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Age and novelty: Event-related potentials to visual stimuli within an auditory oddball—visual detection task
International Journal of Psychophysiology 62 (2006) 290 – 299 www.elsevier.com/locate/ijpsycho
Age and novelty: Event-related potentials to visual stimuli within an auditory oddball—visual detection task István Czigler ⁎, Lívia Pató, Emese Poszet, László Balázs Institute for Psychology of the Hungarian Academy of Sciences, 1394 Budapest, P.O. Box 398, Hungary Received 30 August 2005; received in revised form 11 May 2006; accepted 24 May 2006 Available online 11 July 2006
Abstract Age-related change of event-related potentials to novel visual stimuli was investigated while participants attended to both auditory and visual stimulation. Meaningful but irrelevant pictures (novel stimuli) were presented to younger (mean = 21.8, range = 18–26 years) and older (mean = 70.0, range = 60–78) participants (10 in each group). The participants were performing an auditory oddball task and counting silently the changes of a visually presented letter. In the younger group novel stimuli elicited a posterior positivity in the 220–255 ms range. This component habituated to the repetition of the same picture. In the older group this component had longer latency, and did not habituate. A later positivity had shorter latency and larger amplitude in the younger group, but this positivity was preceded by a negative component (N2b) only in the elderly. Results show decreased sensitivity to the content of the visual stimuli in an earlier stage of novelty processing in the elderly, and the age-related slowing of both orientation-related and task-related processes. © 2006 Elsevier B.V. All rights reserved. Keywords: Aging; Event-related potentials; Attention; Novelty processing; N2b; P3
1. Introduction Environmental events carry too much information for the cognitive system to fully process stimuli unrelated to the ongoing behavior. However, in order to detect potentially important (threatening or rewarding) events, the organism has to possess a system, capable of organizing transient shifts of attention. Since orienting activity may interrupt the processing of task-related stimuli, the inhibition of such activity is equally important if it turns out that the disrupting stimuli are irrelevant. Majority of the event-related potential (ERP) investigations of age-related differences in the processing of irrelevant novel stimuli were conducted in the auditory modality. Therefore the aim of the present study was the investigation of age-related differences in the processing of novel stimuli in the visual modality. As a specific aim, we investigated the effect of the repetition of identical irrelevant stimuli in younger and older groups.
⁎ Corresponding author. Tel.: +36 1 354 2290; fax: +36 1 354 2416. E-mail address: [email protected] (I. Czigler). 0167-8760/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2006.05.008
The effects of task-irrelevant stimuli are most frequently investigated in the three stimuli oddball (Squires et al., 1975) and novelty oddball (Courchesne et al., 1975) paradigms. In both paradigms infrequent target and frequent non-target stimuli are presented. In the three stimulus paradigm there are also infrequent irrelevant stimuli, usually highly discriminable from the target and non-target, whereas in the novelty paradigm the infrequent irrelevant stimuli are different in all trials. Irrelevant stimuli in both paradigms elicit similar late positive components (P3a and novel P3, respectively). The two components have similar scalp distribution, and they are frequently more anterior than the distribution of the target-related P3b component (e.g. Courchesne et al., 1975; Cycowicz and Friedman, 1998; Dien et al., 2004; Friedman and Simpson, 1994; Katayama and Polich, 1998; Knight, 1984; Simons et al., 2001; Squires et al., 1975), but the amplitude, latency, and even the distribution of the P3a/ novel are dependent on the relationship between the stimuli of the ongoing task and the irrelevant stimuli (Comerchero and Polich, 1998). In this paper we use the term P3novel for the late positivity evoked by task-irrelevant visual stimuli. This term describes only the relation between the eliciting stimuli (novel) and the component (late positivity), i.e. we do not intend to
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suggest that this positivity is specific to stimulus novelty. In fact, related late positivities are elicited even by the task relevant stimuli of oddball sequences and stimuli of other designs (Dien et al., 2004). The involvement of frontal structures in generation of the P3novel is generally accepted (e.g. Alho et al., 1998; Baudena et al., 1995; Escera et al., 2001; Knight, 1984; Mecklinger and Ullsperger, 1995). Beside the classical” P3a/novel (i.e. a positivity with peak latency longer than 300 ms), in the auditory modality an earlier P3a emerged with 230 ms latency (Escera et al., 1998, 2001). Emergence of this component is attributed to the activity of a broad neural network, involving auditory structures in the temporal lobe (Alho et al., 1998). Concerning visual novelty, using intra-cranial recording, Halgren et al. (1995) obtained early novelty effects in visual structures like in the fusiform gyrus, latetal occipito-temporal areas and MT. It is supposed that this activity is driven by a feed-back loop, originated in anterior structures (Baudena et al., 1995; Yago et al., 2003). On a functional level, as Polich and his colleagues (Comerchero and Polich, 1998; Demiralp et al., 2001) emphasized, P3a is elicited when attention is diverted by stimuli outside the task set. It seems that the emergence of this component follows the categorization of the eliciting stimuli (Friedman et al., 2003). Late positive components are usually preceded by a negative component, the anterior N2 (N2b). This component is considered to be a correlate of attentional orientation (Näätänen and Picton, 1986). Event-related potential research indicates that the effects of stimuli unrelated to the ongoing task (novel stimuli) are compromised in the elderly. Older adults show less responsiveness to task-irrelevant and/or novel stimuli, and repetition of novel stimuli habituates in less extent in the elderly (see Kok, 2000 for a review). However, this view is based on the results of auditory studies which reported a larger late positive component (P3a) with faster habituation in younger adults (Friedman and Simpson, 1994; Friedman et al., 1998; Gaeta et al., 2001). In spite of the relatively large body of research on younger participants in the visual modality only few studies investigated the age-related effects. In a recent study as a function of age P3a latency increased and P3a amplitude decreased (Fjell and Walhovd, 2004). The amplitude change was larger in the vertex than in more anterior locations. However, in this study all irrelevant stimuli were identical (a rectangle within the train of target and non-target ellipses). In some studies irrelevant but rare stimuli elicited smaller N2b in the elderly (e.g. Czigler et al., 1994). However, opposite results were also reported, i.e. novel auditory stimuli elicited larger N2b in older participants (Friedman et al., 1998). In a visual letter-matching task (Czigler and Balázs, 2005) a large anterior negativity emerged to novel stimuli in younger participants, while no such activity appeared in the older group. The authors related the negativity to inhibitory processes, similar to the Nogo negativity, which was reported to be smaller in the elderly (Falkenstein et al., 2002).
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In the present study the novel stimuli were highly different from those of the ongoing tasks presented. Participants performed an auditory oddball task, i.e. they responded to button press to infrequent (target) tones within the series of frequent ones. In order to ensure fixation to the location of the onset of novel stimuli, a concomitant visual task was also introduced. The participants silently counted the infrequent change of continuously presented letters. This way it was a divided attention task with the occasional presentation of irrelevant meaningful pictures. Due to the presentation of taskrelated and unrelated stimuli, we were able to compare the endogenous components (N2b and P3) to target and non-target (novel) stimuli in the two age-groups. The same picture appeared once, two, or three times in different stimulus sequences, therefore we had the possibility to assess the possibility of age-related change of content-specific ERP habituation. 2. Materials and methods 2.1. Participants Ten older (five women, mean age = 70.0 years, range = 60– 78 years) and 10 younger adults (five women, mean age = 21.8 years, range = 18–26 years) participated in the study. The older participants were recruited through advertisements. Their expenses were reimbursed. According to a health questionnaire1 they were all healthy. All but one had university degrees. The younger participants were the students of various universities in Budapest. According to the Hungarian version of the Wechsler Adult Intelligence Scale (Kun and Szegedi, 1977) there was no IQ difference between the groups [124.3 and 121.6 in the older and younger groups, respectively; t(18) < 1)]. Participants had normal or corrected to normal vision and normal hearing. Due to misunderstanding of the task (one older participant) or excessive eye movements and other artefacts (two older and three younger participants), the data of additional six participants were omitted. An informed consent had been obtained from all participants. 2.2. Stimuli and procedure Auditory stimuli were pure tones of 600 Hz (Standard) and 700 Hz (Target) tones of 70 db SPL, presented binaurally via earphones. Stimulus duration was 50 ms (5 ms rise and fall time). Visual stimuli were presented on a sVGA monitor. The background was light grey (42 cd/m2). Black capital letters (A or B, 0.6° horizontally and 0.9° vertically) appeared in the center of the screen. Throughout the stimulus sequences letter A was continuously present, except from periods of 950 ms, when
1 There is no standardized health questionnaire in Hungarian. This questionnaire concentrated on medication, vascular, neurological and psychiatric diseases.
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it was replaced by letter B (Visual Target) or Novel. Novel stimuli were various colored pictures depicting landscapes, animals, flowers and urban scenes. Pictures had no larger dimension (neither horizontal nor vertical) than 8°, and appeared in the center of the screen for 950 ms. Visual stimuli (visual target and novels) appeared always together with Standard tones. Within a stimulus sequence there were Standards alone (p = 0.68), Auditory targets (p = .012), Visual targets and Standards (p = 0.05) and Novels and Standards (p = 0.15). Inter-stimulus interval was 1100– 1200 ms between the pure auditory stimuli and 2050– 2150 ms after the audio-visual compounds (this way the offset-onset duration was constant). Average duration of the stimulus sequences was 6 min. The experiment was controlled by the E-Prime software. Fig. 1 shows the general outline of the stimulus sequences. There were three types of sequences, namely either each Novel was presented once, twice in successive Novel presentations, or three times in successive Novel presentations. The interval between two presentations of the identical Novels was 3–4 s. Within a session the sequence types were presented two times, in different random order for each participant. In each sequence there were different Novels. No target stimulus appeared after a visual stimulus, and vice versa. Measured sequences were preceded by a practice sequence of 6 min. This sequence was identical to the measured sequences with one repetition of the Novel. Participants were instructed to respond with button press (right hand) to the appearance of the target tone (“as fast as possible, but without error”), and count silently the appearance of letter B. (They reported the result of the count at the end of the sequence). 2.3. EEG recording and data analysis EEG was recorded (0.5–70 Hz, 30 Hz upper cut offline filtering; 250 Hz sampling rate, NeuroScan NuAmps amplifier), using an electrode cap (Easy Cap). Ag/AgCl electrodes were placed on Fp1, Fp2, Fpz, F3, Fz, F4, Pz, T3, T4, T5, T6, OL
(2 cm from O1), O1, Oz, O2, OR (2 cm from O2) locations. The reference electrodes were on the nose tip, the ground was on the forehead. Electrode impedance was below 5 Ω. Bipolar recordings monitored eye movement between electrodes above and below the right eye, and electrodes near the outer canthi of the two eyes. Epochs were created from − 100 to 800 ms post-stimulus. Epochs containing amplitude changes larger that 70 μV on any EEG or EOG channels (except from the occipital ones) were rejected from further analysis. Genuine occipital responses have frequently larger amplitude, therefore the limit on the occipital locations was 100 μV. ERPs were averaged separately for Standard, Target, Novel plus Standard and Letter plus Standard stimuli. Even in case of the least number of individual ERPs (three repetition of the same novel) at least 16 responses were averaged. Due to the long-lasting effects, ERPs to Standard stimuli following an auditory target or visual stimuli were omitted from averaging. In this study we concentrated on the novelty-related ERP components, therefore age-related effects on the ‘endogenous’ (P1 and N1) and target-related (P3b) components will be summarized only briefly. In order to disclose the novelty effects, the ERPs to the Standard stimuli were subtracted from ERPs elicited by the Novel plus Standard compound. Components of event-related activity were identified from the group average difference potentials. Amplitudes were measured as mean values around the peak values of the group average, and individual participants' mean amplitude values were scored using these windows. The ranges of the windows were ± 12 ms for the N2b (at Fz location) and late positive components (at Oz location for the P3novel/early and at Cz for the other late positive components). Unless otherwise stated, ERP data were analyzed in mixed factor ANOVAs with factors of age-group as between group factor, and electrode location [Fpz, Fz, Cz, Pz (midline locations) or O1, Oz, O2 (posterior locations)] as within group factor. ERP components to visual stimuli were analyzed in difference potentials, i.e. ERPs to Standard were subtracted from the ERPs to visual–auditory compounds and from the auditory Target. When appropriate, the Greenhouse–Geisser
Fig. 1. Timing and stimulus probabilities of the experimental design.
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Fig. 2. Group average ERPs to Auditory target, Standard,l, Visual target plus Standard event-related potentials (ERPs) and the (Visual Target plus Standard) minus Standard difference potential (n = 10 in both groups).
correction (ε) was applied and the corrected p values are reported. 3. Results 3.1. Behavioral results There was no performance difference between the two agegroups. Although reaction time to the auditory Target was
shorter in the younger group [534 ms (S.E. = 27.3) vs. 571 ms (S.E.M = 28.3), respectively), the difference was not significant [t(18) < 1]. Omission rates were 8.7% (S.E.M. = 3.3) and 7.5% (S.E. = 3.5) in the younger and older group, respectively [t(18) < 1]. Counting of letter changes was scored as the absolute value of difference from the actual number of changes. Results of the younger and older participants were 6.6 (S.E.M. = 1.9) and 2.2 (S.E. = 1.3), respectively. This difference was not significant [t (18) = 1.15].
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Fig. 3. Group average ERPs to the Novel plus Standard stimuli in the old and young participants (n = 10 in both groups). +: P3anovel/early; ⁎: P3anovel/late.
3.2. ERP 3.2.1. Exogenous components and target-related activity Fig. 2 shows the ERPs to the Standard and Target stimuli in the midline locations in the two age-groups.2 Concerning the main age-related differences, the auditory N1 component had longer latency in the elderly. While in the younger group this component had larger amplitude to the Auditory target than to the Standard, in the older group the Standard elicited larger N1. The auditory P2 latency increased in the older participants. N1 to the Visual target was larger in the younger group, whereas P2 had larger amplitude in the elderly. In case of the Auditory target both the N2b and P3b latencies were shorter in the younger group, but the group-related N2b latency difference decreased at Fpz. N2b and P3b had larger amplitude in the younger group. However, while in the younger group the P3b increased from Fz to Cz, the reverse effect appeared in the older group. As Fig. 2 shows, Visual target (letter change) elicited P3b component with longer latency in the elderly. This component had a parietal maximum in the younger group, and more anterior distribution in the elderly.
2 Detailed results and statistics on the endogenous and target-related components are available from the corresponding author.
3.2.2. Novel ERPs Figs. 3 and 4 shows the ERPs to the Novel plus Standard compound and the Novel plus Standard compound minus Standard difference potentials, respectively. Novel stimuli elicited different ERPs in the two age-groups. Comparison of the ERPs to the Novel plus Standard compound and the difference potentials shows that N1 component over the anterior location was an auditory effect (see also the auditory ERPs in Fig. 2).3 N2b component (∼ 300 ms latency) emerged only in the older group. Over the posterior (occipital) locations, and later in the anterior locations two positivities were recorded. Both components had shorter latency in the younger group. Hereafter we refer to the earlier positivity as P3novel/early and to the later positivity as P3novel/late. In the younger group the late positivity was followed by a long-lasting late negative wave. The scalp distribution of the two positivities is shown in Fig. 5. According to an ANOVA with factors of age as between group factor and electrode location (O1, Oz and O2) as within group factor, the P3novel/early latency was longer in the elderly [F 3 We conducted LORETA analysis (Pascual-Marqui et al., 1994) on peaks of the novelty-related components. In both age-groups LORETA analysis located P3novel/early in broad areas of temporal cortex and in the fusiform gyrus. A broad neural network was indicated for the P3novel/late component. In both groups there was activity in the anterior cingular cortex, posterior (Br 18) and parietal (Br 31). In the younger group broader temporal areas were involved in P3novel/late than in the older group. However, it should be noted that due to low density of the electrode array, one has to be cautious in interpreting the LORETA results.
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Fig. 4. Group average Novel plus Standard minus Standard difference potentials in the old and young participants (n = 10 in both groups).
(1,18) = 16.55, p < 0.001]. The amplitude difference was also significant [F(1,18) = 7.50, p < 0.05]. Fig. 6 shows the ERPs to the picture repetitions, while Table 1 shows the latency and amplitude values of the P3novel/early for these repeated stimuli. Repetition effects on P3novel/early amplitude were calculated in two ANOVAs with age as between group factor, and repetition an electrode location as within group factors. We compared the P3novel/early amplitudes for the first, second and third presentation from the three-presentation sequence, and the effect of the first and second presentation from the two-presentation sequence. In the three presentation sequence the main effect of age on P3novel/early was significant [F(1,18) = 4.39, p < .05]. More important, the main effect of repetition and the group × repetition interaction were also significant [F(2, 36) = 4.59, ε = 0.76, p < 0.05 and F(2,36) = 4.00, ε = 0.76, p < 0.05, respectively]. The group × repetition interaction was due to the considerable amplitude decrease in the young group, and the smaller change of the amplitude in the older participants. Similar results appeared in the two-presentation sequence. In this case the group main effect [F(1,18) = 8.74, p < 0.01], the repetition main effect [F(1,18) = 7.94, p < 0.05], and the group × repetition interaction [F(1,18) = 5.78, p < 0.05] were all significant. In separate ANOVAs for the two agegroups the order effects were significant only in the younger participants [F(2,18) = 5.38, ε = 070, p < 0.05 and F(1,9) = 9.67, p < 0.05 in the three-presentation and two-presentation sequences, respectively]. Comparison of amplitudes in the
first presentations of the three, two and single presentation sequences, and the comparison of amplitudes of the second presentations in the three and second presentation sequences did not reveal any significant difference. P3novel/late had longer latency, and it was smaller in the older group. Accordingly, in ANOVAs with factors of age as between group factor and electrode location (Fpz, Fz, Cz, Pz) as within group factor, the main effects of group on the latency and on the amplitude were significant [F(1,18) = 12.58, p < 0.01 and F (1,18) = 5.32, p < 0.05, respectively]. Table 2 shows the amplitude and latency values of the P3novel/late component. In the young group the late positivity was followed by a negative shift. In the 500–600 ms latency range we obtained significant group main effect [F(1,18) = 6.92, p < 0.05], location main effect [F(3,54) = 20.50, ε = 0.45, p < 0.001], and group × location interaction [F(3,54) = 5.29, ε = 0.46, p < 0.05]. The interaction was due to the increase of the negativity from Fpz to Pz. 4. Discussion In the present study novel visual stimuli elicited late positive components with longer latency and smaller amplitude in the older participants. As a new findings of our study, meaningful irrelevant pictures elicited an earlier and a later positive component (P3novel/early and P3novel/late, respectively), and P3novel/early was sensitive to the stimulus content in the younger participants, i.e. repeating the same picture this component
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Fig. 5. Scalp distribution of the Novel minus Standard difference potential in the P3novel/early and the P3novel/late latency ranges in the old and young participants (n = 10 in both groups).
became smaller. One may argue that this amplitude change is due the repeated stimulation of the same structures of lower vision. According to this view the amplitude change is attributed to the habituation of the exogenous P2 component. The latency of the occipital positivity was longer than that of the usual P2 latency. Furthermore, the 3–4 s interval between the two presentations, together with the bright inter-stimulus field and the presence of a high-contrast pattern (the letter) on the field may favor a ‘cognitive’ interpretation. The component we labeled as P3novel/early has a parallel in the auditory modality (Escera et al., 2001, 1998) and also in some intra-cranial recordings (even in posterior visual structures, Halgren et al., 1995). The age-related repetition effects on the posterior positivity (P3novel/early) are similar to findings in the auditory modality, i.e. fast P3a habituation in the younger group and hardly any habituation in the elderly (Friedman et al., 1998). Similar age-related differences were also observed in the electrodermal activity (McDowd and Filion, 1992). Diminished habituation is considered as a sign of compromised inhibitory activity (see Hasher and Zacks, 1988 for a general theory on age-related inhibitory loss). Following a suggestion by Baudena et al. (1995) and Yago et al. (2003), an anterior–posterior feedback loop, activated by the presence of the to-be-processed stimuli is less susceptible to inhibitory processes in the elderly. P3novel/late latency increased and P3novel/late amplitude decreased in the older group. This result corresponds to the age-related latency change of the P3a in the three-stimulus
oddball paradigm (Fjell and Walhovd, 2004; Tachibana et al., 1992). In the younger group P3novel/late had a more posterior distribution than the distribution of this component in the older group. Our results in the younger group were similar to those reported by Comerchero and Polich (1998), Polich (2003). These authors reported similar late positivities to variable novel visual stimuli and to a repeated salient irrelevant visual stimulus. As Polich (2003) pointed out, P3novel (and P3a) distribution is dependent on the context of the irrelevant stimuli (i.e. the stimuli of the ongoing task). In case of easy discrimination, together with highly discrepant infrequent non-target stimuli, late positivity had a posterior maximum (Katayama and Polich, 1998). Indeed, in our experiment the auditory task was relatively easy, and the infrequent non-target was highly different from the task-stimuli (it was in another modality). Accordingly, the context-related interpretation of the P3novel fits to the results of paradigm using both auditory and visual events. The age-related distribution difference of P3novel/late in the present study was similar to that of the P3b component. “Anteriorization” of the late positivities is considered to be the consequence of morphological and functional changes in the frontal cortex (see West, 1996 for a review). However, predictions stemming from the supposed compromised frontal activity are equivocal. Enlarged frontal positivity can be explained as a consequence of compensatory activity, e.g. the recruitment of larger cortical areas. As a more
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Fig. 6. Repetition effects on the average Novel minus Standard difference potentials in the young and old participants (n = 10 in both groups) from sequences with three repetitions. Group average Novel plus Standard minus Standard difference potentials from the sequences with three repetitions of identical novel stimuli.
sophisticated account age-related distribution difference is due to the longer orientation and categorization processes in the elderly (Friedman et al., 1998). While in younger participants the “task-irrelevant stimulus” category is quickly established, this process may be slower in the elderly. The different speed of categorization may be reflected by the different involvement of anterior and posterior structures in the age-groups. In the present study the age and novelty effects on the N2b component were different from the results of previous
experiments (Czigler and Balázs, 2005). When novel visual stimuli were mixed to the trials of a letter-matching task, these stimuli elicited a large anterior negativity in the younger group, and only small P3a. Neither of these components emerged in the older group. On the contrary, in the present study novel visual stimuli elicited positivities in both groups, and the N2b-like activity was absent in the younger group. The absence of N2b in the young group can be attributed to the masking effect of the ascending limb of the P3novel/late. We have only a post hoc explanation for the discrepant results of the present study and
Table 1 Group average latency (ms) and amplitude (μV) values of the P3novel/early component to the first, second and third presentation in the younger and older participants Three presentations
Two presentations
Younger 1
Older
Younger
One presentation Older
Younger
Older
256 (8.4) 241 (11.1) 246 (10.4)
228 (4.4) 231 (8.1) 231 (9.4)
255 (9.5) 257 (9.0) 250 (11.3)
4.5 (1.4) 3.6 (1.6) 3.8 (1.7)
12.1 (1.2) 10.1 (1.3) 10.9 (1.5)
3.7 (1.4) 2.9 (1.5) 3.4 (1.8)
2
3
1
2
3
1
2
1
2
Latency O1 223 (2.8) Oz 222 (3.0) O2 221 (3.2)
230 (5.3) 230 (8.6) 231 (7.9)
231 (7.9) 234 (9.5) 231 (7.9)
259 (9.7) 259 (9.6) 253 (11.3)
251 (8.8) 250 (10.2) 247 (10.1)
256 (8.6) 248 (9.7) 255 (9.5)
223 (4.0) 221 (4.0) 222 (3.8)
240 (8.7) 237 (8.5) 237 (8.7)
251 (12.1) 248 (11.8) 248 (11.8)
Amplitude O1 13.1 (2.4) Oz 12.1 (2.4) O2 12.6 (2.6)
10.7 (2.1) 9.4 (1.9) 10.0 (2.2)
8.5 (1.1) 7.3 (1.3) 7.7 (1.3)
5.1 (1.4) 4.7 (1.4) 5.1 (1.7)
4.4 (1.0) 3.7 (1.1) 4.4 (1.2)
3.9 (1.3) 4.6 (1.7) 4.3 (1.7)
14.2 (1.7) 13.1 (1.5) 14.1 (2.0)
11.0 (2.1) 10.0 (2.0) 10.9 (2.2)
4.4 (1.5) 3.9 (2.6) 4.5 (1.9)
The values were calculated from the difference potentials (n = 10 in both groups; S.E. in parenthesis).
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Table 2 Group average latency (ms) and amplitude (μV) values of the P3novel/late components in the younger and older participants (n = 10 in both groups; S.E. in parenthesis) Latency
Fpz Fz Cz Pz
Amplitude
Younger
Older
Younger
Older
386 (10.6) 343 (12.5) 335 (6.8) 347 (10.3)
392 (15.2) 400 (16.6) 385 (15.4) 379 (17.6)
3.0 (0.3) 5.9 (0.9) 6.9 (1.3) 7.3 (1.8)
1.5 3.0 3.3 2.9
(0.4) (0.8) (0.8) (1.7)
that of the results reported by Czigler and Balázs (2005). This is because the antecedent conditions of the emergence of the P3a/ P3novel/late are unclear (Dien et al., 2004), and the situation is similar in case of the N2b component. On the one hand, in the matching task the stimuli to-be-compared were presented simultaneously, and the stimuli of the previous trials carried no information about the next trial. Therefore no specific memory representations of the task-related stimuli were required. On the other hand, the oddball task of the present study required the memory representation of the task-related stimuli. Even if the memory representation was simple (like in the majority of the oddball tasks) this memory representation had to be preserved during the processing of the novel stimuli. This is why the present task may be more sensitive to the disturbing effects of the novel stimuli than the matching task. This shift of attention and/or the demand for the inhibition of the consequences of the involuntary attentional shift may contribute to the emergence of the P3novel components. In this study we replicated some earlier age-related ERP results. Late positivity to the auditory and visual targets (P3b) delayed in the older participants (e.g. Anderer et al., 1998; Czigler et al., 1994; Iragui et al., 1993; Knott et al., 2003; Polich, 1996). P3b amplitude was smaller in the elderly. P3b distribution was different in the two age-groups, i.e. P3b difference was larger over the posterior locations (see Friedman et al., 1997 for a review). We also replicated the age-related delay and amplitude decrease of the N2b to the auditory target (e.g. Amenedo and Díaz, 1998). The obvious delay of the novelty-related and targetrelated components in the older can be attributed to a manifestation of the general age-related slowing of mental operations (e.g. Cerella, 1985; Salthouse, 1996). Acknowledgements This research was supported by NKFF5/0071/2002 and OTKA T47038 grants. We thank Drs. Júlia Weisz and István Winkler for their help and Gabriella Pálfy and Zsuzsa d'Albini for their technical assistance. References Alho, K., Winkler, I., Escera, C., Huotilainen, M., Virtanen, J., Jääskeläinen, I.P., Pekkonen, E., Ilmoinemi, R.J., 1998. Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings. Psychophysiology 35, 200–204.
Amenedo, E., Díaz, F., 1998. Aging-related changes in processing of non-target and target stimuli during an auditory oddball task. Biol. Psychol. 48, 235–267. Anderer, P., Pasqual-Marqui, R.D., Semlitsch, H.V., Saletu, B., 1998. Differential effects of normal aging on sources of standard N1, target N1 and target P300 auditory event-related brain potentials revealed by low resolution electromagnetic tomography (LORETA). Evoked Potentials— Electroencephalogr. Clin. Neurophysiol. 108, 160–174. Baudena, P., Halgren, E., Heit, G., Clarke, J.M., 1995. Intracerebral potentials to rare visual stimulus and distractor auditory and visual stimuli: III. Frontal cortex. Electroencephalogr. Clin. Neurophysiol. 94, 251–264. Cerella, J., 1985. Information processing rates in the elderly. Psychol. Bull. 98, 67–83. Comerchero, M.D., Polich, J., 1998. P3a, perceptual distinctiveness, and stimulus modality. Cogn. Brain Res. 7, 41–48. Courchesne, E., Hillyard, S.A., Galambos, R., 1975. Stimulus novelty, task relevance and visual evoked-potential in man. Electroencephalogr. Clin. Neurophysiol. 39, 131–143. Cycowicz, Y.M., Friedman, D., 1998. Effect of sound familiarity on the eventrelated potentials elicited by novel environmental sounds. Brain Cogn. 36, 30–51. Czigler, I., Balázs, L., 2005. Age-related effects of novel visual stimuli in a letter-matching task: an event-related potential study. Biol. Psychol. 69, 229–242. Czigler, I., Csibra, G., Ambró, Á., 1994. Event-related potentials and aging: identification of deviant visual stimuli. J. Psychophysiol. 8, 193–210. Demiralp, T., Ademoglu, A., Comerchero, M.D., Polich, J., 2001. Wavelet analysis of P3a and P3b. Brain Topogr. 13, 251–267. Dien, J., Spencer, K.M., Donchin, E., 2004. Parsing the late positive complex: mental chronometry and the ERP components that inhibit the neighborhood of the P300. Psychophysiology 41, 665–678. Escera, C., Alho, K., Winkler, I., Näätänen, R., 1998. Neural mechanisms of involuntary attention to acoustic novelty and change. J. Cogn. Neurosci. 10, 590–604. Escera, C., Yago, E., Alho, K., 2001. Electrical responses reveal the temporal dynamics of brain events during involuntary attention switching. Eur. J. Neurosci. 14, 877–883. Falkenstein, M., Hoorman, J., Hohnsbein, J., 2002. Inhibition-related ERP components: variation with modality, age and time-on task. J. Psychophysiol. 16, 167–175. Fjell, A.M, Walhovd, K.B., 2004. Life-span changes in P3a. Psychophysiology 41, 74–83. Friedman, D., Simpson, G., 1994. ERP amplitude and scalp distribution to target and novel events—effects of temporal-order in young, middle-aged and older adults. Cogn. Brain Res. 2, 49–63. Friedman, D., Kazmersi, V.A., Fabiani, M., 1997. An overview of age-related changes in the scalp distribution of P3b. Electroencephalogr. Clin. Neurophysiol. 104, 498–513. Friedman, D., Kazmerski, V.A., Cycowicz, Y.M., 1998. Effects of aging on the novelty P3 during attend and ignore oddball tasks. Psychophysiology 35, 508–520. Friedman, D., Cycowicz, Y.M., Dziobek, I., 2003. Cross-form conceptual relations between sounds and words: effects on the novelty P3. Cogn. Brain Res. 18, 58–64. Gaeta, H., Friedman, D., Ritter, W., Cheng, J., 2001. An event-related potential evaluation of involuntary attentional shifts in young and older adults. Psychol. Aging 16, 55–68. Halgren, E., Baudena, P., Clarke, J.M., Heit, G., Marinkovic, K., Devaux, B., Vignal, J., Biraben, A., 1995. Intracerebral potentials to rare target and distractor auditory and visual stimuli: II. Medial, lateral and posterior temporal lobe. Electroencephalogr. Clin. Neurophysiol. 94, 229–250. Hasher, L., Zacks, R.T., 1988. Working memory, comprehension, and aging: a review and a new view. In: Bower, G.G. (Ed.), The Psychology of Learning and Motivation, vol. 22. Academic Press, San Diego, CA, pp. 193–225. Iragui, V.J., Kutas, M., Mitchiner, M.R., Hillyard, S.A., 1993. Effects of aging on event-related brain potentials and reaction time in an auditory oddball task. Psychophysiology 30, 10–22.
I. Czigler et al. / International Journal of Psychophysiology 62 (2006) 290–299 Katayama, J., Polich, J., 1998. Stimulus context determines P3a and P3b. Psychophysiology 35, 23–33. Knight, R.T., 1984. Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr. Clin. Neurophysiol. 59, 9–20. Knott, V., Bradford, L., Dulude, L., Millar, A., Alwahabi, F., Lau, T., Shea, S., Wiens, A., 2003. Effects of stimulus modality and response mode on the P300 event-related potential differentiation of young and elderly adults. Clin. Electrophysiol. 34, 182–190. Kok, A., 2000. Age-related changes in involuntary and voluntary attention as reflected in components of the event-related potential (ERP). Biol. Psychol. 54, 107–143. Kun, M., Szegedi, M., 1977. Az intelligencia mérése. Akadémiai Kiadó, Budapest. McDowd, J.M., Filion, D.F., 1992. Aging, selective attention, and inhibitory processes: a psychophysiological approach. Psychol. Aging 7, 65–71. Mecklinger, A., Ullsperger, P., 1995. The P300 to novel and target events: a spatiotemporal dipole model analysis. NeuroReport 7, 241–245. Näätänen, R., Picton, T., 1986. N2 and automatic versus controlled processes. In: McCallum, W.C., Zapolli, R., Denoth, F. (Eds.), Cerebral Psychophysiology: Studies in Event-Related Potentials. EEG Supplement, vol. 38. Elsevier, Amsterdam, pp. 169–187. Pascual-Marqui, R.D., Michel, C.M., Lehmann, D., 1994. Low-resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int. J. Psychophysiol. 18, 49–65.
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Polich, J., 1996. Meta-analysis of P300 normative aging studies. Psychophysiology 33, 334–353. Polich, J., 2003. Theoretical overview of P3a and P3b. In: Polich, J. (Ed.), Detection of Change: Event-Related Potential and fMRI Findings. Kluwer Academic Publishers, Boston, pp. 83–98. Salthouse, T.A., 1996. The processing speed theory of adult age differences in cognition. Psychol. Rev. 103, 403–428. Simons, R.F., Graham, F.K., Miles, M.A., Chen, X., 2001. On the relationship of P3a and the Novelty-P3. Biol. Psychol. 56, 207–218. Squires, N.K., Squires, K.C., Hillyard, S.A., 1975. Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalogr. Clin. Neurophysiol. 38, 387–401. Tachibana, H., Toda, K., Sugita, M., 1992. Age-related changes in attended and unattended P3-latency in normal subjects. Int. J. Neurosci. 66, 277–284. West, R.L., 1996. An application of prefrontal cortex function theory to cognitive aging. Psychol. Bull. 120, 272–292. Yago, E., Escera, C., Alho, K., Giard, M.-H., Serra-Grabulosa, J.M., 2003. Spatiotemporal dynamics of the auditory novelty-P3 event-related brain potential. Cogn. Brain Res. 16, 383–390.
Age and novelty: Event-related potentials to visual stimuli within an auditory oddball—visual detection task István Czigler ⁎, Lívia Pató, Emese Poszet, László Balázs Institute for Psychology of the Hungarian Academy of Sciences, 1394 Budapest, P.O. Box 398, Hungary Received 30 August 2005; received in revised form 11 May 2006; accepted 24 May 2006 Available online 11 July 2006
Abstract Age-related change of event-related potentials to novel visual stimuli was investigated while participants attended to both auditory and visual stimulation. Meaningful but irrelevant pictures (novel stimuli) were presented to younger (mean = 21.8, range = 18–26 years) and older (mean = 70.0, range = 60–78) participants (10 in each group). The participants were performing an auditory oddball task and counting silently the changes of a visually presented letter. In the younger group novel stimuli elicited a posterior positivity in the 220–255 ms range. This component habituated to the repetition of the same picture. In the older group this component had longer latency, and did not habituate. A later positivity had shorter latency and larger amplitude in the younger group, but this positivity was preceded by a negative component (N2b) only in the elderly. Results show decreased sensitivity to the content of the visual stimuli in an earlier stage of novelty processing in the elderly, and the age-related slowing of both orientation-related and task-related processes. © 2006 Elsevier B.V. All rights reserved. Keywords: Aging; Event-related potentials; Attention; Novelty processing; N2b; P3
1. Introduction Environmental events carry too much information for the cognitive system to fully process stimuli unrelated to the ongoing behavior. However, in order to detect potentially important (threatening or rewarding) events, the organism has to possess a system, capable of organizing transient shifts of attention. Since orienting activity may interrupt the processing of task-related stimuli, the inhibition of such activity is equally important if it turns out that the disrupting stimuli are irrelevant. Majority of the event-related potential (ERP) investigations of age-related differences in the processing of irrelevant novel stimuli were conducted in the auditory modality. Therefore the aim of the present study was the investigation of age-related differences in the processing of novel stimuli in the visual modality. As a specific aim, we investigated the effect of the repetition of identical irrelevant stimuli in younger and older groups.
⁎ Corresponding author. Tel.: +36 1 354 2290; fax: +36 1 354 2416. E-mail address: [email protected] (I. Czigler). 0167-8760/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2006.05.008
The effects of task-irrelevant stimuli are most frequently investigated in the three stimuli oddball (Squires et al., 1975) and novelty oddball (Courchesne et al., 1975) paradigms. In both paradigms infrequent target and frequent non-target stimuli are presented. In the three stimulus paradigm there are also infrequent irrelevant stimuli, usually highly discriminable from the target and non-target, whereas in the novelty paradigm the infrequent irrelevant stimuli are different in all trials. Irrelevant stimuli in both paradigms elicit similar late positive components (P3a and novel P3, respectively). The two components have similar scalp distribution, and they are frequently more anterior than the distribution of the target-related P3b component (e.g. Courchesne et al., 1975; Cycowicz and Friedman, 1998; Dien et al., 2004; Friedman and Simpson, 1994; Katayama and Polich, 1998; Knight, 1984; Simons et al., 2001; Squires et al., 1975), but the amplitude, latency, and even the distribution of the P3a/ novel are dependent on the relationship between the stimuli of the ongoing task and the irrelevant stimuli (Comerchero and Polich, 1998). In this paper we use the term P3novel for the late positivity evoked by task-irrelevant visual stimuli. This term describes only the relation between the eliciting stimuli (novel) and the component (late positivity), i.e. we do not intend to
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suggest that this positivity is specific to stimulus novelty. In fact, related late positivities are elicited even by the task relevant stimuli of oddball sequences and stimuli of other designs (Dien et al., 2004). The involvement of frontal structures in generation of the P3novel is generally accepted (e.g. Alho et al., 1998; Baudena et al., 1995; Escera et al., 2001; Knight, 1984; Mecklinger and Ullsperger, 1995). Beside the classical” P3a/novel (i.e. a positivity with peak latency longer than 300 ms), in the auditory modality an earlier P3a emerged with 230 ms latency (Escera et al., 1998, 2001). Emergence of this component is attributed to the activity of a broad neural network, involving auditory structures in the temporal lobe (Alho et al., 1998). Concerning visual novelty, using intra-cranial recording, Halgren et al. (1995) obtained early novelty effects in visual structures like in the fusiform gyrus, latetal occipito-temporal areas and MT. It is supposed that this activity is driven by a feed-back loop, originated in anterior structures (Baudena et al., 1995; Yago et al., 2003). On a functional level, as Polich and his colleagues (Comerchero and Polich, 1998; Demiralp et al., 2001) emphasized, P3a is elicited when attention is diverted by stimuli outside the task set. It seems that the emergence of this component follows the categorization of the eliciting stimuli (Friedman et al., 2003). Late positive components are usually preceded by a negative component, the anterior N2 (N2b). This component is considered to be a correlate of attentional orientation (Näätänen and Picton, 1986). Event-related potential research indicates that the effects of stimuli unrelated to the ongoing task (novel stimuli) are compromised in the elderly. Older adults show less responsiveness to task-irrelevant and/or novel stimuli, and repetition of novel stimuli habituates in less extent in the elderly (see Kok, 2000 for a review). However, this view is based on the results of auditory studies which reported a larger late positive component (P3a) with faster habituation in younger adults (Friedman and Simpson, 1994; Friedman et al., 1998; Gaeta et al., 2001). In spite of the relatively large body of research on younger participants in the visual modality only few studies investigated the age-related effects. In a recent study as a function of age P3a latency increased and P3a amplitude decreased (Fjell and Walhovd, 2004). The amplitude change was larger in the vertex than in more anterior locations. However, in this study all irrelevant stimuli were identical (a rectangle within the train of target and non-target ellipses). In some studies irrelevant but rare stimuli elicited smaller N2b in the elderly (e.g. Czigler et al., 1994). However, opposite results were also reported, i.e. novel auditory stimuli elicited larger N2b in older participants (Friedman et al., 1998). In a visual letter-matching task (Czigler and Balázs, 2005) a large anterior negativity emerged to novel stimuli in younger participants, while no such activity appeared in the older group. The authors related the negativity to inhibitory processes, similar to the Nogo negativity, which was reported to be smaller in the elderly (Falkenstein et al., 2002).
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In the present study the novel stimuli were highly different from those of the ongoing tasks presented. Participants performed an auditory oddball task, i.e. they responded to button press to infrequent (target) tones within the series of frequent ones. In order to ensure fixation to the location of the onset of novel stimuli, a concomitant visual task was also introduced. The participants silently counted the infrequent change of continuously presented letters. This way it was a divided attention task with the occasional presentation of irrelevant meaningful pictures. Due to the presentation of taskrelated and unrelated stimuli, we were able to compare the endogenous components (N2b and P3) to target and non-target (novel) stimuli in the two age-groups. The same picture appeared once, two, or three times in different stimulus sequences, therefore we had the possibility to assess the possibility of age-related change of content-specific ERP habituation. 2. Materials and methods 2.1. Participants Ten older (five women, mean age = 70.0 years, range = 60– 78 years) and 10 younger adults (five women, mean age = 21.8 years, range = 18–26 years) participated in the study. The older participants were recruited through advertisements. Their expenses were reimbursed. According to a health questionnaire1 they were all healthy. All but one had university degrees. The younger participants were the students of various universities in Budapest. According to the Hungarian version of the Wechsler Adult Intelligence Scale (Kun and Szegedi, 1977) there was no IQ difference between the groups [124.3 and 121.6 in the older and younger groups, respectively; t(18) < 1)]. Participants had normal or corrected to normal vision and normal hearing. Due to misunderstanding of the task (one older participant) or excessive eye movements and other artefacts (two older and three younger participants), the data of additional six participants were omitted. An informed consent had been obtained from all participants. 2.2. Stimuli and procedure Auditory stimuli were pure tones of 600 Hz (Standard) and 700 Hz (Target) tones of 70 db SPL, presented binaurally via earphones. Stimulus duration was 50 ms (5 ms rise and fall time). Visual stimuli were presented on a sVGA monitor. The background was light grey (42 cd/m2). Black capital letters (A or B, 0.6° horizontally and 0.9° vertically) appeared in the center of the screen. Throughout the stimulus sequences letter A was continuously present, except from periods of 950 ms, when
1 There is no standardized health questionnaire in Hungarian. This questionnaire concentrated on medication, vascular, neurological and psychiatric diseases.
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it was replaced by letter B (Visual Target) or Novel. Novel stimuli were various colored pictures depicting landscapes, animals, flowers and urban scenes. Pictures had no larger dimension (neither horizontal nor vertical) than 8°, and appeared in the center of the screen for 950 ms. Visual stimuli (visual target and novels) appeared always together with Standard tones. Within a stimulus sequence there were Standards alone (p = 0.68), Auditory targets (p = .012), Visual targets and Standards (p = 0.05) and Novels and Standards (p = 0.15). Inter-stimulus interval was 1100– 1200 ms between the pure auditory stimuli and 2050– 2150 ms after the audio-visual compounds (this way the offset-onset duration was constant). Average duration of the stimulus sequences was 6 min. The experiment was controlled by the E-Prime software. Fig. 1 shows the general outline of the stimulus sequences. There were three types of sequences, namely either each Novel was presented once, twice in successive Novel presentations, or three times in successive Novel presentations. The interval between two presentations of the identical Novels was 3–4 s. Within a session the sequence types were presented two times, in different random order for each participant. In each sequence there were different Novels. No target stimulus appeared after a visual stimulus, and vice versa. Measured sequences were preceded by a practice sequence of 6 min. This sequence was identical to the measured sequences with one repetition of the Novel. Participants were instructed to respond with button press (right hand) to the appearance of the target tone (“as fast as possible, but without error”), and count silently the appearance of letter B. (They reported the result of the count at the end of the sequence). 2.3. EEG recording and data analysis EEG was recorded (0.5–70 Hz, 30 Hz upper cut offline filtering; 250 Hz sampling rate, NeuroScan NuAmps amplifier), using an electrode cap (Easy Cap). Ag/AgCl electrodes were placed on Fp1, Fp2, Fpz, F3, Fz, F4, Pz, T3, T4, T5, T6, OL
(2 cm from O1), O1, Oz, O2, OR (2 cm from O2) locations. The reference electrodes were on the nose tip, the ground was on the forehead. Electrode impedance was below 5 Ω. Bipolar recordings monitored eye movement between electrodes above and below the right eye, and electrodes near the outer canthi of the two eyes. Epochs were created from − 100 to 800 ms post-stimulus. Epochs containing amplitude changes larger that 70 μV on any EEG or EOG channels (except from the occipital ones) were rejected from further analysis. Genuine occipital responses have frequently larger amplitude, therefore the limit on the occipital locations was 100 μV. ERPs were averaged separately for Standard, Target, Novel plus Standard and Letter plus Standard stimuli. Even in case of the least number of individual ERPs (three repetition of the same novel) at least 16 responses were averaged. Due to the long-lasting effects, ERPs to Standard stimuli following an auditory target or visual stimuli were omitted from averaging. In this study we concentrated on the novelty-related ERP components, therefore age-related effects on the ‘endogenous’ (P1 and N1) and target-related (P3b) components will be summarized only briefly. In order to disclose the novelty effects, the ERPs to the Standard stimuli were subtracted from ERPs elicited by the Novel plus Standard compound. Components of event-related activity were identified from the group average difference potentials. Amplitudes were measured as mean values around the peak values of the group average, and individual participants' mean amplitude values were scored using these windows. The ranges of the windows were ± 12 ms for the N2b (at Fz location) and late positive components (at Oz location for the P3novel/early and at Cz for the other late positive components). Unless otherwise stated, ERP data were analyzed in mixed factor ANOVAs with factors of age-group as between group factor, and electrode location [Fpz, Fz, Cz, Pz (midline locations) or O1, Oz, O2 (posterior locations)] as within group factor. ERP components to visual stimuli were analyzed in difference potentials, i.e. ERPs to Standard were subtracted from the ERPs to visual–auditory compounds and from the auditory Target. When appropriate, the Greenhouse–Geisser
Fig. 1. Timing and stimulus probabilities of the experimental design.
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Fig. 2. Group average ERPs to Auditory target, Standard,l, Visual target plus Standard event-related potentials (ERPs) and the (Visual Target plus Standard) minus Standard difference potential (n = 10 in both groups).
correction (ε) was applied and the corrected p values are reported. 3. Results 3.1. Behavioral results There was no performance difference between the two agegroups. Although reaction time to the auditory Target was
shorter in the younger group [534 ms (S.E. = 27.3) vs. 571 ms (S.E.M = 28.3), respectively), the difference was not significant [t(18) < 1]. Omission rates were 8.7% (S.E.M. = 3.3) and 7.5% (S.E. = 3.5) in the younger and older group, respectively [t(18) < 1]. Counting of letter changes was scored as the absolute value of difference from the actual number of changes. Results of the younger and older participants were 6.6 (S.E.M. = 1.9) and 2.2 (S.E. = 1.3), respectively. This difference was not significant [t (18) = 1.15].
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Fig. 3. Group average ERPs to the Novel plus Standard stimuli in the old and young participants (n = 10 in both groups). +: P3anovel/early; ⁎: P3anovel/late.
3.2. ERP 3.2.1. Exogenous components and target-related activity Fig. 2 shows the ERPs to the Standard and Target stimuli in the midline locations in the two age-groups.2 Concerning the main age-related differences, the auditory N1 component had longer latency in the elderly. While in the younger group this component had larger amplitude to the Auditory target than to the Standard, in the older group the Standard elicited larger N1. The auditory P2 latency increased in the older participants. N1 to the Visual target was larger in the younger group, whereas P2 had larger amplitude in the elderly. In case of the Auditory target both the N2b and P3b latencies were shorter in the younger group, but the group-related N2b latency difference decreased at Fpz. N2b and P3b had larger amplitude in the younger group. However, while in the younger group the P3b increased from Fz to Cz, the reverse effect appeared in the older group. As Fig. 2 shows, Visual target (letter change) elicited P3b component with longer latency in the elderly. This component had a parietal maximum in the younger group, and more anterior distribution in the elderly.
2 Detailed results and statistics on the endogenous and target-related components are available from the corresponding author.
3.2.2. Novel ERPs Figs. 3 and 4 shows the ERPs to the Novel plus Standard compound and the Novel plus Standard compound minus Standard difference potentials, respectively. Novel stimuli elicited different ERPs in the two age-groups. Comparison of the ERPs to the Novel plus Standard compound and the difference potentials shows that N1 component over the anterior location was an auditory effect (see also the auditory ERPs in Fig. 2).3 N2b component (∼ 300 ms latency) emerged only in the older group. Over the posterior (occipital) locations, and later in the anterior locations two positivities were recorded. Both components had shorter latency in the younger group. Hereafter we refer to the earlier positivity as P3novel/early and to the later positivity as P3novel/late. In the younger group the late positivity was followed by a long-lasting late negative wave. The scalp distribution of the two positivities is shown in Fig. 5. According to an ANOVA with factors of age as between group factor and electrode location (O1, Oz and O2) as within group factor, the P3novel/early latency was longer in the elderly [F 3 We conducted LORETA analysis (Pascual-Marqui et al., 1994) on peaks of the novelty-related components. In both age-groups LORETA analysis located P3novel/early in broad areas of temporal cortex and in the fusiform gyrus. A broad neural network was indicated for the P3novel/late component. In both groups there was activity in the anterior cingular cortex, posterior (Br 18) and parietal (Br 31). In the younger group broader temporal areas were involved in P3novel/late than in the older group. However, it should be noted that due to low density of the electrode array, one has to be cautious in interpreting the LORETA results.
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Fig. 4. Group average Novel plus Standard minus Standard difference potentials in the old and young participants (n = 10 in both groups).
(1,18) = 16.55, p < 0.001]. The amplitude difference was also significant [F(1,18) = 7.50, p < 0.05]. Fig. 6 shows the ERPs to the picture repetitions, while Table 1 shows the latency and amplitude values of the P3novel/early for these repeated stimuli. Repetition effects on P3novel/early amplitude were calculated in two ANOVAs with age as between group factor, and repetition an electrode location as within group factors. We compared the P3novel/early amplitudes for the first, second and third presentation from the three-presentation sequence, and the effect of the first and second presentation from the two-presentation sequence. In the three presentation sequence the main effect of age on P3novel/early was significant [F(1,18) = 4.39, p < .05]. More important, the main effect of repetition and the group × repetition interaction were also significant [F(2, 36) = 4.59, ε = 0.76, p < 0.05 and F(2,36) = 4.00, ε = 0.76, p < 0.05, respectively]. The group × repetition interaction was due to the considerable amplitude decrease in the young group, and the smaller change of the amplitude in the older participants. Similar results appeared in the two-presentation sequence. In this case the group main effect [F(1,18) = 8.74, p < 0.01], the repetition main effect [F(1,18) = 7.94, p < 0.05], and the group × repetition interaction [F(1,18) = 5.78, p < 0.05] were all significant. In separate ANOVAs for the two agegroups the order effects were significant only in the younger participants [F(2,18) = 5.38, ε = 070, p < 0.05 and F(1,9) = 9.67, p < 0.05 in the three-presentation and two-presentation sequences, respectively]. Comparison of amplitudes in the
first presentations of the three, two and single presentation sequences, and the comparison of amplitudes of the second presentations in the three and second presentation sequences did not reveal any significant difference. P3novel/late had longer latency, and it was smaller in the older group. Accordingly, in ANOVAs with factors of age as between group factor and electrode location (Fpz, Fz, Cz, Pz) as within group factor, the main effects of group on the latency and on the amplitude were significant [F(1,18) = 12.58, p < 0.01 and F (1,18) = 5.32, p < 0.05, respectively]. Table 2 shows the amplitude and latency values of the P3novel/late component. In the young group the late positivity was followed by a negative shift. In the 500–600 ms latency range we obtained significant group main effect [F(1,18) = 6.92, p < 0.05], location main effect [F(3,54) = 20.50, ε = 0.45, p < 0.001], and group × location interaction [F(3,54) = 5.29, ε = 0.46, p < 0.05]. The interaction was due to the increase of the negativity from Fpz to Pz. 4. Discussion In the present study novel visual stimuli elicited late positive components with longer latency and smaller amplitude in the older participants. As a new findings of our study, meaningful irrelevant pictures elicited an earlier and a later positive component (P3novel/early and P3novel/late, respectively), and P3novel/early was sensitive to the stimulus content in the younger participants, i.e. repeating the same picture this component
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Fig. 5. Scalp distribution of the Novel minus Standard difference potential in the P3novel/early and the P3novel/late latency ranges in the old and young participants (n = 10 in both groups).
became smaller. One may argue that this amplitude change is due the repeated stimulation of the same structures of lower vision. According to this view the amplitude change is attributed to the habituation of the exogenous P2 component. The latency of the occipital positivity was longer than that of the usual P2 latency. Furthermore, the 3–4 s interval between the two presentations, together with the bright inter-stimulus field and the presence of a high-contrast pattern (the letter) on the field may favor a ‘cognitive’ interpretation. The component we labeled as P3novel/early has a parallel in the auditory modality (Escera et al., 2001, 1998) and also in some intra-cranial recordings (even in posterior visual structures, Halgren et al., 1995). The age-related repetition effects on the posterior positivity (P3novel/early) are similar to findings in the auditory modality, i.e. fast P3a habituation in the younger group and hardly any habituation in the elderly (Friedman et al., 1998). Similar age-related differences were also observed in the electrodermal activity (McDowd and Filion, 1992). Diminished habituation is considered as a sign of compromised inhibitory activity (see Hasher and Zacks, 1988 for a general theory on age-related inhibitory loss). Following a suggestion by Baudena et al. (1995) and Yago et al. (2003), an anterior–posterior feedback loop, activated by the presence of the to-be-processed stimuli is less susceptible to inhibitory processes in the elderly. P3novel/late latency increased and P3novel/late amplitude decreased in the older group. This result corresponds to the age-related latency change of the P3a in the three-stimulus
oddball paradigm (Fjell and Walhovd, 2004; Tachibana et al., 1992). In the younger group P3novel/late had a more posterior distribution than the distribution of this component in the older group. Our results in the younger group were similar to those reported by Comerchero and Polich (1998), Polich (2003). These authors reported similar late positivities to variable novel visual stimuli and to a repeated salient irrelevant visual stimulus. As Polich (2003) pointed out, P3novel (and P3a) distribution is dependent on the context of the irrelevant stimuli (i.e. the stimuli of the ongoing task). In case of easy discrimination, together with highly discrepant infrequent non-target stimuli, late positivity had a posterior maximum (Katayama and Polich, 1998). Indeed, in our experiment the auditory task was relatively easy, and the infrequent non-target was highly different from the task-stimuli (it was in another modality). Accordingly, the context-related interpretation of the P3novel fits to the results of paradigm using both auditory and visual events. The age-related distribution difference of P3novel/late in the present study was similar to that of the P3b component. “Anteriorization” of the late positivities is considered to be the consequence of morphological and functional changes in the frontal cortex (see West, 1996 for a review). However, predictions stemming from the supposed compromised frontal activity are equivocal. Enlarged frontal positivity can be explained as a consequence of compensatory activity, e.g. the recruitment of larger cortical areas. As a more
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Fig. 6. Repetition effects on the average Novel minus Standard difference potentials in the young and old participants (n = 10 in both groups) from sequences with three repetitions. Group average Novel plus Standard minus Standard difference potentials from the sequences with three repetitions of identical novel stimuli.
sophisticated account age-related distribution difference is due to the longer orientation and categorization processes in the elderly (Friedman et al., 1998). While in younger participants the “task-irrelevant stimulus” category is quickly established, this process may be slower in the elderly. The different speed of categorization may be reflected by the different involvement of anterior and posterior structures in the age-groups. In the present study the age and novelty effects on the N2b component were different from the results of previous
experiments (Czigler and Balázs, 2005). When novel visual stimuli were mixed to the trials of a letter-matching task, these stimuli elicited a large anterior negativity in the younger group, and only small P3a. Neither of these components emerged in the older group. On the contrary, in the present study novel visual stimuli elicited positivities in both groups, and the N2b-like activity was absent in the younger group. The absence of N2b in the young group can be attributed to the masking effect of the ascending limb of the P3novel/late. We have only a post hoc explanation for the discrepant results of the present study and
Table 1 Group average latency (ms) and amplitude (μV) values of the P3novel/early component to the first, second and third presentation in the younger and older participants Three presentations
Two presentations
Younger 1
Older
Younger
One presentation Older
Younger
Older
256 (8.4) 241 (11.1) 246 (10.4)
228 (4.4) 231 (8.1) 231 (9.4)
255 (9.5) 257 (9.0) 250 (11.3)
4.5 (1.4) 3.6 (1.6) 3.8 (1.7)
12.1 (1.2) 10.1 (1.3) 10.9 (1.5)
3.7 (1.4) 2.9 (1.5) 3.4 (1.8)
2
3
1
2
3
1
2
1
2
Latency O1 223 (2.8) Oz 222 (3.0) O2 221 (3.2)
230 (5.3) 230 (8.6) 231 (7.9)
231 (7.9) 234 (9.5) 231 (7.9)
259 (9.7) 259 (9.6) 253 (11.3)
251 (8.8) 250 (10.2) 247 (10.1)
256 (8.6) 248 (9.7) 255 (9.5)
223 (4.0) 221 (4.0) 222 (3.8)
240 (8.7) 237 (8.5) 237 (8.7)
251 (12.1) 248 (11.8) 248 (11.8)
Amplitude O1 13.1 (2.4) Oz 12.1 (2.4) O2 12.6 (2.6)
10.7 (2.1) 9.4 (1.9) 10.0 (2.2)
8.5 (1.1) 7.3 (1.3) 7.7 (1.3)
5.1 (1.4) 4.7 (1.4) 5.1 (1.7)
4.4 (1.0) 3.7 (1.1) 4.4 (1.2)
3.9 (1.3) 4.6 (1.7) 4.3 (1.7)
14.2 (1.7) 13.1 (1.5) 14.1 (2.0)
11.0 (2.1) 10.0 (2.0) 10.9 (2.2)
4.4 (1.5) 3.9 (2.6) 4.5 (1.9)
The values were calculated from the difference potentials (n = 10 in both groups; S.E. in parenthesis).
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Table 2 Group average latency (ms) and amplitude (μV) values of the P3novel/late components in the younger and older participants (n = 10 in both groups; S.E. in parenthesis) Latency
Fpz Fz Cz Pz
Amplitude
Younger
Older
Younger
Older
386 (10.6) 343 (12.5) 335 (6.8) 347 (10.3)
392 (15.2) 400 (16.6) 385 (15.4) 379 (17.6)
3.0 (0.3) 5.9 (0.9) 6.9 (1.3) 7.3 (1.8)
1.5 3.0 3.3 2.9
(0.4) (0.8) (0.8) (1.7)
that of the results reported by Czigler and Balázs (2005). This is because the antecedent conditions of the emergence of the P3a/ P3novel/late are unclear (Dien et al., 2004), and the situation is similar in case of the N2b component. On the one hand, in the matching task the stimuli to-be-compared were presented simultaneously, and the stimuli of the previous trials carried no information about the next trial. Therefore no specific memory representations of the task-related stimuli were required. On the other hand, the oddball task of the present study required the memory representation of the task-related stimuli. Even if the memory representation was simple (like in the majority of the oddball tasks) this memory representation had to be preserved during the processing of the novel stimuli. This is why the present task may be more sensitive to the disturbing effects of the novel stimuli than the matching task. This shift of attention and/or the demand for the inhibition of the consequences of the involuntary attentional shift may contribute to the emergence of the P3novel components. In this study we replicated some earlier age-related ERP results. Late positivity to the auditory and visual targets (P3b) delayed in the older participants (e.g. Anderer et al., 1998; Czigler et al., 1994; Iragui et al., 1993; Knott et al., 2003; Polich, 1996). P3b amplitude was smaller in the elderly. P3b distribution was different in the two age-groups, i.e. P3b difference was larger over the posterior locations (see Friedman et al., 1997 for a review). We also replicated the age-related delay and amplitude decrease of the N2b to the auditory target (e.g. Amenedo and Díaz, 1998). The obvious delay of the novelty-related and targetrelated components in the older can be attributed to a manifestation of the general age-related slowing of mental operations (e.g. Cerella, 1985; Salthouse, 1996). Acknowledgements This research was supported by NKFF5/0071/2002 and OTKA T47038 grants. We thank Drs. Júlia Weisz and István Winkler for their help and Gabriella Pálfy and Zsuzsa d'Albini for their technical assistance. References Alho, K., Winkler, I., Escera, C., Huotilainen, M., Virtanen, J., Jääskeläinen, I.P., Pekkonen, E., Ilmoinemi, R.J., 1998. Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings. Psychophysiology 35, 200–204.
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