing system and in particular on speech processing are to low levels of baseline dopamine neuron firing. Neuro- reported in a recent review [22]. computationally the MBA model shows that more exter- nal environmental noise is required for optimal Individual differences in the SR effect performance in cognitive tasks for such low gain “indivi- The novel aspect of the proposed framework is that the duals” compared to high gain “individuals”. Accordingly, SR phenomena differs between individuals and these external noise, it is predicted by the model” will Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 3 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 compensate for reduced neural background activity in (WCST). In another study on healthy controls by Mattay ADHD. That is to say that increased levels of external et al. [42] dextroamphetamine was found to increase auditive noise can activate internal noise and restore the N-back working memory performance in group with low activity level. Further, given the inverted U function that baseline working-memory capacity, whereas the perfor- operates in relation to noise and performance in SR, the mance worsened in a group with high baseline perfor- MBA model also predicts that levels of background noise mance [42]. Dextroamphetamine also had differential that might be beneficial for ADHD children would be effects on the BOLD fMRI response on these groups. detrimental for those with normal attention. Crucially, These findings have been corroborated in a study using a the beneficial effects are not specific to ADHD (Figure 1): spatial working memory task where stimulant medication they are also found in dopamine-related neurodegenera- only improved memory performance in healthy indivi- tive disorders such as: akinesia [36], Parkinson’s disease duals with low baseline working memory capacity [43]. [37] and in aging [38]. These effects have been modeled This was also mirrored by increased cerebral blood flow in terms of age dependent dopamine loss [39]. in dorsolateral prefrontal cortex and posterior parietal In this paper we investigate, for the first time, how cortex. Taken together these studies indicate that dopa- noise influences cognitive performance in a normal, non- mine function influences performance and brain activity clinical, group of children that differ from each other in differently also in groups consisting of healthy controls their attentional abilities. Recent evidence suggests that depending on tasks that are linked to attention and work- dopamine plays a role in attention also in non-clinical ing memory (e.g., WCST, N-back, spatial working mem- groups. When a visual orienting task was used to study a ory). This body of data is consistent with the view that normal group of children, it was found that those chil- ADHD and related attentional problems is best concep- dren who were homozygous for alleles influencing dopa- tualized as a continuum rather than a discrete category mine transportation displayed inattention on left-hand and that ADHD symptoms are distributed in populations sided stimuli, whereas those who were heterozygotes did [44]. The syndrome of ADHD represents a transition of not [40]. The response to amphetamine has also been degree rather than of a kind and diagnostic thresholds found to be influenced by genetic factors; it depends on are therefore somewhat arbitrary resting on general and the functional polymorphisms of the Catechol O-methyl- cultural norms about behavior and development [45]. transerase (COMT) gene in a normal population of In addition, a comparison of the extreme points in a nor- humans. Mattay et al. [41] found that amphetamine mal distribution shows the same heritability patterns as a enhanced prefrontal efficiency measured by fMRI for the comparison between ADHD and control [46]. This, in val/val (high DA metabolism) genotype, whereas met/ turn, suggests that non-clinical persons with low and met (low DA metabolism), had no such effect on low to high attention may show similar effect from noise as medium workload, and decreased efficiency on high ADHD and control persons do. workload tasks. Furthermore, preservations errors were In this paper, we study inattentive and normally atten- decreased by amphetamine in the val/val, but not the tive children’s episodic memory in a verb-noun sentence met/met groups, in a Wisconsin Card Sorting Test recall task under two conditions varying in terms of the Figure 1 Individual difference in SR curves. Note. Performance on cognitive tests (y-axis) is optimal for moderate noise levels (x-axis), and attenuated for both too low and too high noise levels. More noise is required for optimal performance in inattentive or low performing children compared to attentive or high performing children. Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 4 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 levels of background auditive white noise. Our predic- sentences in each list. Each sentence consisted of a tion is that in the low noise condition the inattentive unique verb and a unique noun (e.g., “roll the ball”)in children will perform less well than attentive children Norwegian. The sentences were placed in random order. while in the high noise condition these differences List-order (1-8) and condition-order (no noise vs. noise) should diminish as the addition of white noise benefits were counterbalanced and noise was present on every the inattentive but not the normally attentive children. second list. All to-be-remembered sentences were recorded on a CD. A new item was read every 9th sec- Methods ond. The sentences were read in both the low noise and Participants the high noise condition. The equivalent continuous Fifty-one secondary school pupils (25 boys and 26 girls) sound level of the white noise was 78 and the speech between 11-12 years (M = 11.7) participated in the signal was 86 dB; thus the signal-to-noise ratio was study. The group consisted of children from two school 8 dB. The signal was sufficiently strong so that all parti- classes, year seven (86% of children participated). Parti- cipants could perceive the content of the words in both cipants where divided into two groups after their atten- conditions without error (i.e., the tests were a cognitive tion abilities were assessed by teachers using a seven memory test and not a perceptual test). The two noise point Likert scale. The assessment scale is the same as levels were chosen to correspond to levels that have that used in the longitudinal research program Indivi- been found in earlier studies to affect cognition in an dual Development and Adaptation [47]. Participants arithmetic’s test for a normal population [19] and work- that scored high (6 or 7 - severe problems in the class ing memory performance in patients with Alzheimer’s room) on inattention where assigned to the inattentive disease [4]. Recordings were made in a sound studio. group. This group consisted of 10 participants, 6 of them also scored high on hyperactivity as evaluated by Procedure the teachers. The comparison group comprised the The testing was conducted at the child’s school, following remaining 41 children thatscored5or loweratthe permission from parents and children. The University scale, and were assessed as average- or highly attentive. College of Sogndal, Norway and the regional ethic board None of the inattentive group had an ADHD diagnosis in Stockholm approved the study. The participants were and none were treated with medication. Achievements tested individually in a room during the school day. The and scholastic skills (3 point scale) and reading ability test lasted for about 45 minutes including the presenta- (7 point scale) used in [47] were also rated by their tea- tion of instructions. Before starting the experiment chers. Children’s school achievement was assessed in proper, two practice sentences were presented. The time terms of whether their school performance was at the taken to present each list was approximately 1 minute level expected for this age group. General cognitive skills and 40 seconds. The to-be-remembered sentences were and reasoning ability were assessed using the Raven’s presented concurrent with continuous white noise during progressive matrices test [48]. The Raven’s test assesses the encoding phase in the high noise condition and in learning and problem solving ability and correlates silence in the low noise condition. Noise conditions highly with the g-factor in IQ tests. Forward and back- changed after every sentence list in outbalanced order. ward digit span measuring short-term and working No noise was presented during retrieval. Directly after memory respectively were assessed. Table 1 shows the presentation of the last item in a list, participants results from these tests for the high and low attentive performed a free recall test in which they spoke out loud groups as well as other background characteristics of as many sentences as possible, in any order. these groups. The groups were well matched on school performance and general cognitive ability - the inatten- Results tive group had less developed reading skills. Recall performance A 2 × 2 mixed ANOVA was conducted with one Design between-subject factor, Group (normal attention vs inat- We used a 2 × 2 design, where noise levels (low versus tentive) and one within-subjects factor, encoding condi- high) was the within participant manipulation and the tion (low noise vs high noise). We choose the standard between group variable was teacher rated classroom scoring procedure in the action memory literature attention level (normal versus inattentive). [10,49], where strict scoring is used for the nouns (exact matches were required) and lenient scoring is used for Materials verbs (where non-exact matches are scored as correct). All participants undertook a verbal episodic recall test. This is because nouns are typically recalled somewhat The to-be-remembered (TBR) items consisted of 96 sen- more easily than verbs [50]. There where no main effects tences divided into 8 separate lists with 12 verb-noun of noise (F(49,1) = .01, p =.94)orgroup (F(49,1) = .30, Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 5 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 Table 1 Participant characteristics and cognitive test scores Cognitive and behavioral measures Attentive group Inattentive group Attentive vs. Inattentive N= 41 N=10 (20 boys, 21 girls) (5 boys, 5 girls) Mean SD Range Mean SD Range t-test score Inattention 2.8 (1.6) 1 - 7 6.2 (0.4) 1 - 7 t(49) = 6.67*** (1 = low, 7 = high) Hyperactivity 2.5 (1.6) 1 - 7 4.9 (2.0) 1 - 7 t(49) = 4.11*** (1 = low, 7 = high) School performance 2.3 (0.7) 1 - 3 2.1 (0.7) 1 - 3 t(49) = 0.94 (1 = below, 2 = average, 3 = above) Reading skill 5.0 (2.0) 1 - 7 3.5 (1.7) 1 - 7 t(49) = 2.38* (1 = low, 7 = high) Raven score 41.2 (8.6) 16 - 55 37.3 (10.6) 19 - 53 t(49) = 1.09 Digits forward 23.1 (9.1) 4 - 42 15.0 (6.6) 4 - 23 t(49) = 3.22** Digits backwards 14.9 (6.9) 2 - 34 13.2 (4.2) 7 - 18 t(49) = 0.97 Note: * p < .05, ** p < .01, *** p < .001. p = .59). Both groups performed at the same level overall group (M = .46 vs. .41). Inattentive children performed across the two conditions. However, the interaction better in the high rather than the low noise condition between noise and group was significant (F(49,1) = 9.96, (t(9) = 1.84, p = .05 one-tailed). The opposite was p = .003, eta = .17) (Figure 2). This interaction was the case for the normally attentive group (t(40) = -3.46, further explored with planned simple contrasts for the p = .001). Using attention (score 1-7) and noise-effect within subjects factors, using paired sample t-tests. Con- (noise - no noise) as variables a Spearman rank-order sistent with the hypothesis the addition of white noise correlation revealed positive correlation between atten- enhanced performance for the inattentive group (M = .39 tion and noise (r = .378, N = 51, p = .006; a medium vs..44),and impaired performance for the attentive effect size according to Cohen’sd). Thehigherscore on Figure 2 Recall performance as a function of noise and attention; inattentive vs. attentive children (teachers judgments: attentive N = 41; inattentive: N = 10). Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 6 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 inattention the larger was the positive effect of noise and auditive white noise may have its effects either at a per- vice versa, attentive children performed worse in pre- ceptual or neuro-psychological level or may operate a sence of noise. neuro-chemical level directly altering levels of dopamine As reported above the two groups differed with respect release [13,51]. Animal models of dopamine function or to reading skills, as judged by teachers; with the inatten- pharmacological probes to manipulate tonic and phasic tive group having inferior reading skills compared to the dopamine are called for to investigate these effects. attentive group. However, when reading ability was Stimulant medication (e.g. methylphenidate) also added as a covariate to the main analysis the original improves cognitive performance in children with ADHD interaction effect, although diminished, persisted (F(48,1) [52,53]. This medication increases dopamine levels by = 7.13, p = .010). Reading level was independently related blocking the dopamine transporter [54]. Low performing to performance (F(6,1) = 1.46, p = .213). A Spearman’s healthy controls also benefit from increased dopamine rank order correlation revealed negative correlation transmission, which is manifested in improved cognitive between reader skills and positive effect of noise (r = performance and increased prefrontal cortical activity .335, N = 51, p = .016), a positive correlation between [43]. Our data show that auditory white noise may exert attention and reading ability (r = .498, N = 51, p < .001) potentially similar effects on cognition as medication and finally, a high positive correlation between teacher through the phenomenon of stochastic resonance (SR). ratings of inattention and hyperactivity (r =.789,N=51, White noise is characterized by randomness and so p < .001). However, there was no correlation between introduces variability in the nervous system [14]. hyperactivity and noise-effect (r = .141, N = 51, p = .323). A poorly tuned neural system benefit from additional white noise. In fact, the stochastic resonance theory pre- Discussion dicts that noise that is applied to the signal as an input We have proposed a framework for understanding indi- to a neural cell, improves the signaling efficiency of the vidual difference in the facilitative effects of auditive output of that cell, where the non-linearity in the firing white noise on performance. As predicted the results threshold of the neural cells is the key to improvement show different effects of noise in attentive and inatten- of the signal to noise ratio [14,55]. tive children selected from the normal population. Despite the fact that it appears that noise and methyl- There was significant improvement in performance for phenidate both improve cognitive performance, the under- the children rated as inattentive by their teachers, and a lying mechanism that is the basis of these phenomena are significant decline in performance for those rated as likely to be different. According to the model theoretically attentive as noise levels were increased. Furthermore speaking the difference between these phenomena is clear. these effects seem independent of other factors mea- Methylphenidate changes the strength (but not the varia- sured in the study - attentional ability seems to be a key bility) of the input, which is typically modeled by the gain marker of this effect. Even if inattention and hyperactiv- parameter in abstract neural networks [23]. In contrast, ity are strongly correlated, no correlation between noise changes the variability of the input (but per defini- hyperactivity and a positive noise effect was found, this tion does not influence the strength) of the input. How- suggests that in this study inattention is the key factor ever, despite these clear differences in the underlying level, to explain noise improvement. These results are similar the behavioral outcome may be similar, and the two to those previously reported with ADHD patients [10]. mechanisms interact in a complex way, making it difficult Here we discuss theoretical and practical implications of to distinguish the phenomena at the behavioral level [56]. these findings. Furthermore, direct evidence of difference between these From a theoretical point of view the findings are con- levels is emerging. Pålsson and Söderlund et al. (Noise sistent with the suggestion that the neural noise level benefit in pre-pulse inhibition of the acoustic startle reflex, associated with dopamine tone in inattentive children is submitted) studied the effect of methylphenidate, dopa- sub-optimal, see also [13] and that noise may enhance mine and noise on the startle response in a rat model of performance through the phenomenon of stochastic ADHD. They found that both control and ADHD strains resonance (SR). According to the model developed here, (SHR) benefited from noise; however, this effect was also noise in the environment yields an input to the percep- found in dopamine lesioned rats, suggesting that dopa- tual system, which can either compensate for low noise mine is not a necessary requirement for the stochastic in the neural system leading to an output consisting of resonance phenomenon to occur. improved cognitive performance, or, depending on pre- Another theoretical interpretation of the data is that existing levels of neural noise, can add too much to an noise in a general way increase arousal that makes the already well functioning system. The specific neuro- subject more alert, and less drowsy. The optimal stimu- biological and neuro-chemical mechanisms responsible lation model states that hyperactivity is as a homeostatic for these effects need further research. For instance, response to underarousal in order to achieve an optimal Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 7 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 arousal level [11]. However, this model does not make around 100 dB [62-64]. In later experiments by Broad- any explicit predictions about the selective effects of bent and colleagues, (memory recall of unrelated words) external stimulation whereas in the current study inat- lower noise levels (80-85 dB) were used; results showed tentive persons benefited from extra stimulation and no effects of noise on memory when exposed during the attentive children did not. In the cognitive energetic encoding phase but deteriorating results if exposed dur- model state factors like arousal, activation and effort are ing the recall phase [65,66]. More recently, episodic taken into account to explain shortcomings in ADHD memory has been found to be particularly vulnerable to patients [57]. According to this model state factors can speech noise, whereas traffic noise showed no effect [2]. be moderated by event rate (inter-stimulus-intervals, Results from the present study would indicate that the ISI) and workload in cognitive tasks both under- and effects of external noise would have look quite different over arousal can be produced. Recent research has in many of these studies if participants had been divided shown that stimulant medication (methylphenidate) and into attentive and inattentive or young and elderly, that shortened event rate can produce the same effect in a is high and low gain participants (tentatively high/low Go-Nogotask[58].Fromour pointofviewthe term dopamine groups). Selective effects of noise can easily arousal is poorly defined in the literature, and could be get hidden in group-means if some participants improve interpreted in terms of wakefulness or in term of neural and others are impaired. Our data may encourage noise arousal. To fully investigate the arousal-noise hypothesis researchers to reanalyze their experiments dividing par- an experiment would have to be designed where physio- ticipants by individual differences in attention and per- logical arousal is explicitly manipulated and measured. formance. Preliminary data from our lab, on an ADHD We arguethatthatproposedframework,including the rat model provide further support for the benefits of dopaminergic influence on stochastic resonance, pro- adding white noise. The Spontaneous hypertensive rat vides a more elaborated view both at the neural and at (SHR)showedimprovedsensorimotorgatingbyshow- the behavioral level. To account for the current data an ing more a pronounced pre-pulse inhibition of the star- arousal view would have to argue for a selective lower tle reflex when exposed to white noise as compared to arousal for the inattentive children. Finally, our experi- control strains, even though control rats also increased ence is that the subjects in our experiment are fully their inhibition in noise conditions (Pålsson, Söderlund aroused, the testing conditions at hand are very stimu- et al., Noise benefit in pre-pulse inhibition of the acous- lating, and subjects are very motivated to perform well. tic startle reflex, submitted). By highlighting the role of individual differences in the Reading disability is a common co-morbidity in ADHD. facilitative effects of auditive noise the current study Consistent with these findings, our data show lower read- refines our understanding of SR. SR exhibits an inverted ing skill for the inattentive group. Reading disability is also U-curve function, where performance peaks at a moder- linked with reduced short-term verbal memory that ate noise level. However, this is an oversimplification, as requires phonetic coding of material, but not necessarily there is no absolute sense in which a moderate noise with executive functions or long-term memory [67,68]. level is optimal. An “optimal” noise level for one indivi- This is also consistent with our data that show a lower dual could be either too high, or too low amount of performance in the digits forward task that measures noise for another individual. These complex interactions short-term memory, but no deficits for digits backward between noise and performance may account for some task that is related to working memory capacity. The of the contradictory findings in the previous literature. MBA model accounts for these findings because the digits For example, earlier research on noise in normal popu- backward task is a more demanding task leading to higher lations has shown both enhancing and diminishing brain arousal and thus good performance for inattentive effects of auditory white noise on cognition in non- children, whereas the less demanding digit forwards task clinical groups (90 dB) on simpler, short-term memory does not sufficiently arouse the brain for the low attention tasks like anagrams, whereas speech noise was detrimen- children [13]. Additionally, the positive correlation tal [59]. These noise effects also interacted with other between reading ability and noise enhancement suggests variables such as gender and time of the day [60], which that white noise may enhance awareness. This is consis- makes these results equivocal. No effect of white noise tent with the idea that dyslexia is caused by phonological was found in digit span recall in two experiments, deficits [69], however, a further investigation of phonologic whereas speech noise had a detrimental effect [4,5]. awareness is outside the scoop of the present study. However, noise improvement was found in a simple addition task in selected groups, elderly and young par- Limitations ticipants [61] and among elderly and Alzheimer patients Thecurrent studyhas anumberoflimitations.First, [4]. In Broadbent’s early research negative effects of ratings of academic attainment and reading were based noise have been found using high (excessive) noise levels on single item non-validated scales. Second, only two Söderlund et al. Behavioral and Brain Functions 2010, 6:55 Page 8 of 10 http://www.behavioralandbrainfunctions.com/content/6/1/55 Author details noise levels were investigated. It would be interesting to 1 2 Department of Linguistics, Stockholm University, Sweden. Linné University, include different levels so that the entire stochastic reso- 3 4 Växjö, Sweden. Sogn and Fjordane University College, Norway. University nance curve can be mapped out. One prediction from of Southampton, Dept. of Psychology, UK. Department of Experimental Clinical and Health Psychology, Ghent University, Belgium. our model is that in attentive group, a subset of partici- pants will benefit from noise when levels are individually Authors’ contributions adjusted. Furthermore, it would be of interest to investi- GS planned and designed the experiment, performed the statistical analysis and drafted the manuscript. SS have been involved in drafting and revision gate if the SR effect is dependent on task difficulty. of the manuscript. LML was responsible for the data collection. ESB have Third, only one test of cognitive ability was tested. been involved in revising the manuscript critically for important intellectual Future research may study whether the effects found content. All authors read and approved the final manuscript. here generalizestoother taskssuchasexecutive and Competing interests inhibitory functions. This is of particular importance The authors G. Söderlund, S. Sikström and, J-M. Loftesnes declare that they while investigating the possibility of noise, as an inter- have no competing interest. Financial disclosures and conflicts of interest statement E. Sonuga-Barke: vention in ADHD. A final limitation of the present Recent speaker board: Shire, UCB Pharma study is that the experiment was not designed to study Current & recent consultancy: UCB Pharma, Shire differential effects of noise on study and recall. The Current & recent research support: Janssen Cilag, Shire, Qbtech, Flynn Pharma experiment manipulates noise at encoding, but not at Advisory Board: Shire, Flynn Pharma, UCB Pharma, Astra Zeneca retrieval, so the effects of noise seen can only be attribu- Conference support: Shire ted to the conditions at encoding. To what extent noise Received: 2 March 2010 Accepted: 29 September 2010 presented at recall influences performance cannot be Published: 29 September 2010 determined by the experiment. However, the MBA pre- dicts that the conditions where noise is beneficial during References encoding should also be beneficial for performance dur- 1. Broadbent DE: The effects of noise on behaviour. Elmsford, NY, US: Pergamon Press, Inc 1958. ing retrieval. At same time it may be difficult to directly 2. Boman E, Enmarker I, Hygge S: Strength of noise effects on memory as a compare encoding and retrieval conditions, because the function of noise source and age. 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Papageorgiou C, Giannakakis GA, Nikita KS, Anagnostopoulos D, Papadimitriou GN, Rabavilas A: Abnormal auditory ERP N100 in children with dyslexia: comparison with their control siblings. Behav Brain Funct 2009, 5:26. doi:10.1186/1744-9081-6-55 Cite this article as: Söderlund et al.: The effects of background white noise on memory performance in inattentive school children. Behavioral and Brain Functions 2010 6:55. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

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Behavioral and Brain FunctionsSpringer Journals

Published: Sep 29, 2010

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