Effects of aging on habituation to novelty: An ERP study

International Journal of Psychophysiology 79 (2011) 97–105

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International Journal of Psychophysiology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j p s yc h o

Effects of aging on habituation to novelty: An ERP study Cassandra Richardson a,b,⁎, Romola S. Bucks a,b, Alexandra M. Hogan c a b c

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

a r t i c l e

i n f o

Article history: Received 7 June 2010 Received in revised form 16 September 2010 Accepted 17 September 2010 Available online 24 September 2010 Keywords: Aging Novelty Habituation ERPs P3 Attention

a b s t r a c t Age-related effects on novelty processing have been reported and are linked with changes in frontal lobe functioning. Auditory novelty processing and habituation of the novelty P3 event-related potential were investigated in younger and older adults. Novelty processing, as indexed by novelty P3 amplitude, was similar between the groups. We found the expected decrease in novelty P3 amplitude at frontal regions in younger adults with repetition of novel stimuli. In contrast, older adults displayed no evidence of habituation, rather an increase in novelty P3 amplitude at frontal sites was found when novel stimuli were repeated. We extend current understanding of novelty processing in normal aging by comparing this habituation relatedhyperfrontality 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 of environmental noise. In particular, novel or unexpected stimuli require further processing due to the potential for such stimuli to signal danger (Friedman et al., 2001). The efficient processing of novel stimuli is, thus, important for learning (Ranganath and Rainer, 2003), and consistent with this, has been shown to enhance memory retrieval (Kishiyama et al., 2009). Repetition of novel stimuli is associated with rapid habituation, the process by which novel stimuli become familiar or learnt (Courchesne et al., 1975; Yamaguchi et al., 2004). Novelty processing and habituation involves widely distributed neural circuits including the prefrontal cortex and the medial temporal lobe (e.g. Daffner et al., 2000; Knight, 1984; Strange and Dolan, 2001; Yamaguchi et al., 2004), and is constrained by brain damage involving these areas (Daffner et al., 2000; Kishiyama et al., 2009; Knight, 1984). More subtle change in brain morphology occurs with 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 with increasing age, irrespective of brain damage. A variable effect of normal aging on novelty processing has been reported, with some studies suggesting less efficient novelty processing (e.g. Friedman ⁎ Corresponding author. Neurocognitive Development Unit, School of Psychology, University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia. Tel.: + 61 8 6488 4652; fax: + 61 8 6488 1006. E-mail address: [email protected] (C. Richardson).

et al., 1993, 1998; Friedman and Simpson, 1994) whilst others demonstrate stability or even improvement (e.g. Daffner et al., 2006; Riis et al., 2008). Nonetheless, there is consensus that such change reflects age-related modification to frontal lobe function (Daffner et al., 2006; Friedman et al., 1998; Friedman and Simpson, 1994; Friedman et al., 1993; Riis et al., 2008). However, there is little empirical support for a direct relationship between novelty processing and frontal lobe functioning. Electrophysiological investigations of novelty processing and habituation employ novelty oddball tasks in which unexpected novel stimuli are randomly interspersed with frequent irrelevant stimuli and infrequent target stimuli. The P3b is elicited by target stimuli, and is associated with the updating of mental representations of stimuli (Donchin and Coles, 1988). More specifically, the amplitude of the P3b is considered to index the allocation of attention to information processing, whilst the latency provides a measure of the timing of this processing (Polich, 1996). Infrequent irrelevant stimuli in three-stimuli and novelty oddball tasks elicit the P3a and novelty P3, respectively (Comerchero and Polich, 1999; Spencer et al., 1999). The P3a and novelty P3 occur at ~250 ms and have more anterior scalp distributions compared to the P3b. However, there are few differences between these components (see Simons et al., 2001), and in a recent review, it was concluded that the P3a and novelty P3 were “variants of the same ERP that var[y]...as a function of attentional and task demands” (Polich, 2007, p. 2134). In the current study, we use the term novelty P3 to refer to the P3 elicited by novel stimuli; this nomenclature is in line with other studies employing a novelty oddball paradigm (Courchesne et al., 1975; Cycowicz and Friedman, 1997; Daffner et al., 2006; Fabiani and Friedman, 1995; Friedman

0167-8760/$ – see front matter. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2010.09.007

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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 novelty P3a component occurring at ~320 ms that was associated with orienting to novel stimuli. Convergent evidence from fMRI and intracranial ERP studies has indicated that widely distributed networks involving the bilateral superior and middle frontal gyrus, temporal-parietal junction, hippocampus, cingulate gyrus and fusiform 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), and novelty P3 latency increased (Czigler et al., 2006; Fabiani and Friedman, 1995; Friedman et al., 1993; Weisz and Czigler, 2006) in older compared to younger age groups. In both younger and older adults, the novelty P3 has an increased anterior distribution compared to the parietally distributed P3 elicited by target stimuli. However, the topography differs between the age groups. In younger adults, novelty P3 amplitude increases from frontal to parietal regions, in contrast, novelty P3 amplitude is similar across midline locations in older adults (Fabiani and Friedman, 1995; Friedman et al., 1993, 1998; Friedman and Simpson, 1994). In other words, these studies indicate that novelty processing is attenuated and delayed with increasing age, but that the same underlying neural networks are likely to be involved. The N2b has also been investigated to address the potential concern that the delay in the P3 found in older adults is due to delayed earlier processing (e.g. Czigler et al., 2006; Riis et al., 2008; Weisz and Czigler, 2006). More recent studies have found that novelty P3 amplitude was actually increased in high-functioning older adults compared to average-functioning older adults: a finding that was explained by compensatory recruitment of other neural networks involving the frontal lobes (Daffner et al., 2006; Riis et al., 2008). Indeed, P3 amplitudes have been linked with performance on the Matrices subtest of the Wechsler Abbreviated Scale of Intelligence (WASI) in older adults (e.g. Fjell and Walhovd, 2001, 2003). It should be acknowledged, however, that a direct comparison between the different aging and novelty processing studies is limited by methodological differences. For example, Daffner and colleagues used a modified visual oddball paradigm, whilst others have administered auditory 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 the novelty P3 according to the first presentation of the stimulus and then each repetition of the same novel stimulus. By this means, habituation has been consistently found in younger adults (e.g. Cycowicz and Friedman, 1997; Cycowicz et al., 1996), evidenced by reduction in novelty P3 amplitude at fronto-central locations with increasing time spent on task, and suggests a process of rapid familiarisation (learning) of novel stimuli. Interestingly, this pattern of activity has not been found in older adults (Friedman et al., 1993, 1998; Friedman and Simpson, 1994; Weisz and Czigler, 2006). The lack of habituation of the novelty P3 in older adults has been interpreted as an inability to construct 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 our knowledge, ERP studies conducted with older adults have not, thus far, considered the possibility that lack of novelty P3 attenuation with 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 cognitive function. Such information is important for interpreting the relevance of novelty habituation for everyday cognitive function. The current study thus aimed to examine relationships between the novelty P3 elicited by repeated novel stimuli and a neuropsycho-

logical measure of intellectual function that involves solving problems based on novel information, the RSPM (Raven et al., 2000). The secondary aim of the study was to provide convergent evidence for the effects of repetition of novel stimuli on the novelty P3 in a group of older and younger adults. Evidence that age-related change in habituation of novelty ERP activity is associated with level of behavioural performance would extend the current habituation literature by indicating its relevance for everyday functioning. 2. Method Approval for the study was given by the Human Research Ethics Committee 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 in Table 1. The older adults (OA) were recruited from a research volunteer database (Exploring the Mind, directed by RSB, School of Psychology, University of Southampton, UK). The younger adult (YA) participants were recruited opportunistically from the University of Southampton, and received course credits in return for their participation. 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 on medication, had been taking stable dosages for the preceding 3 months. All participants underwent a hearing assessment prior to testing. Where there was mild-to-moderate hearing loss in one or both ears (25–45 dB, and 45+ dB, respectively), the sound pressure level was adjusted to compensate. 2.2. Measures 2.2.1. Novelty auditory oddball paradigm Auditory stimuli were presented via headphones. Sound pressure levels of stimuli (65 dB: level 1 ≤ 25 dB loss; 75 dB: level 2 = 25–40 dB loss; 85 dB: level 3 ≥ 40 dB loss) were set for each participant depending 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 ms rise and fall time) were pure sinusoidal tones: standard tone (1 kHz, 0.8 probability) and target tone (1.5 kHz, 0.1 probability), and computer-generated novel sounds (e.g. dog bark, drum beat, car horn, 0.1 probability), with stimulus-onset-asynchrony of 900 ms. A total of 48 novel stimuli were presented in the paradigm. Fourteen unique novel stimuli were presented at different intervals throughout Table 1 Demographic information and behavioural data.

Age MMSE MoCA NART predicted IQ Years of education Raven Matrices HADS Anxiety HADS Depression Target hits (%) Target RT (ms) Novel false alarms (%) Standard false alarms (%)

Younger (n = 13)

Older (n = 14)

d

20.3 29.0 28.3 102.8 15.1 39.8 7.0 4.0 96.3 427.3 4.3 0.3

69.1 29.0 28.1 120.7 13.0 39.7 7.6 6.4 92.7 451.1 6.0 1.5

9.12 0.00 0.16 3.34 0.97 0.03 0.24 1.39 0.47 0.50 0.31 1.00

(3.6) (0.9) (1.4) (6.4) (2.4) (3.1) (2.4) (1.2) (5.1) (40.9) (6.1) (0.3)

(7.1) (0.8) (1.2) (4.5) * (2.1) * (3.2) (2.7) (2.2) * (9.8) (56.9) (5.2) (1.7) *

Note. Mean (SD); * p b 0.05 younger vs. older adults; MMSE = Mini Mental State Examination, Folstein et al. (1975); MoCA = Montreal Cognitive Assessment, Nasreddine et al. (2005); National Adult Reading Test, 2nd edition, Nelson and Willison (1991); Raven Matrices (raw scores = 0–48; Sets A–D) = Raven's standard progressive matrices, Raven et al. (2000); HADS (0–21; clinically significant threshold ≥ 11) = Hospital Anxiety and Depression Scale, Zigmond and Snaith (1983).

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the task, and each was randomly repeated up to four times during the paradigm, facilitating an exploration of habituation to novel stimuli. Participants were requested to press a mouse button upon hearing the target tone, but were not informed about the novel stimuli. A practice trial of eight standard tones randomly interspersed with four target tones was administered to ensure that participants could discriminate between the tones and understood the instructions. All participants were able to perform the practice trial successfully on the first attempt. 2.3. ERP acquisition and processing The EEG was recorded using NeuroScan SynAmps™ amplifiers at a sampling rate of 500 Hz (band-pass 0.05–70 Hz) with an Easy-Cap™ fitted with 24 electrodes positioned according to the International 1020 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 less than 10 KΩ. Vertical (right eye) and lateral ocular electrodes enabled offline blink reduction according to a standard algorithm (Semlitsch et al., 1986). EEG data were divided into epochs of −200 to 1000 ms centred on presentation of stimuli, baseline corrected at −200 to 0 ms, and automatically artefact-rejected at ±100 μV. Epochs associated with novel stimuli were averaged in two ways: firstly, across all novel stimuli, irrespective of repetition, and secondly, by repetition of the presentation of the novel stimuli (e.g. first time a particular novel sound is heard = Novel 1, second time the same novel sound is heard = Novel 2, Novel 3 and Novel 4) in order to explore novelty habituation. This factor was labelled time. The mean number of trials across groups were 13.30 (1.2 SD), 11.44 (1.0 SD), 8.56 (1.1 SD), and 7.41 (0.9 SD) for the first to fourth presentations, respectively. Importantly, the numbers of trials in each repetition waveform did not 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 3 and 4, a discernable P3 was found in these waveforms (see Fig. 3). Moreover, these numbers of trials are comparable to Friedman and Simpson (1994). However, to address the possibility that these waveforms had a poor signal-to-noise ratio, a second habituation analysis was undertaken in which the first two and last two repetitions were averaged together (Novel 1/2 and Novel 3/4). The mean numbers of trials were 24.74 (1.8 SD) and 15.93 (1.6 SD), respectively, and again 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 X time, respectively]. The N2b is maximal at Fz, therefore, only this site was considered in the analyses. The N2b and P3 were identified as the maximum peak within a specific time frame: N2b (70–250 ms) at Fz and 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 interactions with electrode sites cannot differentiate between amplitude changes and topographic changes, thus McCarthy and Wood (1985) advocated using normalized data to investigate topography. The root mean square method eliminates amplitude differences between conditions and groups and topographic analyses were conducted with these normalized data. 2.4. Data analysis The distributions of the data were assessed using the Shapiro Wilk test of normality. Behavioural responses made b 150 ms after stimulus presentation were excluded from the analysis. Behavioural data were investigated with Independent Samples t-tests. ERP data were examined using mixed-design ANOVA models: The amplitude and latency of the P3 stimulus (x2: target, novel), and location (x3: Fz, Cz, Pz) as within-subjects factors and group (x2: younger and older

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adults). Main effects of stimulus type and interactions with location were analysed separately using the normalized data with hemisphere (x2: left, right) and caudality (x5: F3/4, F7/8, C3/4, T7/8, P3/4) as within-subjects factors for each group separately, for the novelty P3 and 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-subjects factors and Age-group. Due to the small number of trials in the waveforms of Novel 3 and Novel 4, the analysis of habituation included time (x2: Novel 1 + 2 combined, and Novel 3 + 4 combined) and location (x2: Fz, Pz) and Age-group. A topographic analysis used normalized data and included time (x2: Novel 1 + 2 combined, and Novel 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-line analyses were also conducted and the results were similar to the caudality analyses, thus they will not be further described. Where appropriate, the Greenhouse-Geisser corrected value is reported. The Bonferroni correction was used to adjust for multiple comparisons. 3. Results 3.1. Behavioural responses Behavioural data are presented in Table 1. Target detection and reaction times to targets were equivalent across groups. The false alarm rate to novel stimuli was also similar between younger and older adults. In contrast, older adults responded erroneously to standard 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 amplitude of the N2b elicited by target and novel stimuli was significantly greater in younger compared to older adults. There were no latency differences 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, p b 0.001, d = 1.67] and location [F(2, 50) = 15.92, p b 0.001, d = 1.60] on P3 amplitude (see Fig. 1). These results indicated that novel stimuli elicited significantly greater amplitude compared to target stimuli. The main effect of location was explained by the fact that P3 amplitude at both Cz and Pz was significantly greater than that recorded at Fz (all p b 0.001). A location by group interaction [F(2, 50) = 16.43, p b 0.001, d = 1.62] indicated topographic differences between the 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 of the P3 differed between the stimulus types. A series of planned comparisons revealed that older adults had lower P3b amplitudes at Pz, but higher P3b amplitudes at Fz compared to younger adults (see Fig. 1). The lack of age-group effects indicated that the amplitude of the novelty P3 and P3b did not differ significantly between the younger and older adults. There was a main effect of group for P3 latency [F(1, 25) = 7.78, p = .010, d = 1.12], which showed that, regardless of stimulus type, the timing of the P3 was significantly slower 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, p b 0.001, d = 2.12]. A series of post-hoc examinations revealed that the novelty P3 amplitude at the posterior location (P3/4) was significantly greater than at all of the other regions (F7/8,

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

F3/4 and T7/8: all p b .05). There were no significant effects in the older adults, which indicated that novelty P3 amplitude was similar across the scalp. These divergent age-group results indicated that the topography of the novelty P3 was different between younger and older adults.

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

3.5. Topographic analysis of target stimuli

3.6.1. Preliminary analysis with four repetitions of novel stimuli As 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 of maximal P3 amplitude in younger adults, whereas older adults had increased frontal (Fz) orientation, irrespective of time spent on task.

3.6. Habituation to novelty

There were significant main effects of caudality [F(4, 48) = 31.89, p b 0.001, d = 2.26] on the amplitude of the P3b in the younger adults. Post-hoc examination again found that amplitude was maximal at posterior regions (P3/4). The lack of effects in the older adults

Time on task Novel 2

Novel 1

Novel 3

Novel 4

Younger Adults

Older Adults

+ 15

µV

-5

Fig. 2. Topographic maps of the effect of habituation on the novelty P3 amplitude for younger and older adults.

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

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

3.6.2. Analysis of habituation to novel stimuli A main 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 P3 amplitude (see Fig. 4). Similarly to the preliminary analyses, there was an interaction between location and group [F(1, 25) = 11.68, p = 0.002, d = 1.37]. Post hoc analyses revealed that there was a significant increase in novelty P3 amplitude in the older adults at Fz for the third and fourth repetitions combined compared to the younger adults (p = .023; see Fig. 4). In further support of the preliminary results, an interaction between time and group was also found [F(1, 25) = 5.11, p = .033, d = 0.90], indicating a decrease in novelty P3 amplitude with time in the younger adults, but an increase in the older adults (see Fig. 4). The post hoc examination of this interaction found a significant decrease in novelty P3 amplitude between 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, in that the novelty P3 amplitudes at time 3/4 were greater than those found at time 1/2. In contrast to the preliminary results, the difference at Fz was no longer significant (p = .053), however, the effect size was large (d = 0.84), and indicated a substantial increase in novelty P3 amplitude between times 1/2 and 3/4. A similar result was found in the older adults with novelty P3 amplitudes between time 1/2 and 3/4 at Pz (p = .018, d = 1.06; see Fig. 4). A main effect of group was found for novelty P3 latency [F(1, 25) = 13.54, p = 0.001, d = 1.47] and indicated that the novelty P3 occurred faster in the younger adults compared to the older adults. An interaction between time and age group [F(1, 25) = 6.67, p = 0.016, d = 1.03] was also found, and indicated that older adults had significantly slower novelty P3 components at Fz at both times 1/2

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and 3/4 (p = 0.005; p = .030; times 1/2 and 3/4, respectively) and at Pz at time 1/2 (p = 0.001). 3.6.3. Topographic analysis of novel stimuli habituation As shown in Fig. 4, a main effect of caudality [F(4, 48) = 31.51, p b 0.001, d = 2.25] was found in the younger adult normalized data. Post hoc examination replicated the previous findings of a posterior maximum for the novelty P3. Similar to previous topographic analyses, there were no effects in the older adults and indicated that the novelty P3 had a widespread distribution in this group. The lack of time effects indicated that the topography of the novelty P3 did not change with time in either group. 3.6.4. Relationship between novelty P3 and fluid intellectual function In order to explore a possible association between the strength of novelty processing and novelty habituation with neuropsychological test performance in older adults (see: Daffner et al., 2006; Fjell and Walhovd, 2001, 2003), we conducted a series of exploratory twotailed correlations. These correlations revealed two main findings. Firstly, the amplitude of the novelty P3, irrespective of time spent on task, at Fz, Cz and Pz was not significantly correlated with Raven's SPM raw scores (all p N 0.10), in either younger or older age groups, or when age groups were combined. Secondly, we explored a possible association with the degree of habituation to novel stimuli, typically interpreted as the extent of decrease in novelty P3 amplitude over the frontal lobes with increasing time spent on task; the reduction suggestive of greater efficacy of cognitive processing. If such a relationship exists, greater decline in novelty P3 amplitude may be correlated with higher scores on the Raven's SPM in the younger group. Conversely, there may be no correlation in older adults who showed an increase in frontal novelty P3 amplitude with increasing exposure. In order to investigate this hypothesis, we subtracted the novelty P3 amplitude at Fz for Novel 1 from Novel 3, as the greatest amplitude difference was between the first and third presentation of a novel stimulus. A negative difference score indicated a reduction in amplitude between Novel 1 and Novel 3, whilst a positive difference score showed an increase. However, there was no significant relationship between Raven's SPM score and the amplitude difference score 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).

Fig. 3. Grand average waveforms for each repetition of novel stimuli at frontal (Fz) and parietal (Pz) regions for younger and older adults.

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

4. Discussion This study explored novelty processing and habituation in normal aging. In support of previous studies (e.g. Fabiani and Friedman, 1995; Friedman et al., 1993; Friedman and Simpson, 1994), the novelty P3 component was of significantly greater amplitude compared to target stimuli in both older and younger adult groups. As target stimuli were of similar low frequency to novel stimuli, we may conclude that both age groups distinguished stimulus novelty controlling, simultaneously, for low frequency of stimulus presentation. Furthermore, rate and speed of target detection was comparable between age groups, indicating that the waveforms are unlikely to be influenced by performance of the ERP task. We nevertheless found significant differences between the age groups in the processing of repeated novel stimuli although, contrary to previous studies (e.g. Fabiani and Friedman, 1995; Friedman et al., 1993; Friedman and Simpson, 1994), consistent amplitude reductions and delayed latencies were not found. Our findings are compatible with the hypothesis (Cabeza, 2002; Daffner et al., 2006; Riis et al., 2008) that normal aging may result in alteration to neural networks underpinning the processing of novel information, but such change may be subtle, potentially adaptive and not apparently explained by a generalised reduction of amplitude per se. We explored the novelty P3 component in general and according to time spent on task. The general results are considered first. In a novelty oddball task, the amplitude of the P3 component is typically greatest for novel stimuli (e.g. Fabiani and Friedman, 1995; Friedman et al., 1993; Friedman and Simpson, 1994), and this was the case for both younger and older adult groups in the present study. Another consistent finding in the literature is that the P3b is both attenuated and delayed in older adults (e.g. Czigler et al., 2006; Fabiani and Friedman, 1995; Friedman et al., 1993; Friedman and Simpson, 1994; Polich, 1996, 1997; Weisz and Czigler, 2006). Although the current study did not find the expected age reduction in P3b amplitude, post hoc analyses found that P3b amplitude at Pz was attenuated in older adults supporting earlier studies. Results diverge, however, when it is

noted that P3b amplitude was, by contrast, significantly greater at frontal regions in older compared to younger adults. This is a finding shared with Fabiani, Friedman and Cheng (1998) who found that older adults with a frontal maximal P3 performed worse on a number of subtests from the Wisconsin Card Sorting Test than the older adults with a parietal maximal P3. However, contrasting results were reported by Fjell, Walhovd and Reinvang (2005). They found that the cognitive and executive functioning of older adults with a frontocentral maximal P3a and P3b was not significantly different to the older adults with parietal P3a and P3b maxima. The greater parietal orientation of activity to target stimuli in younger adults has been interpreted to indicate the delegation of attentional work to association cortices, whilst the frontal orientation found in the older adults may be indicative of impaired ability to construct and maintain mental representations of stimuli (Fabiani and Friedman, 1995). Essentially, even target stimuli may have been treated as “novel” by the older adults. A reduction in ability to sustain attention might also explain the increase in false alarms to standard stimuli in older adults (e.g. Giambra, 1997). In this view, changes in brain morphology with aging require older adults to allocate increased attention in order to perform the task similarly to younger adults, but that such upregulation of attentional networks also incurs a possible cost of increased likelihood of false alarms. This interpretation is consistent with our finding of increased P3b amplitude over the frontal lobes in older compared to younger adults. Due to the simple requirements of our task, it should not be assumed, however, that altered attentional processing in older adults negatively impacts on more general performance. Indeed, Raven's Matrices scores did not differ significantly between the two age groups. A more difficult oddball paradigm with increased attentional load, for example, by including a fourth category of stimuli (e.g. stimuli with a similar tone to targets), may make the discrimination of targets harder, facilitating the exploration of possible effects of age-related attentional impairments on target detection, but this would also make greater demands on working memory 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 the novelty P3 amplitude, contrary to early studies (Czigler et al., 2006; Fabiani and Friedman, 1995; Friedman et al., 1993, 1998; Friedman and Simpson, 1994), but in support of a more recent study which described comparable novelty P3 amplitudes in younger adults and average performing older adults (Riis et al., 2008). This result indicates that immediate attention to auditory novel stimuli, as indexed by the novelty P3 (Friedman et al., 2001), was not significantly different between younger and older adults. The difference between our data and those published by Friedman and colleagues (Fabiani and Friedman, 1995; Friedman et al., 1993, 1998; Friedman and Simpson, 1994), are not easily explained, as the age and IQ level of our older adult sample is similar to that of Friedman's. The IQ level of our younger adults is lower than the levels reported in other studies, although other studies using the National Adult Reading Test (NART) have also found significantly reduced NART predicted IQ in younger compared to older adults (e.g. Bunce and Macready, 2005). Perhaps lower IQ in the younger adults may offer some explanation for these discrepant results, as better cognitive abilities have been associated with greater P3a and P3b amplitudes and shorter latencies across the lifespan (see Fjell and Walhovd, 2001, 2003), but this is unlikely to have made a major contribution to our results. If true, our lower-performing younger adults may have had reduced ERP amplitudes in general and this may have masked any significant reduction in older adults. However, we failed to find a significant relationship between a measure of fluid intelligence (RSPM) and novelty P3 amplitude at mid-line locations in either younger or older adults. Of particular interest to our understanding of learning potential in older adults is the analysis of rate, degree and topographical pattern of habituation to novel stimuli. Increasing familiarity with a stimulus typically results in a reduction of novelty P3 amplitude over the frontal lobes (e.g. Courchesne et al., 1975), and consistent with earlier findings (Cycowicz and Friedman, 1997; Cycowicz et al., 1996; Friedman et al., 1998; Friedman and Simpson, 1994; Weisz and Czigler, 2006), this pattern of activity was found only in the younger adult group. Novelty P3 amplitude at parietal regions did not differ with time in younger adults, similarly to Cycowicz and Friedman (1997). Although we did not find a statistically significant linear reduction in novelty P3 amplitude at frontal regions with repetition in the younger adults in the raw amplitude analyses, we did find an amplitude reduction between the first and third presentation in the preliminary results. Others have found a P3 amplitude reduction between 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 occurred with minimally increased experience of stimuli in our younger adults. The current study employed fewer unique novel stimuli with more repetition, and whilst this is a difference with previous novelty oddball studies, the number of trials in the waveforms were comparable with other studies (e.g. Friedman et al., 1998; Friedman and Simpson, 1994), and our stimuli were of similar duration to Escera et al. (2001). Interestingly, Cycowicz and Friedman (1998) found that the novelty P3 did not change at fronto-central regions with a second repetition of novel stimuli that were confirmed to be unfamiliar to the participant. Our novel stimuli included mechanical sounds, but we did not include an assessment of familiarity of these stimuli. The present study also found that novelty processing was delayed in older adults, and this is in line with previous studies (Fabiani and Friedman, 1995; Friedman et al., 1993). The delay is unlikely to be due to prolonged early processing of the stimulus in the older adults, as the N2b component was of similar timing across the groups. It may be inferred that both groups heard the stimuli. Rather, there may be impaired disengagement of attention to novel stimuli (Weisz and Czigler, 2006) reflected in the later novelty P3 component. The finding of delayed novelty processing in aging is of importance, as novel

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stimuli can represent potential danger requiring an immediate response. One implication of this finding is that older adults are slower to process and respond to these novel types of stimuli, for example, a delay in processing a warning car horn may result in an accident (Friedman et al., 2001). Interestingly, older adults actually demonstrated increased novelty P3 amplitude at Fz with increasing time spent on task, with amplitude values for the novelty P3 significantly exceeding those obtained from younger adults from half-way through the task. In other words, whilst the younger group appeared to down-regulate their frontal lobes with habituation to novel stimuli, the older adults appeared to do the opposite, and up-regulate their frontal lobes. Normal aging is associated with morphological changes in the brain described by some as a loss of brain volume, affecting white and grey matter (Raz, 2000). The fact that these present data suggest increased amplitude in older adults might, at first hand, appear paradoxical. However, the pattern of brain activation is likely to reflect greater recruitment of existing neural networks despite gross reduction in brain size, an interpretation consistent with that of earlier authors (e.g. Daffner et al., 2006), and further supported by the widespread distribution of the novelty P3 in the topographic analyses. This view is also consistent with the hypothesis outlined above, that older adults allocate greater attention to processing stimuli in the novelty auditory oddball task than younger adults. The increase in frontal activity to novel stimuli in older adults is unlikely to be explained by an increase in their startle response, as there were equivalent, low rates of false alarm responding to novel stimuli across groups. As a novel stimulus may also represent a threat, the perception and processing of which may be influenced by other factors, such as anxiety, but, anxiety is unlikely to have influenced our results as there were similar HADS anxiety scores between the groups. While this suggests that the current findings are unlikely to be due to an exaggerated startle response in older adults, it would be of considerable interest to investigate this possibility more directly using other autonomic nervous system measures of startle such as eyeblink. Ford et al. (1997) measured eye blinks and found older adults were less responsive than younger adults, however, they did not use unexpected novel stimuli. Only two previous studies (Friedman et al., 1993; Weisz and Czigler, 2006) have found that older adults give significantly more false alarms to novel stimuli, interpreted as more impulsive responding and/or less inhibition. The finding of increased false alarms to standard stimuli in older adults, shared with Friedman et al. (1993), does not necessarily indicate a deficit in the inhibition of attention to frequent irrelevant stimuli, as the false alarm rate was very small (1.5%), rather we believe that it results from a general enhancement of neural networks underlying attentional processes in older adults. In other words, the threshold for response may be lower in older adults and thus less discriminating. Others have suggested that aging is associated with the recruitment of compensatory neural networks (Cabeza, 2002; Daffner et al., 2006; Riis et al., 2008), and our results may be consistent with this hypothesis also. Although studies have indicated that the prefrontal cortex contributes to the novelty P3 signal (Baudena et al., 1995; Halgren et al., 1995; Kiehl et al., 2001; Yamaguchi et al., 2004), the activity at the surface of the scalp does not necessarily correspond with specific underlying neural generators due to the volume conducting properties of the brain and signal propagation by dipoles. Thus, the increase in frontal activity in older adults does not confirm increased generating power of the original signal or a change in the recruitment of neural regions per se. A further caveat is the use of linked-mastoid reference leads which have the potential to distort topographic maps as there may be asymmetrical impedances between the mastoid areas (Nunez, 1991). Whilst neuroimaging studies have shown greater recruitment of the prefrontal cortex in high performing older adults (e.g. Cabeza et al., 2002), discrepant results are found in electrophysiological 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 was similar between younger and high-performing older adults (e.g. Duarte et al., 2006). In summary, the implications of the findings in the current study are that the aging brain is able to distinguish and process novel stimuli, but subtle differences, particularly in latency and topography, suggest that more widespread neural networks are required 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 been demonstrated (Friedman et al., 1998; Friedman and Simpson, 1994; Weisz and Czigler, 2006). Supporting and extending these data, the present study shows differentiation of activity associated with the novelty P3 at frontal and parietal regions in the younger adults, compatible with the proposition that the novelty P3 is composed of two 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 understanding about the behavioural relevance of such ERP data. It is not clear, therefore, whether such changes in ERP morphology, power and latency with normal aging make cognitive deficit inevitable or if cognitive function is maintained despite these changes and/or adapted. In order to explore this issue, we administered the RSPM as a test of “[...] the ability to reason and solve problems involving new information, without relying extensively on an explicit base of declarative knowledge derived from schooling or previous experience” (Carpenter et al., 1990, p. 404). Thus, similar to the ERP novelty paradigm, it is also a measure of the ability to attend to and process novel information but with a view to decision making. Moreover, Fjell and Walhovd (2003) found that better Matrices subtest scores were associated with increased P3 amplitudes elicited by target and deviant and tones at central and parietal regions. We hypothesised that if novelty habituation reflects the efficiency of novelty processing, then the extent of decrease in frontal novelty P3 amplitude with habituation might be related to performance on Raven's SPM, but this was not the case in younger adults, nor was there any association in the older adults, in whom there was the opposite pattern of an increase in frontal novelty P3 amplitude with increasing time spent on task. This highlights that the relationship between neuropsychological (the RSPM test) and ERP measures in normal aging is complex, but that such investigation may be key to understanding the relevance of ERP data. Two important discussion points arise from our data. Firstly, the use of more sensitive neuropsychological measures is an obvious starting point in any progression of this line of research. For example, the novelty P3 reflects relatively early sensory processing of novel information (within half a second of hearing the stimulus), whereas the Raven's SPM was not timed, and success on this task is likely to be determined by the interaction of more complex networks. Secondly, as both our novelty ERP and RSPM tasks share a requirement for novelty processing, and thus are theoretically similar, it must be considered that lack of significant findings is due to insufficient statistical power. Of note, whilst the hypothesised correlations were not significant, they were of moderate strength [r (11) = −0.33; r (12) = 0.31; younger and older adults, respectively; negative difference scores indicated a reduction in amplitude with time, whereas a positive score indicated an increase], showing that 10% of the shared variance between the change in novelty P3 amplitude with habituation was related to better fluid intelligence. If confirmed,1 this would indicate support for the view that increased novelty P3 amplitude in 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 required to find relationships with an alpha level of .05, power .80 (G*Power 3 program: Faul et al., 2007).

interpretation of normal aging underpinned by subtle and normal changes (adaptation) in brain function, rather than one of deficit which may be the most logical inference from the results of some earlier studies (e.g. Fabiani et al., 1998; Fabiani and Friedman, 1995). In summary, we found that older adults had similar novelty processing to younger adults, albeit delayed. The contrasting increase in frontal novelty P3 amplitude and orientation in our older adults is consistent with the view that each novel stimulus is treated more as new than as familiar (cf. Amenedo and Diaz, 1998). Thus, this may reduce older adults' capacity for habituation and learning to which Courchesne et al. (1975) originally referred. Lack of novelty P3 habituation over the frontal lobes in older adults is compatible with the proposition that older adults are less able to construct “novel category templates” (Friedman and Simpson, 1994, p. 62). Particularly pertinent, however, it may not be assumed on the basis of our ERP findings, that such habituation reflects behaviour in everyday life, and few studies have attempted to validate such claims by looking for associations between ERP components and neuropsychological measures.

Acknowledgments This study was funded by the Economic Social Research Council, The Gerald Kerkut Trust and the Alzheimer's Research Trust. We thank Dr. Torsten Baldeweg (Institute of Child Health, University College London, UK) for his permission to use his novelty auditory oddball paradigm and for his helpful comments. Our gratitude extends to Miguel A. Rodriguez, Compumedics, UK, and Luke Phillips, Computer Sciences Corporation, UK, for software program design and technical support.

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