International Journal of Psychophysiology 79 (2011) 97–105

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International Journal of Psychophysiology

j ourna l homepage: www.e lsev ie r.com/ locate / i jpsycho

Effects of aging on habituation to novelty: An ERP study

Cassandra Richardson a,b,⁎, Romola S. Bucks a,b, Alexandra M. Hogan c

a School of Psychology, University of Southampton, UKb Neurocognitive Development Unit, School of Psychology, University of Western Australia, Western Australia, Australiac Developmental Cognitive Neuroscience Unit, UCL Institute of Child Health, UK

⁎ Corresponding author. Neurocognitive DevelopmeUniversity of Western Australia, 35 Stirling Highway, CraAustralia. Tel.: +61 8 6488 4652; fax: +61 8 6488 100

E-mail address: cassie.richardson@uwa.edu.au (C. Ri

0167-8760/$ – see front matter. Crown Copyright © 20doi:10.1016/j.ijpsycho.2010.09.007

a b s t r a c t

a r t i c l e i n f o

Article history:Received 7 June 2010Received in revised form 16 September 2010Accepted 17 September 2010Available online 24 September 2010

Keywords:AgingNoveltyHabituationERPsP3Attention

Age-related effects on novelty processing have been reported and are linked with changes in frontal lobefunctioning. Auditory novelty processing and habituation of the novelty P3 event-related potential wereinvestigated in younger and older adults. Novelty processing, as indexed by novelty P3 amplitude, was similarbetween the groups. We found the expected decrease in novelty P3 amplitude at frontal regions in youngeradults with repetition of novel stimuli. In contrast, older adults displayed no evidence of habituation, rather anincrease in novelty P3 amplitude at frontal sites was found when novel stimuli were repeated. We extendcurrent understanding of novelty processing in normal aging by comparing this habituation related-hyperfrontality with intellectual functioning.

Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.

1. Introduction

Adaptive cognitive functioning depends on the ability to detect,locate and process important stimuli against a background ofenvironmental noise. In particular, novel or unexpected stimulirequire further processing due to the potential for such stimuli tosignal danger (Friedman et al., 2001). The efficient processing of novelstimuli is, thus, important for learning (Ranganath and Rainer, 2003),and consistent with this, has been shown to enhance memoryretrieval (Kishiyama et al., 2009). Repetition of novel stimuli isassociated with rapid habituation, the process by which novel stimulibecome familiar or learnt (Courchesne et al., 1975; Yamaguchi et al.,2004). Novelty processing and habituation involves widely distribut-ed neural circuits including the prefrontal cortex and the medialtemporal lobe (e.g. Daffner et al., 2000; Knight, 1984; Strange andDolan, 2001; Yamaguchi et al., 2004), and is constrained by braindamage involving these areas (Daffner et al., 2000; Kishiyama et al.,2009; Knight, 1984). More subtle change in brain morphology occurswith normal aging, for example, affecting the prefrontal cortex (Raz,2000) and potentially its connections (Damoiseaux et al., 2009),suggesting that novelty processing might also be altered withincreasing age, irrespective of brain damage. A variable effect ofnormal aging on novelty processing has been reported, with somestudies suggesting less efficient novelty processing (e.g. Friedman

nt Unit, School of Psychology,wley 6009, Western Australia,6.chardson).

10 Published by Elsevier B.V. All rig

et al., 1993, 1998; Friedman and Simpson, 1994) whilst othersdemonstrate stability or even improvement (e.g. Daffner et al., 2006;Riis et al., 2008). Nonetheless, there is consensus that such changereflects age-related modification to frontal lobe function (Daffner etal., 2006; Friedman et al., 1998; Friedman and Simpson, 1994;Friedman et al., 1993; Riis et al., 2008). However, there is littleempirical support for a direct relationship between novelty proces-sing and frontal lobe functioning.

Electrophysiological investigations of novelty processing andhabituation employ novelty oddball tasks in which unexpectednovel stimuli are randomly interspersed with frequent irrelevantstimuli and infrequent target stimuli. The P3b is elicited by targetstimuli, and is associated with the updating of mental representationsof stimuli (Donchin and Coles, 1988). More specifically, the amplitudeof the P3b is considered to index the allocation of attention toinformation processing, whilst the latency provides a measure of thetiming of this processing (Polich, 1996). Infrequent irrelevant stimuliin three-stimuli and novelty oddball tasks elicit the P3a and noveltyP3, respectively (Comerchero and Polich, 1999; Spencer et al., 1999).The P3a and novelty P3 occur at ~250 ms and havemore anterior scalpdistributions compared to the P3b. However, there are few differencesbetween these components (see Simons et al., 2001), and in a recentreview, it was concluded that the P3a and novelty P3 were “variants ofthe same ERP that var[y]...as a function of attentional and taskdemands” (Polich, 2007, p. 2134). In the current study, we use theterm novelty P3 to refer to the P3 elicited by novel stimuli; thisnomenclature is in line with other studies employing a noveltyoddball paradigm (Courchesne et al., 1975; Cycowicz and Friedman,1997; Daffner et al., 2006; Fabiani and Friedman, 1995; Friedman

hts reserved.

Table 1Demographic information and behavioural data.

Younger (n=13) Older (n=14) d

Age 20.3 (3.6) 69.1 (7.1) 9.12MMSE 29.0 (0.9) 29.0 (0.8) 0.00MoCA 28.3 (1.4) 28.1 (1.2) 0.16NART predicted IQ 102.8 (6.4) 120.7 (4.5) * 3.34Years of education 15.1 (2.4) 13.0 (2.1) * 0.97Raven Matrices 39.8 (3.1) 39.7 (3.2) 0.03HADS Anxiety 7.0 (2.4) 7.6 (2.7) 0.24HADS Depression 4.0 (1.2) 6.4 (2.2) * 1.39Target hits (%) 96.3 (5.1) 92.7 (9.8) 0.47Target RT (ms) 427.3 (40.9) 451.1 (56.9) 0.50Novel false alarms (%) 4.3 (6.1) 6.0 (5.2) 0.31Standard false alarms (%) 0.3 (0.3) 1.5 (1.7) * 1.00

Note. Mean (SD); * pb0.05 younger vs. older adults; MMSE=Mini Mental StateExamination, Folstein et al. (1975); MoCA=Montreal Cognitive Assessment,Nasreddine et al. (2005); National Adult Reading Test, 2nd edition, Nelson andWillison (1991); Raven Matrices (raw scores=0–48; Sets A–D)=Raven's standardprogressive matrices, Raven et al. (2000); HADS (0–21; clinically significantthreshold≥11) = Hospital Anxiety and Depression Scale, Zigmond and Snaith (1983).

98 C. Richardson et al. / International Journal of Psychophysiology 79 (2011) 97–105

et al., 1993, 1998, 2001; Friedman and Simpson, 1994; Riis et al.,2008). The novelty P3 represents immediate attention to the stimulus,but not memory processing per se (Friedman et al., 2001). In support,Escera, Yago and Alho (2001) described a frontally distributed noveltyP3a component occurring at ~320 ms that was associated withorienting to novel stimuli. Convergent evidence from fMRI andintracranial ERP studies has indicated that widely distributed net-works involving the bilateral superior and middle frontal gyrus,temporal-parietal junction, hippocampus, cingulate gyrus and fusi-form gyrus are likely to contribute to the novelty P3 scalp signal(Baudena et al., 1995; Bledowski et al., 2004; Friedman et al., 2009;Halgren et al., 1995; Kiehl et al., 2001; Yamaguchi et al., 2004).

Novelty P3 amplitude is typically reduced (Fabiani and Friedman,1995; Friedman et al., 1993, 1998; Friedman and Simpson, 1994), andnovelty P3 latency increased (Czigler et al., 2006; Fabiani andFriedman, 1995; Friedman et al., 1993; Weisz and Czigler, 2006) inolder compared to younger age groups. In both younger and olderadults, the novelty P3 has an increased anterior distribution comparedto the parietally distributed P3 elicited by target stimuli. However, thetopography differs between the age groups. In younger adults, noveltyP3 amplitude increases from frontal to parietal regions, in contrast,novelty P3 amplitude is similar acrossmidline locations in older adults(Fabiani and Friedman, 1995; Friedman et al., 1993, 1998; Friedmanand Simpson, 1994). In otherwords, these studies indicate that noveltyprocessing is attenuated and delayed with increasing age, but that thesame underlying neural networks are likely to be involved.

The N2b has also been investigated to address the potentialconcern that the delay in the P3 found in older adults is due to delayedearlier processing (e.g. Czigler et al., 2006; Riis et al., 2008; Weisz andCzigler, 2006). More recent studies have found that novelty P3amplitude was actually increased in high-functioning older adultscompared to average-functioning older adults: a finding that wasexplained by compensatory recruitment of other neural networksinvolving the frontal lobes (Daffner et al., 2006; Riis et al., 2008).Indeed, P3 amplitudes have been linked with performance on theMatrices subtest of the Wechsler Abbreviated Scale of Intelligence(WASI) in older adults (e.g. Fjell and Walhovd, 2001, 2003). It shouldbe acknowledged, however, that a direct comparison between thedifferent aging and novelty processing studies is limited by method-ological differences. For example, Daffner and colleagues used amodified visual oddball paradigm, whilst others have administeredauditory paradigms (e.g. Fabiani and Friedman, 1995; Fabiani et al.,1998; Friedman et al., 1993, 1998; Friedman and Simpson, 1994;Knight, 1984).

Habituation to novel stimuli can be examined by averaging thenovelty P3 according to the first presentation of the stimulus and theneach repetition of the same novel stimulus. By this means, habituationhas been consistently found in younger adults (e.g. Cycowicz andFriedman, 1997; Cycowicz et al., 1996), evidenced by reduction innovelty P3 amplitude at fronto-central locations with increasing timespent on task, and suggests a process of rapid familiarisation(learning) of novel stimuli. Interestingly, this pattern of activity hasnot been found in older adults (Friedman et al., 1993, 1998; Friedmanand Simpson, 1994; Weisz and Czigler, 2006). The lack of habituationof the novelty P3 in older adults has been interpreted as an inability toconstruct a “novel category template” (Friedman and Simpson, 1994,p. 62), with older adults treating repeated novel stimuli as new(Fabiani and Friedman, 1995; Friedman and Simpson, 1994). To ourknowledge, ERP studies conducted with older adults have not, thusfar, considered the possibility that lack of novelty P3 attenuationwith increasing time spent on task, is, like the novelty P3 in general(cf. Daffner et al., 2006; Riis et al., 2008), sensitive to level of cognitivefunction. Such information is important for interpreting the relevanceof novelty habituation for everyday cognitive function.

The current study thus aimed to examine relationships betweenthe novelty P3 elicited by repeated novel stimuli and a neuropsycho-

logical measure of intellectual function that involves solving problemsbased on novel information, the RSPM (Raven et al., 2000). Thesecondary aim of the study was to provide convergent evidence forthe effects of repetition of novel stimuli on the novelty P3 in a group ofolder and younger adults. Evidence that age-related change inhabituation of novelty ERP activity is associated with level ofbehavioural performance would extend the current habituationliterature by indicating its relevance for everyday functioning.

2. Method

Approval for the study was given by the Human Research EthicsCommittee of the School of Psychology, University of Southampton,UK. Written informed consent was provided by all participants.

2.1. Participants

The demographic profile of the participant groups is presented inTable 1. The older adults (OA) were recruited from a researchvolunteer database (Exploring the Mind, directed by RSB, School ofPsychology, University of Southampton, UK). The younger adult (YA)participants were recruited opportunistically from the University ofSouthampton, and received course credits in return for theirparticipation. All participants were healthy at the time of testing,had no self-reported history of neurological or psychiatric conditions,normal or corrected-to-normal vision and hearing and, if onmedication, had been taking stable dosages for the preceding3 months. All participants underwent a hearing assessment prior totesting. Where there was mild-to-moderate hearing loss in one orboth ears (25–45 dB, and 45+dB, respectively), the sound pressurelevel was adjusted to compensate.

2.2. Measures

2.2.1. Novelty auditory oddball paradigmAuditory stimuli were presented via headphones. Sound pressure

levels of stimuli (65 dB: level 1≤25 dB loss; 75 dB: level 2=25–40 dBloss; 85 dB: level 3≥40 dB loss) were set for each participantdepending on their hearing threshold level (YA: level 1, n=13; OA:level 1, n=11; level 2, n=2; level 3, n=1). Stimuli (200 ms, 5 msrise and fall time) were pure sinusoidal tones: standard tone (1 kHz,0.8 probability) and target tone (1.5 kHz, 0.1 probability), andcomputer-generated novel sounds (e.g. dog bark, drum beat, carhorn, 0.1 probability), with stimulus-onset-asynchrony of 900 ms. Atotal of 48 novel stimuli were presented in the paradigm. Fourteenunique novel stimuli were presented at different intervals throughout

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the task, and each was randomly repeated up to four times during theparadigm, facilitating an exploration of habituation to novel stimuli.Participants were requested to press amouse button upon hearing thetarget tone, but were not informed about the novel stimuli. A practicetrial of eight standard tones randomly interspersed with four targettones was administered to ensure that participants could discriminatebetween the tones and understood the instructions. All participantswere able to perform the practice trial successfully on the firstattempt.

2.3. ERP acquisition and processing

The EEG was recorded using NeuroScan SynAmps™ amplifiers at asampling rate of 500 Hz (band-pass 0.05–70 Hz) with an Easy-Cap™fitted with 24 electrodes positioned according to the International 10-20 system (Fp1, Fp2, F7, F3, Fz, F4, F8, FC1, FCz, FC2, T7, C3, Cz, C4, T8,CP1, CP2, P7, P3, Pz, P4, P8, O1, O2), using a ground lead situated at Fp1,and a linked-mastoid reference. Impedance was maintained at lessthan 10 KΩ. Vertical (right eye) and lateral ocular electrodes enabledoffline blink reduction according to a standard algorithm (Semlitschet al., 1986). EEG data were divided into epochs of −200 to 1000 mscentred on presentation of stimuli, baseline corrected at−200 to 0 ms,and automatically artefact-rejected at ±100 μV. Epochs associatedwith novel stimuli were averaged in two ways: firstly, across all novelstimuli, irrespective of repetition, and secondly, by repetition of thepresentation of the novel stimuli (e.g. first time a particular novelsound is heard=Novel 1, second time the same novel sound isheard=Novel 2, Novel 3 and Novel 4) in order to explore noveltyhabituation. This factor was labelled time. The mean number of trialsacross groups were 13.30 (1.2 SD), 11.44 (1.0 SD), 8.56 (1.1 SD), and7.41 (0.9 SD) for the first to fourth presentations, respectively.Importantly, the numbers of trials in each repetition waveform didnot differ between the groups [main effect − group: F(1,25)=0.56,p=.461, d=0.30; group X number of trials: F(3,75)=0.31, p=.762;d=0.22]. Although there were a smaller number of trials in Novels 3and 4, a discernable P3 was found in these waveforms (see Fig. 3).Moreover, these numbers of trials are comparable to Friedman andSimpson (1994). However, to address the possibility that thesewaveforms had a poor signal-to-noise ratio, a second habituationanalysiswas undertaken inwhich the first two and last two repetitionswere averaged together (Novel 1/2 andNovel 3/4). Themeannumbersof trials were 24.74 (1.8 SD) and 15.93 (1.6 SD), respectively, andagain there were no effects of group [F(1, 25)=0.47, p=.497,d=0.27; F(1, 25)=0.48, p=0.497, d=0.28, group and group Xtime, respectively]. The N2b is maximal at Fz, therefore, only this sitewas considered in the analyses. The N2b and P3 were identified as themaximum peak within a specific time frame: N2b (70–250 ms) at Fzand P3 (200–520 ms) at F7, F3, Fz, F4, F8, T7, C3, Cz, C4, T8, P3, Pz, P4.The P3 data were normalized using the root mean square method(McCarthy and Wood, 1985). ANOVA models to assess interactionswith electrode sites cannot differentiate between amplitude changesand topographic changes, thusMcCarthy andWood (1985) advocatedusing normalized data to investigate topography. The root meansquare method eliminates amplitude differences between conditionsand groups and topographic analyses were conducted with thesenormalized data.

2.4. Data analysis

The distributions of the data were assessed using the Shapiro Wilktest of normality. Behavioural responses madeb150 ms after stimuluspresentation were excluded from the analysis. Behavioural data wereinvestigated with Independent Samples t-tests. ERP data wereexamined using mixed-design ANOVA models: The amplitude andlatency of the P3 stimulus (x2: target, novel), and location (x3: Fz, Cz,Pz) as within-subjects factors and group (x2: younger and older

adults). Main effects of stimulus type and interactions with locationwere analysed separately using the normalized data with hemisphere(x2: left, right) and caudality (x5: F3/4, F7/8, C3/4, T7/8, P3/4) aswithin-subjects factors for each group separately, for the novelty P3and P3b, separately. For preliminary analysis of habituation to novelty,the ANOVA model included time (x4: Novel 1 {1st presentation},Novel 2, Novel 3, Novel 4) and location (x2: Fz, Pz) as within-subjectsfactors and Age-group. Due to the small number of trials in thewaveforms of Novel 3 and Novel 4, the analysis of habituationincluded time (x2: Novel 1+2 combined, and Novel 3+4 combined)and location (x2: Fz, Pz) and Age-group. A topographic analysis usednormalized data and included time (x2: Novel 1+2 combined, andNovel 3+4 combined), hemisphere (x2: left, right) and caudality (x5:F3/4, F7/8, C3/4, T7/8, P3/4) for each age group separately. Mid-lineanalyses were also conducted and the results were similar to thecaudality analyses, thus they will not be further described. Whereappropriate, the Greenhouse-Geisser corrected value is reported. TheBonferroni correction was used to adjust for multiple comparisons.

3. Results

3.1. Behavioural responses

Behavioural data are presented in Table 1. Target detection andreaction times to targets were equivalent across groups. The falsealarm rate to novel stimuli was also similar between younger andolder adults. In contrast, older adults responded erroneously tostandard stimuli more often than younger adults [t(25)=2.63,p=.014, d=1.00].

3.2. N2b component

There was a main effect of group, [F(1, 25)=6.13, p=.010,d=0.99] for N2b amplitude at Fz, which indicated that the amplitudeof the N2b elicited by target and novel stimuli was significantlygreater in younger compared to older adults. There were no latencydifferences between the groups (see Fig. 1).

3.3. Novelty P3 in relation to the P3 elicited by target stimuli

There were main effects of stimulus [F(1, 25)=17.48, pb0.001,d=1.67] and location [F(2, 50)=15.92, pb0.001, d=1.60] on P3amplitude (see Fig. 1). These results indicated that novel stimulielicited significantly greater amplitude compared to target stimuli.The main effect of location was explained by the fact that P3 am-plitude at both Cz and Pz was significantly greater than that recordedat Fz (all pb0.001). A location by group interaction [F(2, 50)=16.43,pb0.001, d=1.62] indicated topographic differences betweenthe younger and older adults, and a stimulus by location interaction[F(2, 50)=9.39, p = 0.001, d=1.23] revealed that the distribution ofthe P3 differed between the stimulus types. A series of plannedcomparisons revealed that older adults had lower P3b amplitudes atPz, but higher P3b amplitudes at Fz compared to younger adults (seeFig. 1). The lack of age-group effects indicated that the amplitude ofthe novelty P3 and P3b did not differ significantly between theyounger and older adults. There was a main effect of group for P3latency [F(1, 25)=7.78, p=.010, d=1.12], which showed that,regardless of stimulus type, the timing of the P3 was significantlyslower in the older adults.

3.4. Topographic analysis of novel stimuli

There was a main effect of caudality for the younger adults[F(4, 48)=28.11, pb0.001, d=2.12]. A series of post-hoc examina-tions revealed that the novelty P3 amplitude at the posterior location(P3/4) was significantly greater than at all of the other regions (F7/8,

Fig. 1. Grand average waveforms for target and novel stimuli for younger and older adults. Stimulus presentation occurred at time 0 ms.

100 C. Richardson et al. / International Journal of Psychophysiology 79 (2011) 97–105

F3/4 and T7/8: all pb .05). There were no significant effects in theolder adults, which indicated that novelty P3 amplitude was similaracross the scalp. These divergent age-group results indicated that thetopography of the novelty P3 was different between younger andolder adults.

3.5. Topographic analysis of target stimuli

There were significant main effects of caudality [F(4, 48)=31.89,pb0.001, d=2.26] on the amplitude of the P3b in the younger adults.Post-hoc examination again found that amplitude was maximal atposterior regions (P3/4). The lack of effects in the older adults

Younger

Adults

Older

Adults

Novel 1 Novel 2

Time on task

µV+ 15

Fig. 2. Topographic maps of the effect of habituation on th

indicated that the amplitude of the P3b did not differ at any region,revealing widespread orientation of both the novelty P3 and P3b inolder adults.

3.6. Habituation to novelty

3.6.1. Preliminary analysis with four repetitions of novel stimuliAs shown in Fig. 2, there was an interaction between location and

group for the novelty P3 amplitude [F(1, 25)=14.50, p=0.001,d=1.52]. These findings indicated that Pz was the location ofmaximal P3 amplitude in younger adults, whereas older adults hadincreased frontal (Fz) orientation, irrespective of time spent on task.

Novel 3 Novel 4

-5

e novelty P3 amplitude for younger and older adults.

101C. Richardson et al. / International Journal of Psychophysiology 79 (2011) 97–105

Of particular interest was a significant interaction between group andtime [F(3, 75)=3.15, p=.030, d=0.71]. A closer inspection of thewithin group differences at Fz found significant differences inamplitude between the first and third presentation of a novelstimulus in each group (p=.050, d=0.61; p=.028, d=0.54,younger and older adults, respectively), in that there was a significantincrease in older adults and a decrease in younger adults (see Fig. 3).However, after adjusting for multiple comparisons (pb .017) thesedifferences were no longer significant.

3.6.2. Analysis of habituation to novel stimuliAmain effect of location [F(1, 25)=11.13, p=0.003, d=1.34] was

found and indicated that Pz was the location of maximal novelty P3amplitude (see Fig. 4). Similarly to the preliminary analyses, there wasan interaction between location and group [F(1, 25)=11.68,p=0.002, d=1.37]. Post hoc analyses revealed that there was asignificant increase in novelty P3 amplitude in the older adults at Fzfor the third and fourth repetitions combined compared to theyounger adults (p=.023; see Fig. 4). In further support of thepreliminary results, an interaction between time and group was alsofound [F(1, 25)=5.11, p=.033, d=0.90], indicating a decrease innovelty P3 amplitude with time in the younger adults, but an increasein the older adults (see Fig. 4). The post hoc examination of thisinteraction found a significant decrease in novelty P3 amplitudebetween time 1/2 to 3/4 in the younger adults at Fz (p=.012,d=0.63), with no significant difference in the amplitude at Pz(p=.803, d=0.08). The converse was found in the older adults, inthat the novelty P3 amplitudes at time 3/4 were greater than thosefound at time 1/2. In contrast to the preliminary results, the differenceat Fz was no longer significant (p=.053), however, the effect size waslarge (d=0.84), and indicated a substantial increase in novelty P3amplitude between times 1/2 and 3/4. A similar result was found inthe older adults with novelty P3 amplitudes between time 1/2 and 3/4at Pz (p=.018, d=1.06; see Fig. 4).

Amain effect of groupwas found for novelty P3 latency [F(1, 25)=13.54, p=0.001, d=1.47] and indicated that the novelty P3 occurredfaster in the younger adults compared to the older adults. Aninteraction between time and age group [F(1, 25)=6.67, p=0.016,d=1.03] was also found, and indicated that older adults hadsignificantly slower novelty P3 components at Fz at both times 1/2

Fig. 3. Grand average waveforms for each repetition of novel stimuli at

and 3/4 (p=0.005; p=.030; times 1/2 and 3/4, respectively) and atPz at time 1/2 (p=0.001).

3.6.3. Topographic analysis of novel stimuli habituationAs shown in Fig. 4, a main effect of caudality [F(4, 48)=31.51,

pb0.001, d=2.25] was found in the younger adult normalized data.Post hoc examination replicated the previous findings of a posteriormaximum for the novelty P3. Similar to previous topographicanalyses, there were no effects in the older adults and indicated thatthe novelty P3 had a widespread distribution in this group. The lack oftime effects indicated that the topography of the novelty P3 did notchange with time in either group.

3.6.4. Relationship between novelty P3 and fluid intellectual functionIn order to explore a possible association between the strength of

novelty processing and novelty habituation with neuropsychologicaltest performance in older adults (see: Daffner et al., 2006; Fjell andWalhovd, 2001, 2003), we conducted a series of exploratory two-tailed correlations. These correlations revealed two main findings.Firstly, the amplitude of the novelty P3, irrespective of time spent ontask, at Fz, Cz and Pzwas not significantly correlatedwith Raven's SPMraw scores (all p N 0.10), in either younger or older age groups, orwhen age groups were combined. Secondly, we explored a possibleassociation with the degree of habituation to novel stimuli, typicallyinterpreted as the extent of decrease in novelty P3 amplitude over thefrontal lobes with increasing time spent on task; the reductionsuggestive of greater efficacy of cognitive processing. If such arelationship exists, greater decline in novelty P3 amplitude may becorrelated with higher scores on the Raven's SPM in the youngergroup. Conversely, there may be no correlation in older adults whoshowed an increase in frontal novelty P3 amplitude with increasingexposure. In order to investigate this hypothesis, we subtracted thenovelty P3 amplitude at Fz for Novel 1 from Novel 3, as the greatestamplitude difference was between the first and third presentation of anovel stimulus. A negative difference score indicated a reduction inamplitude between Novel 1 and Novel 3, whilst a positive differencescore showed an increase. However, there was no significantrelationship between Raven's SPM score and the amplitude differencescore in either younger or older adults (r (11)=−0.33, p=.317;r (12)=0.31, p=0.333, two-tailed, younger and older adults,respectively).

frontal (Fz) and parietal (Pz) regions for younger and older adults.

Fig. 4. Grand average waveforms for the first two and last two repetions of novel stimuli for younger and older adults.

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4. Discussion

This study explored novelty processing and habituation in normalaging. In support of previous studies (e.g. Fabiani and Friedman, 1995;Friedman et al., 1993; Friedman and Simpson, 1994), the novelty P3component was of significantly greater amplitude compared to targetstimuli in both older and younger adult groups. As target stimuliwere ofsimilar low frequency to novel stimuli, we may conclude that both agegroups distinguished stimulus novelty controlling, simultaneously, forlow frequency of stimulus presentation. Furthermore, rate and speed oftarget detection was comparable between age groups, indicating thatthe waveforms are unlikely to be influenced by performance of the ERPtask. We nevertheless found significant differences between the agegroups in the processing of repeated novel stimuli although, contrary toprevious studies (e.g. Fabiani and Friedman, 1995; Friedmanet al., 1993;Friedman and Simpson, 1994), consistent amplitude reductions anddelayed latencies were not found. Our findings are compatible with thehypothesis (Cabeza, 2002; Daffner et al., 2006; Riis et al., 2008) thatnormal agingmay result in alteration to neural networks underpinningthe processing of novel information, but such change may be subtle,potentially adaptive and not apparently explained by a generalisedreduction of amplitude per se.

We explored the novelty P3 component in general and accordingto time spent on task. The general results are considered first. In anovelty oddball task, the amplitude of the P3 component is typicallygreatest for novel stimuli (e.g. Fabiani and Friedman, 1995; Friedmanet al., 1993; Friedman and Simpson, 1994), and this was the case forboth younger and older adult groups in the present study. Anotherconsistent finding in the literature is that the P3b is both attenuatedand delayed in older adults (e.g. Czigler et al., 2006; Fabiani andFriedman, 1995; Friedman et al., 1993; Friedman and Simpson, 1994;Polich, 1996, 1997; Weisz and Czigler, 2006). Although the currentstudy did not find the expected age reduction in P3b amplitude, posthoc analyses found that P3b amplitude at Pz was attenuated in olderadults supporting earlier studies. Results diverge, however, when it is

noted that P3b amplitude was, by contrast, significantly greater atfrontal regions in older compared to younger adults. This is a findingshared with Fabiani, Friedman and Cheng (1998) who found thatolder adults with a frontal maximal P3 performed worse on a numberof subtests from theWisconsin Card Sorting Test than the older adultswith a parietal maximal P3. However, contrasting results werereported by Fjell, Walhovd and Reinvang (2005). They found thatthe cognitive and executive functioning of older adults with a fronto-central maximal P3a and P3b was not significantly different to theolder adults with parietal P3a and P3b maxima. The greater parietalorientation of activity to target stimuli in younger adults has beeninterpreted to indicate the delegation of attentional work toassociation cortices, whilst the frontal orientation found in the olderadults may be indicative of impaired ability to construct and maintainmental representations of stimuli (Fabiani and Friedman, 1995).Essentially, even target stimuli may have been treated as “novel” bythe older adults. A reduction in ability to sustain attention might alsoexplain the increase in false alarms to standard stimuli in older adults(e.g. Giambra, 1997). In this view, changes in brain morphology withaging require older adults to allocate increased attention in order toperform the task similarly to younger adults, but that such up-regulation of attentional networks also incurs a possible cost ofincreased likelihood of false alarms. This interpretation is consistentwith our finding of increased P3b amplitude over the frontal lobes inolder compared to younger adults. Due to the simple requirements ofour task, it should not be assumed, however, that altered attentionalprocessing in older adults negatively impacts on more generalperformance. Indeed, Raven's Matrices scores did not differ signifi-cantly between the two age groups. A more difficult oddball paradigmwith increased attentional load, for example, by including a fourthcategory of stimuli (e.g. stimuli with a similar tone to targets), maymake the discrimination of targets harder, facilitating the explorationof possible effects of age-related attentional impairments on targetdetection, but this would also make greater demands on workingmemory and thus be less focussed on attentional processing per se.

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The current study did not find any main effects of age group on thenovelty P3 amplitude, contrary to early studies (Czigler et al., 2006;Fabiani and Friedman, 1995; Friedman et al., 1993, 1998; Friedmanand Simpson, 1994), but in support of a more recent study whichdescribed comparable novelty P3 amplitudes in younger adults andaverage performing older adults (Riis et al., 2008). This resultindicates that immediate attention to auditory novel stimuli, asindexed by the novelty P3 (Friedman et al., 2001), was notsignificantly different between younger and older adults. Thedifference between our data and those published by Friedman andcolleagues (Fabiani and Friedman, 1995; Friedman et al., 1993, 1998;Friedman and Simpson, 1994), are not easily explained, as the age andIQ level of our older adult sample is similar to that of Friedman's. TheIQ level of our younger adults is lower than the levels reported inother studies, although other studies using the National Adult ReadingTest (NART) have also found significantly reduced NART predicted IQin younger compared to older adults (e.g. Bunce andMacready, 2005).Perhaps lower IQ in the younger adults may offer some explanationfor these discrepant results, as better cognitive abilities have beenassociated with greater P3a and P3b amplitudes and shorter latenciesacross the lifespan (see Fjell and Walhovd, 2001, 2003), but this isunlikely to have made a major contribution to our results. If true, ourlower-performing younger adults may have had reduced ERPamplitudes in general and this may have masked any significantreduction in older adults. However, we failed to find a significantrelationship between a measure of fluid intelligence (RSPM) andnovelty P3 amplitude at mid-line locations in either younger or olderadults.

Of particular interest to our understanding of learning potential inolder adults is the analysis of rate, degree and topographical pattern ofhabituation to novel stimuli. Increasing familiarity with a stimulustypically results in a reduction of novelty P3 amplitude over thefrontal lobes (e.g. Courchesne et al., 1975), and consistent with earlierfindings (Cycowicz and Friedman, 1997; Cycowicz et al., 1996;Friedman et al., 1998; Friedman and Simpson, 1994; Weisz andCzigler, 2006), this pattern of activity was found only in the youngeradult group. Novelty P3 amplitude at parietal regions did not differwith time in younger adults, similarly to Cycowicz and Friedman(1997). Although we did not find a statistically significant linearreduction in novelty P3 amplitude at frontal regions with repetition inthe younger adults in the raw amplitude analyses, we did find anamplitude reduction between the first and third presentation in thepreliminary results. Others have found a P3 amplitude reductionbetween the first and second presentation of a novel stimulus(Cycowicz and Friedman, 1997; Cycowicz and Friedman, 1998;Cycowicz et al., 1996), which suggests that habituation occurredwith minimally increased experience of stimuli in our younger adults.The current study employed fewer unique novel stimuli with morerepetition, and whilst this is a difference with previous noveltyoddball studies, the number of trials in the waveforms werecomparable with other studies (e.g. Friedman et al., 1998; Friedmanand Simpson, 1994), and our stimuli were of similar duration to Esceraet al. (2001). Interestingly, Cycowicz and Friedman (1998) found thatthe novelty P3 did not change at fronto-central regions with a secondrepetition of novel stimuli that were confirmed to be unfamiliar to theparticipant. Our novel stimuli includedmechanical sounds, but we didnot include an assessment of familiarity of these stimuli.

The present study also found that novelty processing was delayedin older adults, and this is in line with previous studies (Fabiani andFriedman, 1995; Friedman et al., 1993). The delay is unlikely to be dueto prolonged early processing of the stimulus in the older adults, asthe N2b component was of similar timing across the groups. It may beinferred that both groups heard the stimuli. Rather, there may beimpaired disengagement of attention to novel stimuli (Weisz andCzigler, 2006) reflected in the later novelty P3 component. The findingof delayed novelty processing in aging is of importance, as novel

stimuli can represent potential danger requiring an immediateresponse. One implication of this finding is that older adults areslower to process and respond to these novel types of stimuli, forexample, a delay in processing a warning car horn may result in anaccident (Friedman et al., 2001).

Interestingly, older adults actually demonstrated increased novel-ty P3 amplitude at Fz with increasing time spent on task, withamplitude values for the novelty P3 significantly exceeding thoseobtained from younger adults from half-way through the task. Inother words, whilst the younger group appeared to down-regulatetheir frontal lobes with habituation to novel stimuli, the older adultsappeared to do the opposite, and up-regulate their frontal lobes.Normal aging is associated with morphological changes in the braindescribed by some as a loss of brain volume, affecting white and greymatter (Raz, 2000). The fact that these present data suggest increasedamplitude in older adults might, at first hand, appear paradoxical.However, the pattern of brain activation is likely to reflect greaterrecruitment of existing neural networks despite gross reduction inbrain size, an interpretation consistent with that of earlier authors(e.g. Daffner et al., 2006), and further supported by the widespreaddistribution of the novelty P3 in the topographic analyses. This view isalso consistent with the hypothesis outlined above, that older adultsallocate greater attention to processing stimuli in the novelty auditoryoddball task than younger adults.

The increase in frontal activity to novel stimuli in older adults isunlikely to be explained by an increase in their startle response, asthere were equivalent, low rates of false alarm responding to novelstimuli across groups. As a novel stimulus may also represent a threat,the perception and processing of which may be influenced by otherfactors, such as anxiety, but, anxiety is unlikely to have influenced ourresults as therewere similar HADS anxiety scores between the groups.While this suggests that the current findings are unlikely to be due toan exaggerated startle response in older adults, it would be ofconsiderable interest to investigate this possibilitymore directly usingother autonomic nervous system measures of startle such as eye-blink. Ford et al. (1997) measured eye blinks and found older adultswere less responsive than younger adults, however, they did not useunexpected novel stimuli. Only two previous studies (Friedman et al.,1993; Weisz and Czigler, 2006) have found that older adults givesignificantly more false alarms to novel stimuli, interpreted as moreimpulsive responding and/or less inhibition. The finding of increasedfalse alarms to standard stimuli in older adults, shared with Friedmanet al. (1993), does not necessarily indicate a deficit in the inhibition ofattention to frequent irrelevant stimuli, as the false alarm rate wasvery small (1.5%), rather we believe that it results from a generalenhancement of neural networks underlying attentional processes inolder adults. In other words, the threshold for response may be lowerin older adults and thus less discriminating. Others have suggestedthat aging is associated with the recruitment of compensatory neuralnetworks (Cabeza, 2002; Daffner et al., 2006; Riis et al., 2008), and ourresults may be consistent with this hypothesis also.

Although studies have indicated that the prefrontal cortexcontributes to the novelty P3 signal (Baudena et al., 1995; Halgrenet al., 1995; Kiehl et al., 2001; Yamaguchi et al., 2004), the activity atthe surface of the scalp does not necessarily correspond with specificunderlying neural generators due to the volume conducting proper-ties of the brain and signal propagation by dipoles. Thus, the increasein frontal activity in older adults does not confirm increasedgenerating power of the original signal or a change in the recruitmentof neural regions per se. A further caveat is the use of linked-mastoidreference leads which have the potential to distort topographic mapsas there may be asymmetrical impedances between the mastoid areas(Nunez, 1991). Whilst neuroimaging studies have shown greaterrecruitment of the prefrontal cortex in high performing older adults(e.g. Cabeza et al., 2002), discrepant results are found in electrophys-iological studies. For example, both younger and older adults with

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poor memory performance had a frontally distributed old/new effect(Walhovd et al., 2006), and the topography of ERP components wassimilar between younger and high-performing older adults (e.g.Duarte et al., 2006). In summary, the implications of the findings inthe current study are that the aging brain is able to distinguish andprocess novel stimuli, but subtle differences, particularly in latencyand topography, suggest that more widespread neural networks arerequired to facilitate this processing (see Cabeza, 2002; Daffner et al.,2006; Riis et al., 2008).

A lack of habituation to novelty in older adults has already beendemonstrated (Friedman et al., 1998; Friedman and Simpson, 1994;Weisz and Czigler, 2006). Supporting and extending these data, thepresent study shows differentiation of activity associated with thenovelty P3 at frontal and parietal regions in the younger adults,compatible with the proposition that the novelty P3 is composed oftwo aspects: a frontal aspect representing initial orienting to novelty,and a parietal aspect reflecting familiarisation or learning (e.g.Courchesne et al., 1975). However, there is limited understandingabout the behavioural relevance of such ERP data. It is not clear,therefore, whether such changes in ERP morphology, power andlatency with normal aging make cognitive deficit inevitable or ifcognitive function is maintained despite these changes and/oradapted.

In order to explore this issue, we administered the RSPM as a testof “[...] the ability to reason and solve problems involving newinformation, without relying extensively on an explicit base ofdeclarative knowledge derived from schooling or previous experi-ence” (Carpenter et al., 1990, p. 404). Thus, similar to the ERP noveltyparadigm, it is also a measure of the ability to attend to and processnovel information but with a view to decision making. Moreover, Fjelland Walhovd (2003) found that better Matrices subtest scores wereassociatedwith increased P3 amplitudes elicited by target and deviantand tones at central and parietal regions. We hypothesised that ifnovelty habituation reflects the efficiency of novelty processing, thenthe extent of decrease in frontal novelty P3 amplitude withhabituation might be related to performance on Raven's SPM, butthis was not the case in younger adults, nor was there any associationin the older adults, in whom there was the opposite pattern of anincrease in frontal novelty P3 amplitudewith increasing time spent ontask. This highlights that the relationship between neuropsychological(the RSPM test) and ERP measures in normal aging is complex, butthat such investigation may be key to understanding the relevance ofERP data. Two important discussion points arise from our data. Firstly,the use of more sensitive neuropsychological measures is an obviousstarting point in any progression of this line of research. For example,the novelty P3 reflects relatively early sensory processing of novelinformation (within half a second of hearing the stimulus), whereasthe Raven's SPM was not timed, and success on this task is likely to bedetermined by the interaction of more complex networks. Secondly,as both our novelty ERP and RSPM tasks share a requirement fornovelty processing, and thus are theoretically similar, it must beconsidered that lack of significant findings is due to insufficientstatistical power. Of note, whilst the hypothesised correlations werenot significant, they were of moderate strength [r (11)=−0.33;r (12)=0.31; younger and older adults, respectively; negative differ-ence scores indicated a reduction in amplitude with time, whereas apositive score indicated an increase], showing that 10% of the sharedvariance between the change in novelty P3 amplitude with habitu-ation was related to better fluid intelligence. If confirmed,1 this wouldindicate support for the view that increased novelty P3 amplitudein older adults is not necessarily indicative of impairment (e.g.Daffner et al., 2006). In other words, this would suggest a positive

1 Based on our results, we estimate that a minimum of 67 participants are requiredto find relationships with an alpha level of .05, power .80 (G*Power 3 program: Faul etal., 2007).

interpretation of normal aging underpinned by subtle and normalchanges (adaptation) in brain function, rather than one of deficitwhich may be the most logical inference from the results of someearlier studies (e.g. Fabiani et al., 1998; Fabiani and Friedman, 1995).

In summary, we found that older adults had similar noveltyprocessing to younger adults, albeit delayed. The contrasting increasein frontal novelty P3 amplitude and orientation in our older adults isconsistent with the view that each novel stimulus is treated more asnew than as familiar (cf. Amenedo and Diaz, 1998). Thus, this mayreduce older adults' capacity for habituation and learning to whichCourchesne et al. (1975) originally referred.

Lack of novelty P3 habituation over the frontal lobes in older adultsis compatible with the proposition that older adults are less able toconstruct “novel category templates” (Friedman and Simpson, 1994,p. 62). Particularly pertinent, however, it may not be assumed on thebasis of our ERP findings, that such habituation reflects behaviour ineveryday life, and few studies have attempted to validate such claimsby looking for associations between ERP components and neuropsy-chological measures.

Acknowledgments

This study was funded by the Economic Social Research Council,The Gerald Kerkut Trust and the Alzheimer's Research Trust.We thankDr. Torsten Baldeweg (Institute of Child Health, University CollegeLondon, UK) for his permission to use his novelty auditory oddballparadigm and for his helpful comments. Our gratitude extends toMiguel A. Rodriguez, Compumedics, UK, and Luke Phillips, ComputerSciences Corporation, UK, for software program design and technicalsupport.

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