Development of auditory selective attention: Event-related potential measures of channel selection...

Development of auditory selective attention:

Event-related potential measures of channel selection

and target detection

HILARY GOMES,a,b MARTIN DUFF,a,b JACK BARNHARDT,c SOPHIA BARRETT,a,b andWALTER RITTERd

aCognitive Neuroscience Program, City College of New York, New York, New York, USAbThe Graduate Center, City University of New York, New York, New York, USAcPsychology Department, Wesley College, Dover, Delaware, USAdNathan S. Kline Institute for Psychiatric Research, Orangeburg, New York, USA

Abstract

In this study, we examined developmental changes in auditory selective attention using both electrophysiological (Nd,

P3b) and behavioral measures while two groups of children (9- and 12-year-olds) and adults were engaged in a two-

channel selective attention task. Channel was determined by frequency (1000 or 2000 Hz). Targets in one condition

were shorter than the standards (duration target) and in the other were softer (intensity target). We found that the Nd

onset and peak latencies for the children were significantly longer than for the adults. Nd amplitude, however, did not

differ between the groups. Further, all groups evidenced P3b to attended targets but not to unattended deviants. Hits,

reaction times, and false alarms to unattended deviants continued to evidence improvements through adolescence.

Taken together, our data aremost consistent with amodel of developmental improvement in the speed and efficiency of

attention allocation.

Descriptors: Nd, Auditory selective attention, Development, ERP, P3b

Many situations require that we attend to a specific stimulus in an

environment that contains complex, competing signals. This

process of selecting stimuli from an ever changing, multisensory

environment is determined not only by the physical character-

istics of the stimuli themselves, but also by the individual inter-

ests, motives, and cognitive strategies of the person perceiving the

stimuli. Because attention is involved in the process of selection,

it plays an important role in learning and development (Gerken,

1994).

Developmental studies of selective attention using a variety of

behavioral paradigms have found that older children perform

better than younger children (for reviews, see Cooly & Morris,

1990; Dempster, 1995; Gomes,Molholm, Christodoulou, Ritter,

& Cowan, 2000; Lane & Pearson, 1982; Plude, Enns & Brodeur,

1994; Ridderinkhof & van der Stelt, 2000). Investigators, how-

ever, disagree about which aspect of the selective attention pro-

cess is responsible for the developmental differences.

Explanations have ranged from interpreting younger children’s

poorer performance as reflecting difficulties differentiating and

blocking out irrelevant stimuli to suggesting that both younger

and older children process the irrelevant stimuli but that older

children are better able to separate the channels in memory and

to selectively report only the target stimuli (Doyle, 1973; Lane &

Pearson, 1982; Maccoby, 1969). Further, some investigators

have argued that the developmental improvement seen on selec-

tive attention tasks is secondary to changes in perception, short-

termmemory, sustained attention, understanding task demands,

and executive control of attention resources (Dempster, 1981;

Geffen & Sexton, 1978; Gibson & Rader, 1979; Guttentag &

Ornstein, 1990; Halperin, McKay, Matier, & Sharma, 1994;

Jensen & Neff, 1993; Kail, 1990; Sexton & Geffen, 1979).

Recent models of attention in typically developing and at-

tentionally challenged children have focused on speed and effi-

ciency of attention allocation (Ridderinkhof & van der Stelt,

2000) and the ability to inhibit processing of irrelevant stimuli

(Cooly & Morris; 1990; Dempster, 1995; Harnishfeger & Bjork-

lund, 1995), both of which are related to the executive control of

attentional processes and are probably mediated by the devel-

opment of the frontal lobe (Dempster, 1995; Foster, Eskes, &

Stuss, 1994; Posner & Rothbart, 2000). Neuroanatomical mea-

sures of frontal lobe development, specifically myelinization and

synaptic density counts, show long developmental courses that

do not appear to be complete until late adolescence (Huttenl-

ocher & Dabholkar, 1997; Sowell, Thompson, Tessner, & Toga,

2001). Further, although different aspects of attention appear to

have differential developmental time courses (McKay, Halperin,

This research was supported by a grant to the first author from the

NIDCD (DC 04992).Address reprint requests to: Hilary Gomes, Psychology Department,

NAC7/120, City College ofNewYork, 137th andConvent Avenue, NewYork, NY 10031, USA. E-mail: [email protected]

Psychophysiology, 44 (2007), 711–727. Blackwell Publishing Inc. Printed in the USA.Copyright r 2007 Society for Psychophysiological ResearchDOI: 10.1111/j.1469-8986.2007.00555.x

711

Schwartz, & Sharma, 1994), studies have found that some as-

pects of attentional control continue to improve into at least early

adolescence (Klenberg, Korkman, & Lahti-Nuuttila, 2001;

McKay et al., 1994; Rebok et al., 1997; van der Stelt, Kok,

Smulders, Snel, & Gunning, 1998; Wetzel, Widmann, Berti, &

Schroger, 2006).

In our study, we further examined the question of develop-

mental change by measuring electrophysiological components of

the auditory event-related potential (ERP) while children and

adults were engaged in an auditory selective attention task. ERPs

offer a unique, underutilized method for expanding our knowl-

edge about these developmental changes by providing informa-

tion about the temporal and spatial dynamics of brain activity

during task performance. In ERP auditory selective attention

tasks, participants are generally required to attend to stimuli in

one of two concurrently presented channels and to respond to

infrequent target stimuli in that channel. In many of these tasks,

an oddball or deviant stimulus is also occasionally presented in

the unattended channel. These tasks allow for the electrophys-

iological correlates of attentional selection to be examined in

three ways: between-channel selection processes can be examined

by comparing the responses to attended and unattended stimuli,

target detection processes can be examined by comparing the

responses to the targets and nontargets in the attended channel,1

and the effectiveness of channel selection can be assessed by de-

termining whether manifestations of target processing are ob-

served exclusively for stimuli in the attended channel or also for

infrequent deviants in the unattended channel (Ridderinkhof &

van der Stelt, 2000).

In the auditorymodality, between-channel selection processes

are reflected in processing negativity (PN) and negative differ-

ence (Nd) waves. The PN component, Naatanen (1992;

Naatanen, Alho, & Schroger, 2001) argues, reflects a compar-

ison process between the presented stimulus and an attentional

trace of the relevant stimulus. The attentional trace is an actively

formed and maintained neural representation of the physical

features that define the channel. Because all stimuli are compared

to the attentional trace, both the attended and unattended stimuli

elicit a PN. However, the PN associated with the irrelevant, un-

attended stimulus is smaller than the PN associated with the

relevant, attended stimulus, as the mismatch between it and

the attentional trace is detected early and processing is stopped.

The offset latency of the PN elicited by the irrelevant stimulus is

earlier when the difference between stimulus features identifying

the attended and unattended channels is large and later when the

difference is small (Alho, Tottola, Reinikainen, Sams, &

Naatanen, 1987).

Nd is the electrically negative difference that results from

subtracting the ERP waveform elicited by the standards when

they are unattended from those elicited by the same standards

when they are attended during selective attention tasks (for a

review, see Hillyard & Hansen, 1986; Hillyard, Mangun, Wold-

orff, & Luck, 1995; Naatanen, 1992; Naatanen et al., 2001). In

contrast to Naatanen, Hillyard and colleagues (e.g., Hillyard et

al., 1995) have argued that at least part of the early Nd reflects

the attention-related enhancement of the perceptual processing

of the stimulus (often referred to as gain theory).

Both views, nevertheless, agree that Nd provides information

regarding the time course of differential processing of attended

and unattended stimuli. It has been suggested that Nd onset

latency is related to the duration of processing required to de-

termine the channel to which a given stimulus belongs, because

onset latency increases as the physical separation between the

channels is decreased. Further, Nd amplitude has been found to

be larger when the difference between stimulus features identi-

fying the channels is larger because the PN elicited by the un-

attended stimulus under these conditions offsets earlier. Nd

amplitude is also thought to reflect the allocation of processing

resources, in part because the amplitude of the PN elicited in

divided attention tasks is between those elicited by the attended

and unattended stimuli in selective attention tasks (Hillyard &

Hansen, 1986; Parasuraman, 1980). Finally, Nd amplitude has

been found to be positively correlated with target detection ac-

curacy (Hillyard & Hansen, 1986; Parasuraman, 1980). Nd is

generally considered to consist of two parts, early and late Nd.

The early Nd is largest at the frontocentral scalp and is probably

generated in the auditory cortex (Kasai et al., 1999; Petkov et al.,

2004; although see Dien, Tucker, Potts, &Hartry-Speiser, 1997).

It reaches its maximum between 80 and 220 ms. The late Nd

usually peaks between 300 and 500 ms. It generally has a more

frontal scalp distribution than the early Nd (Kasai et al., 1999;

Petkov et al., 2004).

Although Nd has been studied extensively in adults (for re-

views, see Hillyard & Hansen, 1986; Naatanen, 1992), relatively

few studies have explored the ERP correlates of selective audi-

tory attention in children, and many of these have focused on

clinical populations (Bartgis, Lilly, & Thomas, 2003; Berman &

Friedman, 1995; Coch, Sanders, &Neville, 2005; Jonkman et al.,

1997; Loiselle, Stamm, Maitinsky, & Whipple, 1980; Maatta,

Paakkonen, Saavalainen, & Partanen, 2005; Rothenberger et al.,

2000; Satterfield, Schell, Nicholas, Satterfield, & Freese, 1990;

Schreiber, Stolz-Born, Kornhuber, & Born, 1992; also see

Brooker, 1980, as reported in Donald, 1983). Berman and

Friedman (1995), in a study with 8-, 14-, and 24-year-old typ-

ically developing participants, demonstrated an age-related in-

crease in the amplitude of early and late Nd that was primarily

attributable to amplitude changes in the waveform elicited by the

unattended stimuli. Further, they found an age-related decrease

in the onset and peak latencies of the early Nd. Satterfield et al.

(1990), in a longitudinal cross-modal selective attention study,

found that significant early Nds were not elicited from the par-

ticipants when they were 6 years old. However, the same children

evidenced Nds when they were 8 (see Bartgis et al., 2003, for a

similar finding in a cross-sectional study). Coch et al. (2005;

also see Sanders, Stevens, Coch, & Neville, 2006), using a very

children-friendly protocol with probe stimuli embedded in

attended and unattended narratives, elicited attention effects to

the probe stimuli from all participants; however, the children

(aged 6–8 years) evidenced a positive attention effect, in

contrast to the adults, who evidenced the more typical pattern

of increased negativity to stimuli in the attended channel. Taken

together, these studies suggest that reliable Nds with adultlike

polarity can be elicited from children approximately 8 or 9 years

of age. Also, there appears to be an age-related increase in Nd

amplitude and decrease in Nd onset and peak latencies. Finally,

much of the developmental change in the Nd appears to be at-

tributable to the unattended waveforms, suggesting that younger

children may be processing the unattended stimuli differently

from older children.

712 H. Gomes et al.

1Comparisons of ERPs elicited by target and standard stimuli usuallyinclude activity related to the physical differences between the stimuli andmotor responses to the targets, as well as target detection processes.

In this study, we wanted to explore the ERP correlates of

continued development in the processes underlying auditory se-

lective attention in preadolescent and adolescent children. Spe-

cifically we were interested in the effect of task or context on the

speed and efficiency of attention allocation in children between

the ages of 9 and 12. Behavioral studies in children have sug-

gested that the ability to discriminate some types of stimulus

features develops earlier than others. Specifically, the ability to

discriminate based on intensity reaches mature levels before dis-

crimination based on frequency and duration (Jensen & Neff,

1993). Further, pilot data collected in our laboratory from clin-

ically referred 10–12-year-old children showed that Nds were

elicited from the channel containing an intensity target but not

from the channel containing a duration target (Duff, Barnhardt,

& Gomes, 2004). Based on this previous work, we hypothesized

that the nature of the target would have an impact on the Nd in

normal children, despite the fact that the Nd of interest is the

differential processing of the attended and unattended standards

and does not directly reflect processing of the target. In one

condition, the participants listened for tones that were shorter

than the standards (duration target) and in the other for tones

that were softer (intensity target). The degree of separation be-

tween the target and the standards was individually determined

during a pretest to control for task difficulty. We expected the

amplitude of the Nd would be smaller and the latency would be

later in the channel with the duration target than in the channel

with the intensity target. Further, we expected the differences

associated with target type would be greatest for the 9-year-olds

and would get smaller with age.

In addition to examining the Nds, a measure of between-

channel processing, we also quantified the electrophysiological

target detection process in both the attended and unattended

channels, as reflected in the P3b. P3b has been extensively studied

in both adults and children (Johnson, 1989; Naatanen, 1992). It

is a large, positive-going, later potential that is largest at the

midline parietal sites. P3b is elicited by rare, randomly presented

stimuli that the subject is actively trying to discriminate. Peak

latency of the P3b varies between approximately 275 and 600 ms

after stimulus onset in adults. P3b peak latency and amplitude

have been found to be sensitive to a variety of task and stimulus

parameters, including manipulations affecting stimulus discrim-

ination (Reinvang, 1998). Developmental studies of the P3b have

found that peak latency decreases with age but that the mor-

phology of the component does not seem to change (Friedman,

1991; Johnson, 1989). We expected P3b would be elicited by the

attended targets from participants in all three age groups. Fur-

ther we expected P3b to be elicited by the unattended deviants in

some of the children but for this tendency to decrease with age as

the children became better at focusing their attention on the rel-

evant channel. A developmental increase in the attention effect

on the P3b in typically developing children was found by Sat-

terfield et al. (1990) in their study exploring intermodal selective

attention (also see Bartgis et al., 2003).

Method

Participants

Participants were 16 adults (10 women) and 32 children (19

girls). The adults ranged from 20 to 42 years of age (M5 29.2,

SD5 8.0 years). Self-reported ethnicity for the adults was as

follows: 5 Hispanic, 2 African American, 7 Caucasian, and 2

Asian. The children ranged from 9 to 13 years of age and were in

the age-appropriate grade in school. Most children were recruit-

ed from a junior high school for advanced studies in math, sci-

ence, and technology in New York City. Self-reported ethnicity

for the children was as follows: 21 Hispanic, 2 African American,

8 Caucasian, and 1 Asian. They were divided into two groups:

9- to 10-year-olds (16 participants; 11 girls; M5 9.7, SD5

4.4 m) and 12- to 13-year-olds (16 participants; 8 girls;M5 12.6,

SD5 8.0 m). Six of the children and 1 of the adults were left-

handed. All participants had normal hearing according to self- or

parent report. The children were paid a total of $50 and the

adults $10 per hour for participating in the study. Some of the

adults had participated in other ERP experiments in our labo-

ratory. Prior to testing, all children signed assent forms that were

read and explained to them in the presence of their guardian. All

guardians and adult participants signed consent forms.

Stimuli

The stimuli were 1000-Hz (low channel) and 2000-Hz (high

channel) tones presented binaurally through insert earphones.

The standard and intensity target tones were of 100ms duration

(including 10-ms rise and fall times). The target duration tones

ranged between 25 and 85 ms (10-ms rise and fall). The standard

and duration target tones were delivered at 82 dB SPL and be-

tween 67 and 79 dB for intensity target tones. The target stimuli

deviated from the standards by an amount that was adjusted

individually according to the detection performance of the par-

ticipants during a same–different test that preceded the actual

experiment.

Target type was counterbalanced over the high and low chan-

nels such that, for half of the subjects, the duration target oc-

curred in the high channel (2000 Hz) and the intensity target in

the low channel (1000 Hz) and for the other half of the subjects

the pairing was reversed. Stimulus order was pseudorandomized

with the high and low standards each occurring 40% of the time

and each of the targets occurring 10% of the time with the re-

strictions that no duration or intensity targets were presented

sequentially, that there were no more than two duration or in-

tensity targets within any sequence of 10 stimuli, and that there

were no more then three of the same standards in a row. All

stimuli were presented in the same run with a 1-s stimulus onset

asynchrony (SOA).

ProcedurePretest. A pretest session preceded the application of the

EEG cap and test session. A forced choice, paired same/different

pretest was used to determine the value of the intensity and du-

ration targets for each participant individually. Targets with five

levels of difference from the standard were presented for each of

the target types. For the intensity targets, possible decibel values

were 79, 76, 73, 70, and 67. For the duration targets possible

millisecond values were 85, 70, 55, 40, and 25. The value was set

one level below where participants were at least 80% accurate.

This was done because pilot testing suggested that the pretest was

significantly easier than the actual task. Table 1 presents the

number of participants in each age group receiving each level of

target for both the intensity and duration conditions.

Test. Two counterbalanced conditions were presented to the

participants: attend high frequency channel and attend low

frequency channel. Participants were asked to respond to

infrequent, target tones within the attended channel via button

Development of auditory selective attention 713

press while ignoring tones from the other frequency channel. In

addition, the participants were asked to avoid excessive blinking

and headmovements during the EEG recording sessions. Stimuli

were presented in runs of approximately 5 min, 300 stimuli per

run. There were four attend high frequency tone blocks and four

attend low frequency tone blocks.

An adult sat with each child during the experiment tomonitor

attention and minimize movement artifact. Short and long

breaks were given. During short breaks between each block (2–3

min), participants remained in their chair but were allowed to

stretch and shift positions. During one longer break (10–20 min)

halfway through the session, participants were disconnected

from the recording apparatus and allowed to walk around. Total

experiment timewas approximately 3 h, including approximately

30 min of electrode application, 2 h of testing with breaks, and 30

min of electrode removal and debriefing.

The protocol for the study was reviewed and approved by the

Internal Review Board at the City College of New York before

any subjects were tested.

Electrode Placement and Recording Techniques

The EEG was recorded from 32 Ag/AgCl electrodes mounted in

a Neuroscan, Compumedics Inc., elastic cap with the amplifier

bandpass set to 0.5–70Hz (� 6 dB points) and a sampling rate of

500 Hz. The scalp sites recorded were frontal/central: Fp1, Fp2,

Fz, F3, F4, F7, F8, FCz, FC3, FC4; frontal/temporal/central:

FT7, FT8, T3, T4, T5, T6, Cz, C3, C4; central/parietal: CPz,

CP3, CP4; temporal/parietal/occipital: Tp7, Tp8, Pz, P3, P4, Oz,

O1, O2; and left (A1) and right (A2) mastoid electrodes. The

vertical electrooculogram (VEOG) was recorded from electrodes

placed above and below the left eye. The horizontal electrooculo-

gram (HEOG) was recorded via electrodes attached to the outer

canthi of each eye. All of these sites were referenced to an elec-

trode placed on the tip of the nose. Impedances at the beginning

of the experimentwere generally below 5 kO and always below 10

kO. They were reexamined after the long, 10–20min break, and

any electrodes found to have higher impedances than at the be-

ginning of the test session were reapplied. The continuous EEG

for all channels was monitored during the recordings so that

problems with electrodes could be identified and corrected and

feedback about excessive motor movement could be given.

The total recording epoch was 1100 ms, including a prestim-

ulus interval of 100 ms. Each epoch was baseline corrected across

the entire sweep before artifact rejecting and averaging. The av-

erages from each block were baseline corrected again using the

average amplitude of the prestimulus portion of the epoch. Ar-

tifact reject levels were set at � 100 mV for all electrodes to

exclude blinks and movement artifacts. Individual block aver-

ages were visually examined for residual artifact.

Data Analysis

Electrophysiological data. Averages for each participant for

the two target type conditions were constructed for the standards

when theywere in the attended channel andwhen theywere in the

unattended channel and the attended targets and the unattended

deviants. Grand mean averages for each age group and target

type were obtained for purposes of display and examination of

ERP topographic distribution.

To select latency windows for amplitude measurements of the

Nd, Nd peak latencies for the grand means were identified in

difference waveforms obtained by subtracting the ERPs elicited

by the standards when they were unattended from the ERPs

elicited by the same standards when they were attended at FCz.

Grandmean peak latencies were as follows: intensity at 240, 290,

310 ms and duration of 244, 250, 324 ms for the adults, 12-year-

olds, and 9-year-olds, respectively. The windows chosen for av-

erage amplitude measurements were the 50 ms surrounding the

peak latency (25 ms on each side of the peak) of the grand

average Nd.

Analysis of the amplitude data occurred in two stages. First,

analyses of the average amplitude of the ERPs elicited by the

attended and unattended standards in the region of the Nd were

undertaken to insure that the observed amplitude differences

between the attended and unattended waveforms were signifi-

cantly different from chance. This analysis was conducted sep-

arately for the duration and intensity target conditions. For each

target condition, a three-way ANOVA on mean amplitude with

factors of age (9-year-olds, 12-year-olds, and adults), condition

(attended, unattended), and electrode (Fz, FCz, Cz, FC3, FC4,

C3, C4) was conducted. Significantmain effects of attentionwere

explored using t tests. Once the presence of significant Nds was

demonstrated, the second stage of analysis was undertaken in

which a three-way ANOVA with factors of age (9-year-olds, 12-

year-olds, and adults), target type (duration, intensity), and

electrode (Fz, FCz, Cz, FC3, FC4, C3, C4) was conducted on the

amplitude of the Nds. Where indicated, appropriate post hoc

ANOVAs and t tests were done.

Onset and peak latencies of the Nd were determined for each

participant in both conditions. Raw and difference waveforms

were examined at FCz independently by three raters who were

experienced in examining Nd. Rating differences were discussed

until agreement was reached. Onset and peak latencies were

compared using a repeated measures MANOVA with factors of

age (9-year-olds, 12-year-olds, and adults) and target type (du-

ration, intensity). Where indicated, appropriate post hoc t tests

were done. Latencymeans for the appropriate condition replaced

missing data for the omnibus test but not for the post hoc t tests.

To further examine developmental changes in the allocation

of attention, the amplitude of P3bs elicited by target and unat-

tended deviant stimuli were examined. To select latency windows

for amplitude measurements, P3b peak latencies for the target

grand means were identified at Pz. Grand mean peak latencies

were as follows: intensity at 400, 405, 415 ms and duration of

445, 425, 425 ms for the adults, 12-year-olds, and 9-year-olds,

respectively. The windows chosen for average amplitude mea-

surements were the 200 ms surrounding the peak latency (100 ms

714 H. Gomes et al.

Table 1. Number of Participants in Each Group Receiving Each

Level of Target

Age group

9-year-olds 12-year-olds Adults

Intensity 79 dB 0 0 076 dB 0 0 1073 dB 9 16 670 dB 6 0 067 dB 1 0 0

Duration 85 ms 0 0 070 ms 0 0 655 ms 10 11 1040 ms 4 3 025 ms 2 2 0

on each side of the peak) of the grand average P3b. To determine

if significant P3bs were elicited, we compared the amplitude of

the target/deviant and standard waveforms in the measurement

window. This analysis was conducted separately for the attended

and unattended channels. Separate three-way repeated measures

AVOVA with factors of tone type (standard or target/deviant

tone), target/deviant type (duration or intensity target/deviant),

and age group were calculated for stimuli in the attended and

unattended channels. Significant main effects of attention were

explored using t tests.

Behavioral data. For the attended channel, reaction time

(RT) and accuracy measures (hits and false alarms; FA) were

recorded for each participant for each type of target. Three types

of FA were possible, FA to attended standards, FA to unat-

tended standards, and FA to unattended deviants. The response

window was 200–1200 ms following stimulus onset. This re-

sponse window slightly overlapped the presentation of the sub-

sequent stimulus. Average median RTs, number of correctly

detected targets, and total number of FA were compared across

age groups and target type using a repeatedmeasuresMANOVA.

Differences in the FA to the unattended target were also exam-

ined with a 3 (age group) � 2 (target type) ANOVA. Signi-

ficant effects in both analyses were explored with post hoc t tests.

The relationships between electrophysiological and behav-

ioral variables were explored using two-tailed partial correla-

tions, controlling for age. An alpha level of .05 was used for all

statistical tests. Geisser–Greenhouse corrections were used in

reporting p values when appropriate.

Results

Our primary focus in this study concerned the development of

between-channel selection processes as reflected in the Nd com-

ponent. TheNd and other ERP data are presented first, followed

by the behavioral data.

ERPs

Figures 1, 2, and 3 display the grandmean waveforms elicited by

the standard toneswhen they were in the attended (thick line) and

unattended channels (thin line) in the duration condition at se-

lected recording sites (FP1, FP2, Fz, FC3, FC4, FCz, C3, C4,

Cz, CP3, CP4, Pz) from participants in the adult, 12- and 9-year-

old groups, respectively. Figure 4 displays the grand mean wave-

forms elicited by the attended and unattended standards in the

intensity condition for all three age groups. It should be noted

that the standard tones are the same in these two conditions.

Condition is determined by the feature identifying the target, and

ERPs elicited by the targets are not contained in these averages.


FC3

C3 Cz C4

Pz

ms −100 150 400 650 900

0.0

1.5

3.0

−1.5

−3.0

Attended

Unattended

µV CP3 CP4

Fz

FCz

FP2

FC4

Duration: Adults

FP1

Figure 1. Grand mean ERPs elicited from the adults at selected electrode sites (FP1, FP2, Fz, FC3, FC4, FCz, C3, C4, Cz, CP3,

CP4, Pz) in the duration condition. The thick lines are the ERPs elicited by the standard tones when they were in the attended

channel and the thin lines are the ERPs elicited by the standard tones when they were in the unattended channel. In this and all

subsequent figures, stimuli were presented at time zero.

Developmental changes in themorphology of the wave forms are

clearly evident. ERPs elicited from each age group are charac-

terized by a P1 peaking at approximately 50–70ms, aN1 peaking

at about 105–110 ms, and a P2 peaking at about 175 ms. P1s are

larger and somewhat later in the children than in the adults, N1s

are somewhat smaller, and P2s are substantially smaller. How-

ever, themost notable developmental difference is the presence of

an additional negative-going wave followed by a positive-going

wave in the children. These components are larger than the N1

and P2 in the 9-year-olds, similar/smaller in amplitude toN1 and

P2 in the 12-year-olds, and almost gone in the adults.

Nd amplitude analysis. Nd was identified as the separation

between the waveforms elicited by the attended and unattended

standards beginning on the downward slope of the P2 compo-

nent for the adults and somewhat later in the children (see Fig-

ures 1–4). Figures 5 and 6 depict the Nds for the duration and

intensity conditions, respectively. Clear Nds are seen for all three

age groups in both target conditions. Consistent with the liter-

ature, Nd was largest in the fronto-central region and peaks at

approximately 240 ms for the adults. Given its latency and mor-

phology, this component is thought to be an early Nd. No late

Nd appears to have been elicited by this paradigm, perhaps re-

flecting the absence of a location cue for channel (Meehan,

Singhal, & Fowler, 2005). Further, the early Nd (which we will

refer to here as Nd) is followed by a positive-going wave that

peaks at approximately 390 ms in the adults and is largest over

centrally located electrodes. This positivity may be similar to the

Pd190 described by Woldorff and Hillyard (1991).

The amplitude pattern across the age groups appears different

for the two target conditions, with adults evidencing a larger Nd

at FCz in the intensity condition than the 9-year-olds but a

comparable, if not smaller amplitude Nd at FCz than the 9-year-

olds in the duration condition.

To establish that the amplitude of the waveform elicited by the

standards when they were in the attended channel was signifi-

cantly different from the amplitude of the waveform elicited by

the standards when they were in the unattended channel in the

Nd latency window, 3 � 2 � 7 ANOVAswere conducted for the

intensity and the duration target conditions. Main effects of at-

tention were found in both analyses, intensity: F(1,45)5 24.49,

po.0005, Zp2 5 .35; duration: F(1,45)5 15.09, po.0005,

Zp2 5 .25, indicating that the amplitude of the ERP was larger

for the attended than for the unattended standards. Tables 2

(duration condition) and 3 (intensity condition) present the Nd

amplitudes for seven electrode sites across the three age groups.

Follow-up t tests demonstrated that the differencewas significant

at po.05 or lower for most electrode sites for the 12-year-olds

and the adults, but only at a couple of sites for the 9-year-olds

(see Tables 2 and 3). The high level of variability in the

716 H. Gomes et al.

FC3

C3

FCz FC4

FP1 Fz FP2

CP3 µV Pz CP4

Cz C4

Attended

Unattended

Duration: 12 Year olds

ms −100 150 400 650 900

0.0

1.5

3.0

−1.5

−3.0

Figure 2.Grandmean ERPs elicited from children in the 12-year-old group in the duration condition at selected electrode sites. The

thick and thin lines are as in Figure 1.

9-year-olds may be responsible for the lack of an attention effect

at some electrode sites. An examination of the tables reveals that

variability reduces with age.

The amplitude of the Nd was compared across condition,

electrode, and age using a 2 � 3 � 7 ANOVA.Amain effect was

found for electrode, F(6,270)5 4.60, po.0005, e5 .514,

Zp2 5 .09, but no other main effects or interactions were signifi-

cant. This was surprising, given the apparent amplitude differ-

ences seen in the figures. To further explore this finding, we

looked at the distribution of individual amplitudes. Table 4

presents the measures of the central tendency and variability of

the Nd elicited at FCz for each age group. The standard devi-

ations and ranges decrease substantially across the age groups,

again reflecting the reduction of amplitude variability with age.

Further, the mean amplitude values for the older groups gener-

ally fall between themaximumandminimumamplitude values of

the youngest group, suggesting that the apparent amplitude

differences in the figures between the age groups were attribut-

able to variability.

To examine the stability of Nd amplitude across conditions,

partial correlation controlling for age were calculated. Nd am-

plitudes at FCz were not significantly correlated across target

types, r(45)5 � .27, p5 .07. This lack of a relationship was

surprising, given that Nd amplitude was calculated as the differ-

ence between the waveforms elicited by the attended and unat-

tended standard stimuli, which are the same in both conditions,

and suggests that task demands may impact the processing of

both standard and target stimuli.

Nd latency analysis. Table 5 presents onset and peak latencies

for the Nd for each age group and target condition. An exam-

ination of Table 5, as well as Figures 5 and 6, suggests that theNd

onset and peak latencies decrease with age in both target con-

ditions. It should be noted, however, that more of the children’s

waveforms were deemed unscoreable for Nd onset and peak la-

tencies than the adult’s, either because there was no negative-

going wave in the time range of the Nd or the waveform was so

noisy that peak and onset latency values could not be deter-

mined. The number of participants in each group with quantifi-

able onset and peak latencies are also presented in Table 5. The

age differences in latency were confirmed using a MANOVA.

Significant multivariate effects were found for age,Wilks’ Lamb-

da: F(4,82)5 6.42, po.0005, Zp2 5 .24, and for the interaction of

age and target type, Wilks’ Lambda: F(4,82)5 2.96, po.05,

Zp2 5 .13.

Greenhouse–Geisser corrected univariate main effects for age

were found for both onset, F(2,42)5 12.62, po.0005, Zp2 5 .38,

and peak latency, F(2,42)5 13.65, po.0005, Zp2 5 .39, reflecting

the decrease in onset and peak latency of the Nd with age. Post

hoc t tests indicated that Nd latencies were longer for the


FP1 Fz FP2

FC3 FCz FC4

C3 Cz C4

CP3 CP4 µV

Pz

Attended

Unattended

Duration: 9 Year olds

ms −100 150 400 650 900

0.0

1.5

3.0

−1.5

−3.0

Figure 3. Grand mean ERPs elicited from the children in the 9-year-old group in the duration condition at selected electrode sites.

The thick and thin lines are as in Figure 1.

9-year-olds than for the adults for duration onset, t(24)5 2.69,

po.05, duration peak, t(24)5 4.29, po.0005, and intensity on-

set, t(25)5 2.59, po.05, and longer for the 12-year-olds than for

the adults for duration onset, t(20)5 3.66, po.005, duration

peak, t(20)5 4.61, po.0005, and intensity peak, t(25)5 3.09,

po.01. The two child groups did not differ on any of the latency

measures. Univariate interaction effects were only found for

peak latency, reflecting the smaller latency differences across the

age groups in the intensity condition than in the duration,

F(2,42)5 3.38, po.05, Zp2 5 .14.

To examine the stability of the latency measures and their

relationship to Nd amplitude, partial correlations controlling for

age were calculated. Onset and peak latencies were found to be

correlated for both target types, duration: r(32)5 .62, po.0005;

intensity r(35)5 .68, po.0005. Peak latencies were correlated

across the target conditions, r(25)5 .64, po.0005, but onset la-

tencies were not, r(25)5 .15, p5 .46, possibly suggesting that

peak latency is a more reliable measure. Peak latency was neg-

atively correlated with Nd amplitude at FCz for the duration

target condition, reflecting the fact that participants with shorter

Nd peak latencies evidenced larger amplitude Nd, even when

controlling for the effect of age, r(32)5 � .72, po.0005. The

relationship between peak latency and amplitude in the intensity

condition was not significant, r(35)5 � .18, p5 .30.

P3b analyses. The allocation of attention can also be assessed

by comparing the ERP correlates of target/deviant detection for

stimuli in the attended and unattended channels. Figure 7

presents the P3bs for the attended targets and the unattended

deviants. Large P3bs were elicited from participants in all three

age groups in both target conditions by the attended targets.

Possible P3bs were elicited by the unattended duration deviants

in the 9-year-old children, but not in the 12-year-old or adults

groups.

For the stimuli in the attended channel, the P3b effects were

confirmed with a 2 (standard/target tone) � 2 (duration/inten-

sity target) � 3 (age group) repeated measures AVOVA. There

was a highly significant main effect of tone, indicating that

the amplitude of the P3bwas larger to the target tones than to the

standard tones, F(1,45)5 118.98, po.0005, Zp2 5 .73. No other

main effects or interactionswere significant. TheANOVA for the

unattended stimuli found no main effect of tone (standard/de-

viant) but did find a significant interaction of tone with age and

target type, F(2,45)5 3.35, po.05, Zp2 5 .14. Follow-up t tests

718 H. Gomes et al.

µV

Fz

FCz

Cz

Pz

Fz

FCz

Cz

Pz

Fz

FCz

Cz

Pz

Attended

Unattended

Adults 12 Year olds 9 Year olds

Intensity

ms −100 150 400 650 900

0.0

1.5

3.0

−1.5

−3.0

Figure 4.Grandmean ERPs elicited from participants in the three age groups in the intensity condition at Fz, FCz, Cz, and Pz. The

thick and thin lines are as in Figure 1.

comparing the amplitude in the vicinity of the P3b for the deviant

and standard tones in the unattended channel found no signifi-

cant differences (see Table 6). A significant main effect of group

was also found in the omnibus ANOVA due to the larger am-

plitude waves elicited by both the standard and the deviant stim-

uli from the children than the adults, F(2,45)5 3.71, po.05,

Zp2 5 .14, as well as an interaction of group and target type, re-

flecting the larger waves elicited from the 9-year-olds in the du-

ration than in the intensity condition, F(2,45)5 3.31, po.05,

Zp2 5 .13.

Behavioral

The behavioral data from this task was examined to explore age-

related changes in the speed (RT) and accuracy (hits and overall

FA) of target detection and efficiency of channel selection (FA to

unattended deviants). To compare speed and accuracy across age

and target type, a MANOVA with the dependent variables of

number of hits, total number of false alarms, andmedian RTwas

performed (see Tables 7 and 8 for variable means and standard

deviations). Significant multivariate effects were found for age,

Wilks’ Lambda: F(6,86)5 2.82, po.05, Zp2 5 .16, target type,

Wilks’ Lambda: F(3,43)5 9.50, po.0005, Zp2 5 .40, and for the

interaction of age and target type, Wilks’ Lambda:

F(6,86)5 4.18, po.005, Zp2 5 .23.

Hits. Despite our attempts to match the groups for the diffi-

culty of the target discrimination, Greenhouse–Geisser corrected

univariate main effects of age and target type were found for hits.

The 9-year-old group performed worse than the other two

groups, main effect of age: F(2,45)5 7.70, po.005, Zp2 5 .26;


ms

µV

FP1 Fz FP2

FC3 FCz

FC4

C3 Cz C4

Adult

12 Yrs

9 Yrs

Duration

−100 150 400 650 900

0.0

0.5

1.5

1.0

−1.5

−1.0

−0.5

Figure 5. Grand mean difference waveforms (Nd) elicited from participants in all three age groups in the duration condition

obtained by subtracting the ERPs elicited by the standard tones when they were unattended from the ERPs elicited by the standard

tones when they were attended at selected electrode sites (FP1, FP2, Fz, FC3, FC4, FCz, C3, C4, Cz). The thick, thin, and dotted

lines are the waveforms elicited in the adult, 12-year-old, and 9-year-old groups, respectively.

duration compared to 12-year-olds: t(30)5 2.07, po.05; dura-

tion compared to adults: t(30)5 2.90, po.01; intensity com-

pared to 12-year-olds: t(30)5 2.09, po.05; intensity compared

to adults: t(30)5 3.95, po.0005. Duration targets were respond-

ed tomore accurately than intensity targets, main effect of target:

F(1,45)5 9.15, po.005, Zp2 5 .17. These findings suggest that

age, as well as target type, impact the accuracy of target detection

in selective attention tasks. Further, the younger children per-

formed more poorly than the older children and adults, despite

receiving targets that were further from the standard.

RT. Greenhouse–Geisser corrected univariate main and in-

teraction effects were found for RT. Although on average par-

ticipants evidenced faster RTs to duration than to intensity

targets, main effect of target: F(1,45)5 20.10, po.0005,

Zp2 5 .31, and adults responded faster than children, main effect

of age: F(2,45)5 5.02, po.05, Zp2 5 .18, the significant interac-

tion suggests that the pattern was different for each target type,

F(2,45)5 13.26, po.0005, Zp2 5 .37. Post hoc t tests indicated

that RTs did not differ between the age groups for the duration

targets, but that RTs to intensity targets were significantly longer

for the 9-year-old group than for the 12-year-old group,

t(30)5 3.23, po.005, or the adults, t(30)5 4.26, po.0005. Fur-

ther, RTs to duration and intensity targets were similar for the

adults but were longer to intensity than duration targets for both

the 12-year-old group, t(15)5 3.73, po.005, and the 9-year-old

group, t(15)5 5.21, po.0005. In summary, the speed of target

detection evidenced developmental improvement for an intensity

change but was stable for a duration change.

FA. Total FA did not evidence significant effects. However,

main and interaction effects were found for FA to unattended

720 H. Gomes et al.

µV

Fz FP2

FC3 FCz FC4

C3 Cz C4

Adult

12 Yrs

9 Yrs

Intensity

FP1

ms−100 150 400 650 900

0.0

0.5

1.5

1.0

−1.5

−1.0

−0.5

Figure 6.Grandmean differencewaveforms (Nd) elicited fromparticipants in all three age groups in the intensity conditionobtained

as in Figure 5 at selected electrode sites. The thick, thin, and dotted lines are as in Figure 5.

deviants in a separate two-way repeated measures ANOVA

across target type and age. On average, participants evidenced

more FA to unattended intensity than to duration deviants, main

effect of target: F(1,45)5 16.4, po.0005, Zp2 5 .27, and children

evidenced more than adults, main effect of age: F(2,45)5 7.95,

po.005, Zp2 5 .26; however, the significant interaction suggests

that the pattern was different for each target type, F(2,45)5

13.95, po.05, Zp2 5 .17. Post hoc t tests indicate that FA do not

differ as much between the age groups for the duration deviants

as they do for the intensity deviants. For the duration condition,

only the adult and 9-year-old groups differed in the number of

FA to the unattended deviants, t(30)5 2.19, po.05. For the

intensity condition, the adults produced fewer FA to the unat-

tended deviants than either the 12-year-old group, t(30)5 2.99,

po.01, and 9-year-old group, t(30)5 4.76, po.0005). Further,

FA to duration and intensity deviants were similar for the adults

but were more frequent to intensity than duration deviants for

both the 12-year-old group, t(15)5 2.55, po.05, and the 9-year-

old group, t(15)5 3.20, po.01. These data suggest that the chil-

dren were more likely to respond to a change in the unattended

channel than the adults, especially if the change was in intensity.

Although, in general the children performed more poorly

than the adults despite receiving targets that on average evi-

denced a greater physical difference from the standards, we

wanted to insure that the developmental changes in performance

described above were not due to target differences between the

age groups. The findings from multivariate and univariate

ANOVAs in which target level was entered as a covariate are

consistent with those discussed above. Further, the effect of the

covariate was not significant in any analysis.

The behavioral data strongly suggest that the ability to se-

lectively attend, as evidenced by the speed and accuracy of target

detection, as well as the efficiency of channel selection are con-

tinuing to develop through early adolescence. Further, the data

indicate that performance is impacted by task. Duration dis-

crimination evidenced less developmental change than intensity

discrimination, possibly suggesting that the task was easier de-

spite attempts to match target discriminability with the pretest.

Comparison of ERP and Behavioral Data

The relationships between the behavioral and electrophysiolog-

ical measures were examined using two-tailed partial correlations

controlling for the effects of age. Table 9 presents the correlations.

Nd amplitude at FCz was not correlated with any behavioral

measures. This was somewhat surprising, as research has sug-

gested a relationship between Nd amplitude and accuracy (Hill-

yard & Hansen, 1986). Further, no significant correlations were

found between the electrophysiological and behavioral measures

for the duration target condition. In the intensity target condition,

Nd peak latency was positively correlated with FA and negatively

correlated with hits due to longer peak latencies being associated

with poorer accuracy (fewer hits and increased FA). Also, in the

intensity target condition, P3b amplitude was correlated with hits

and negatively correlated with RT, replicating the relationship


Table 2. Mean Amplitudes in Microvolts of the Nds in Duration

Condition � Age and Electrode

Age group


Mean St. Dev. Mean St. Dev. Mean St. Dev.

Fz � 1.43n 2.25 � 1.37nn 1.77 � 1.22nnn 1.17FC3 � 1.03 2.77 � 1.16n 1.99 � 0.81n 1.43FCz � 1.69n 3.18 � 1.56nn 2.06 � 1.41nn 1.51FC4 � 1.16 2.55 � 1.33n 2.26 � 0.76n 1.33C3 � 0.87 3.22 � 1.08 2.12 � 1.05n 1.63Cz � 1.20 3.34 � 1.35n 2.19 � 1.22nn 1.55C4 � 0.87 2.80 � 1.26n 2.31 � 0.86n 1.37

npo.05, nnpo.01, nnnpo.001 when comparing the amplitude of the at-tended and unattended waveforms.

Table 4. Variability of Nd Amplitudes Measured at FCz in

Microvolts in the Duration and Intensity Condition � Age

Age group


Duration Mean � 1.69 � 1.62 � 1.47SD 3.18 2.14 1.57Minimum � 6.24 � 6.07 � 4.49Maximum 6.07 1.64 .50Range 12.31 7.71 4.99

Intensity Mean � 1.03 � 1.63 � 1.98SD 2.75 2.36 1.16Minimum � 9.64 � 6.12 � 4.45Maximum 1.76 2.77 .13Range 11.40 8.90 4.58

Table 3. Mean Amplitudes in Microvolts of the Nds in Intensity

Condition � Age and Electrode

Age Group



Fz � 0.70 2.22 � 1.39n 2.25 � 1.74nnn 1.07FC3 � 0.77n 1.43 � 1.56nn 1.97 � 1.07nn 1.17FCz � 1.03 2.75 � 1.63n 2.36 � 1.98nnn 1.16FC4 � 0.99 2.00 � 1.40n 2.28 � 1.30nnn 0.97C3 � 0.57 1.60 � 1.46n 2.02 � 1.06nn 1.27Cz � 0.78 2.64 � 1.57n 2.27 � 1.83nnn 1.26C4 � 1.02 2.13 � 1.48n 2.16 � 1.37nnn 1.16

npo.05, nnpo.01, nnnpo.001 when comparing the amplitude of the at-tended and unattended waveforms.

Table 5.Mean Latencies in Milliseconds of Nd Onset and Peak �Age and Condition

Age group

9-year-olds(durationn5 13,intensityn5 11)

12-year-olds(durationn5 9,

intensityn5 11)

Adults(durationn5 13,intensityn5 16)


Duration onsetA,B 212 58 224 47 163 31Intensity onsetA 221 63 203 46 168 43Duration peakA,B 298 56 295 43 223 30Intensity peakB 283 67 292 30 246 42

ANine-year-olds significantly different from adults at po.05.BTwelve-year-olds significantly different from adults at po.05.

between P3b amplitude and task difficulty reported in the liter-

ature (Muller-Gass & Campbell, 2002; Picton, 1992).

Discussion

This study examined the speed and efficiency of attention

allocation in children and adults during an auditory selective

attention task. Developmental changes in three aspects of

attention selection were assessed in this paradigm, between-

channel selection, target detection in the attended channel,

and the maintenance/strength of the attention directed toward

the identified channel (Ridderinkhof & van der Stelt, 2000). In

addition, the impact of target type on these processes was

explored.

Between-Channel Selection Processes

Between channel selection processes were assessed using Nd am-

plitude and latency measures. Contrary to our hypotheses, which

suggested that Nd amplitude would increase with age, no am-

plitude differences were found across the age groups. However,

there was an age-related decrease in the interindividual variabil-

ity in amplitude. We hypothesized an increase in Nd amplitude

with age, based primarily on the findings of Berman and Fried-

man (1995). They presented participants with two stimulus con-

ditions, one in which the attended and unattended channels were

differentiated by pitch (low and high) and the other in which they

were differentiated by phoneme (ba and da). Targets in both

conditions were stimuli that were longer in duration. There ap-

pear to be two primary differences between their tone condition

722 H. Gomes et al.

±3µV

1100 ms

Target/Deviant

Standard

Attended Channel Unattended Channel

Duration Intensity Duration Intensity

Adults

12 Year Olds

9 Year Olds

Figure 7. Grand mean ERPs (P3b) elicited by the attended targets and unattended deviants compared to the relevant standards in

both the duration and intensity conditions for all three age groups at Pz. The thick lines are the ERPs elicited by the target/deviant

tones and the thin lines are the ERPs elicited by the standard tones.

Table 6. P3b Amplitude (Target/Deviant minus Standard) at Pz in Microvolts in the Duration and Intensity Condition � Age (Standard

Deviations in Parentheses)

Age group


Duration Attended 3.44 (4.64)n 2.47 (2.07)nnn 2.99 (1.45)nnn

Unattended 0.84 (3.50) � 1.19 (2.45) 0.10 (1.33)Intensity Attended 2.68 (2.05)nnn 4.45 (2.72)nnn 3.43 (1.92)nnn

Unattended � 0.79 (4.08) 0.65 (2.55) � 0.05 (1.53)

npo.05, nnnpo.001 when comparing the amplitude of the target/deviant and standard waveforms.

and our study that could explain the divergent results. The am-

plitude of the Nds elicited in the Berman and Friedman study

were substantially bigger than ours, probably as a result of the

larger channel separation used in their study (Naatanen, 1992).

In both studies channel was defined by frequency, but they used

500Hz for their low frequency channel whereas we used 1000Hz.

The high frequency channel was 2000 Hz in both studies. We

choose not to use 500 Hz as this tone is in the frequency range of

the equipment noise in our laboratory and is difficult for some

people to hear at low intensities. Given our smaller Nds than

Berman and Friedman’s, it is possible that our inability to find a

significant age effect was due to our overall smaller amplitudes.

We consider this unlikely, as an examination of the distribution

of Nd amplitudes elicited in our study across participants in each

age group suggests a wide range of amplitudes, especially in the

children.

The second primary difference between the two studies that

could impact the Nd amplitude findings is that Berman and

Friedman (1995) measured amplitude in the same time windows

across age groups, despite latency differences in the Nd. Their

study found a significant effect of age only in the 230–300 ms

time window. Nd peaked in this time window in the adults but

not in the adolescents or in the children. When the average was

calculated for a window encompassing the peaks of all of the age

groups (approximately 230–450 ms), there was no effect of age.

Consequently, the age-related changes in Nd amplitude for tone

stimuli in the Berman study should be considered at best small.

However, the amplitude changes for their phoneme stimuli are

more convincing, suggesting that amplitude may evidence a de-

velopmental increase that is mediated by task but that tone pro-

cessing has begun to reach an asymptote by 8 or 9 years of

age. Consistent with this suggestion, van der Stelt et al. (1998)

also found an age-related increase in the visual analog of the Nd,

the selection negativity (SN), in participants between 7 and 24

years of age.

As Nd amplitude is thought to reflect the amount of attention

allocated to the task, our finding of similar amplitude Nds across

the age groups examined suggests that the average amount of

attention allocated to our taskwas comparable in the 9-year-olds

and the adults. However, it should be noted that this average

masks large interindividual differences in attention allocation

perhaps associated with individual differences in allocation effi-

ciency, motivation, executive control of attention, or task strat-

egies. Future research should explore the impact of these factors

on Nd amplitude.

Although no age differences were found in Nd amplitude, the

onset and peak latencies of the Nd reducedwith age. Further, the

latency measures were highly correlated within target type con-

dition, and peak latency was highly correlated across the two

conditions, suggesting that latency measures may be a more

reliable measure in samples of participants who evidence

waveforms that are scoreable for latency. Onset latency is

thought to reflect the duration of processing required to deter-

mine channel assignment, and peak latency may reflect the com-

pletion of postselection stimulus processing necessary for target

detection decisions. Latencies were significantly longer in the

children, suggesting that they were slower at determining channel

and processing stimuli. Berman and Friedman (1995) and van

der Stelt et al. (1998) have also demonstrated latency decreases

with age in ERP selective attention measures.

In our study, peak latency was negatively correlated with Nd

amplitude at FCz for the duration target condition, reflecting the

fact that participants with shorter Nd peak latencies evidenced

larger amplitude Nd, even when controlling for the effect of age.

This finding is consistent with previous adult literature, which

suggests that onset latency reflects the ease of channel assignment

and that larger amplitude Nds are found with wider channel

separations (Naatanen, 1992). However, the relationship be-

tween peak latency and amplitude in the intensity condition was

not significant.

In summary, these data support amodel of improved speed of

attention allocation with age (Ridderinkhof & van der Stelt,

2000). Children required more time to complete the between-

channel decision processing than adults but evidenced similar


Table 7. Behavioral Data for Each Age Group for Duration Targets

Age group



Percent hits 75.9 9.8 83.1n 10.0 89.2n 9.2Total false alarms (FA) 11.1 7.0 7.9 9.9 9.7 13.0FA to unattended deviants 2.3 2.6 1.6 2.1 0.7n 1.1Median RT (ms) 513 43 486 46 490 57

nSignificantly different from the 9-year-old group at po.05.

Table 8. Behavioral Data for Each Age Group for Intensity Targets

Age group



Percent hits 69.9 15.9 79.7n 9.9 84.6n 12.5Total false alarms (FA) 13.4 15.1 8.1 8.9 4.5 4.8FA to unattended deviants 4.9 3.3 3.2 3.1 0.8n 1.2Median RT (ms) 555 38 510n 41 480n 60

nSignificantly different from the 9-year-old group at po.05.

postselection processing. Further, in the duration condition, the

relationship between channel and postselection processing rep-

licated that found in the adult literature. Our data also suggest

that latency measures, especially peak latency, may be more re-

liable indicators of development than amplitude in children who

evidence waveforms that are scoreable for latency.

Target Detection Processes

Target detection processes were assessed using both behavioral

and electrophysiological measures. Behaviorally age-related im-

provements were seen in both hits and reaction times. Adults

were more accurate than children in both target conditions and

faster than children for intensity targets. Large P3bs were elicited

from participants in all three age groups by attended targets. In

the intensity condition, P3b amplitude was significantly related

to hits and RT (larger P3bs associated with faster RTs) after

controlling for age. These relationships, however, were not sig-

nificant in the duration condition. In summary, children continue

to evidence improvements in speed and accuracy of target de-

tection through adolescence.

In adults research has found that Nd amplitude is associated

with target detection accuracy (Hillyard & Hansen, 1986). In an

absolute sense we know that this is not true of our data, as Nd

amplitudes are similar across the age groups, in contrast to ac-

curacy, which is better for the adults. However, when we con-

trolled for age in the analyses we also found no relationship

between amplitude and accuracy. Further, no relationships were

evident when the correlations were examined within group, per-

haps due to the small sample sizes. Nd amplitude, as calculated

here, reflects processing of the standard stimuli and so would not

be expected to be directly related to accuracy. However, as it is

thought to reflect attention allocation, one might expect there to

be some relationship, as has been shown in the literature. Our Nd

amplitude data evidenced substantial interindividual variability

and is not significantly correlated across target conditions.

Further, pretest matching for target discrimination that led to

interindividual differences in the physical separation between

standards and the presented targets reduced the range of target

accuracy values. Perhaps the impact of these factors on the am-

plitude and accuracy data masked the relationship between

the variables. Alternatively, as Nd occurs relatively early in the

stimulus processing and responding occurs relatively late, the

relationship between these variables may not be as strong early in

development. Consistent with this suggestion, Bartgis et al.

(2003) also found no relationship between Nd amplitude and

measures of accuracy in their study of 5–9-year-olds. Interest-

ingly, however, in our data, peak latency in the intensity con-

dition was significantly correlated with accuracy, again

suggesting that latency may be an important measure of Nd in

developmental studies.

Effectiveness of Channel Selection Processes

The maintenance and strength of the attention directed toward

the identified channel (effectiveness of channel selection) was also

examined using both behavioral and electrophysiological mea-

sures. FA to unattended deviants decreased with age, suggesting

improvements in the effectiveness of channel selection. No age

differences were seen in the amplitudes of the P3bs elicited by the

unattended deviants; however, interparticipant variability was

again large, especially in the children. Mean P3b amplitude

measures may mask occasional awareness and processing of the

unattended deviant and, consequently, may be too gross a mark-

er of effectiveness of channel selection processes in this age range.

The literature is equivocal on the impact of development on

P3b elicited by deviants in the unattended channel. A develop-

mental increase in the attention effect on the P3b was found by

Satterfield et al. (1990) in their study exploring intermodal se-

lective attention (also see Bartgis et al., 2003; Brooker, 1980, as

reported in Donald, 1983). However, no attention effect was

found for unattended deviants in the van der Stelt et al. (1998)

developmental study of visual selective attention or in the van der

Molen, Somsen, and Jennings (2000) study of phasic heart rate

changes. Finally, although P3b was not formally analyzed in the

Berman and Friedman (1995) study, an examination of their

figures suggests that the unattended deviants did not elicit sig-

nificant P3b even from the children in the youngest age group. It

is probable that there is a developmental improvement in the

ability to sustain attention on the relevant channel that is im-

pacted by task, but P3b may be a less sensitive measure than

behavioral responding, especially in early adolescents.

In summary, by age 9 children seem able to successively al-

locate their attention to the appropriate channel; however, they

are slower and less efficient than adults, which results in the more

frequent processing of and inappropriate responding to the un-

attended deviant.

Developmental Effects of Target Type

Based on preliminary data in a clinical group of children, we

expected that the amplitude of Nd would be smaller and the

latency would be longer in the channel with the duration target

than in the channel with the intensity target. No differences inNd

amplitude were found and the impact of task was more compli-

cated than we had anticipated.

Despite matching for accuracy in a pretest, responses to du-

ration targets were faster and more accurate than responses to

intensity targets, suggesting that the duration selective attention

task may have been slightly easier and the duration targets more

salient. No group, however, approached ceiling level perfor-

mance on either task. RTs were stable across the three age groups

for duration but evidenced a developmental decrease for inten-

sity. The age-related stability in RT is difficult to interpret in this

context, as RT is related to the physical separation between the

target and the standard stimuli, which was larger for the children

than for the adults in both conditions. Consequently, the RTs

reflect both developmental improvements in speed of responding

as well as target-size-related differences. In the duration condi-

tion, where the targets were shorter in duration, it is probable

that these two factors canceled each other out, leading to an

absence of a developmental change in the RTs.

724 H. Gomes et al.

Table 9. Partial Correlations Controlling for Age between

Electrophysiological and Behavioral Measures

Hits False alarms Median RT

IntensityNd peak latency (n5 38) � .398n .414n .098Nd amplitude (n5 48) � .041 .059 � .009P3b amplitude (n5 48) .432nn � .210 � .353n

DurationNd peak Latency (n5 35) � .050 .160 .074Nd Amplitude (n5 48) � .045 � .125 .077P3b Amplitude (n5 48) .035 � .192 � .011

npo.05, nnpo.01 two-tailed comparisons.

The pattern of FA to unattended deviants may also have been

impacted by the greater salience of the duration targets/deviants.

Smaller age effects were seen when the unattended deviant

differed in intensity (this is in the duration condition) than when

it differed in duration (this is in the intensity condition). This

finding suggests better maintenance of sustained attention to the

appropriate channel during the duration detection task than the

intensity task, possibly reflecting the less salient, distracting na-

ture of the intensity than the duration deviants.

Consistent with this behavioral suggestion of better sustained

attention during the duration task, peak latency of the Nd was

found to be negatively correlated with Nd amplitude at FCz in

this task. Participants with shorter Nd peak latencies evidenced

larger amplitude Nds, even when controlling for the effect of age.

Larger amplitude Nds have also been associated with faster

channel assignment in the literature (Naatanen, 1992). This re-

lationship between peak latency and amplitude was not seen in

the intensity condition. In summary, there appears to be more

efficient channel assignment, sustained attention, and target de-

tection during the duration task than the intensity task, all pos-

sibly related to the salience of the duration target/deviant.

In contrast, smaller age effects were seen for peak latency in

the intensity condition than in the duration condition, perhaps

suggesting more mature postselection stimulus processing. Sup-

port for this proposal comes from the correlational analyses,

which found that the amplitude of P3b elicited by intensity tar-

getswas related to both hits andRTafter controlling for age. Fast

and accurate responding to intensity targets was associated with

larger P3b amplitudes. These relationships, however, were not

significant in the duration condition.

Task effects on the development of target detection measures

have been previously reported in the literature (e.g., Jensen &

Neff, 1993). However, the task effects on the latency of the Nd

are notable. Nd in this study was calculated by subtracting the

waveform elicited by the unattended standard from those elicited

by the attended standard. The standards were identical in the

duration and intensity target conditions, suggesting that task

impacted the processing of the standards. Other studies have

found that variations in the context determined by the nature of

the standards have impacted the Nd (Arnott & Alain, 2002), but

we believe this is the first study to suggest an effect of target type

on Nd. Further research into the effects of context and target

type onNd and selective attention processes are clearly indicated.

Summary

Our data is most consistent with a model of developmental im-

provement in the speed and efficiency of attention allocation

(Ridderinkhof & van der Stelt, 2000). We found that the onset

andpeak latencies ofNd for the childrenwere significantly longer

than for the adults, suggesting that, although children are able to

selectively attend to a specified channel, they require more in-

formation about the feature distinguishing the channel or more

time to processes that information. Further, it is probable that

the process of selectively attending is more effortful. A conse-

quence of this increased processing time may be that the children

acquire more information about the stimulus prior to channel

assignment than do adults. Once the channel is determined, the

postselection processing reflected in the Nd amplitude does not

appear to change in the age range of our study; however, the

literature suggests that there may be developmental improve-

ments in this process in younger children. During postselection

processing, the presence of a target stimulus must be determined.

Children are less accurate than adults at responding to the tar-

gets, despite the additional time they have taken processing the

stimuli. The process of target detection requires the detection of

the target and the initiation of a response. Changes in either one

or both of these steps may contribute to the developmental im-

provements seen. Further, children are more likely to respond to

the unattended deviants, especially when they are duration de-

viants, suggesting both an awareness of the deviant and a failure

to inhibit responding to the deviant. It is possible that the chil-

dren are more aware of the deviants than the adult due to the

extended time spent processing the stimuli at the channel selec-

tion stage. Consequently, it is not clear whether they are poorer

at inhibiting a response or just more reliant on it. Further, it

appears that the type and/or physical separation between the

standard and the target/deviant may impact the efficiency of

processing at many of these steps. Future research should focus

on developmental changes in the processing at each of these

stages. A better understanding of the developmental changes in

all of the stages of the selective auditory attention process in

typically developing children is critical if wewant to usemeasures

such as Nd to study cognitive processes in children with neuro-

psychological issues. Having better models of normal develop-

ment will allow us to determine whether processing in children

with disabilities reflects developmentally delayed or develop-

mentally aberrant processing.

REFERENCES

Alho, K., Tottola, K., Reinikainen, K., Sams, M., & Naatanen, R.(1987). Brain mechanism of selective listening reflected by event-re-lated potentials. Electroencephalography & Clinical Neurophysiology,68, 458–470.

Arnott, S. R., & Alain, C. (2002). Effects of perceptual context on event-related brain potentials during auditory spatial attention. Psycho-physiology, 39, 625–632.

Bartgis, J., Lilly, A. R., & Thomas, D. G. (2003). Event-related potentialand behavioral measures of attention in 5-, 7-, and 9-year-olds. TheJournal of General Psychology, 130, 311–335.

Berman, S., & Friedman, D. (1995). The development of selective at-tention as reflected by event-related potentials. Journal of Experi-mental Child Psychology, 59, 1–31.

Brooker, B. H. (1980) The development of selective attention in learningdisabled and normal boys: An auditory evoked potential and behav-ioral analysis. Unpublished doctoral dissertation. Kingston, Ontario,Canada: Queens University.

Coch, D., Sanders, L. D., & Neville, H. J. (2005). An event-relatedpotential study of selective auditory attention in children and adults.Journal of Cognitive Neuroscience, 17, 605–622.

Cooly, E. L., & Morris, R. D. (1990). Attention in children: A neuro-psychologically based model for assessment. Developmental Neuro-psychology, 6, 239–274.

Dempster, F. N. (1981). Memory span: Sources of individual and de-velopmental differences. Psychological Bulletin, 89, 63–100.

Dempster, F. N. (1995). Resistance to interference: Developmentalchanges in a basic processing mechanism. Annals of the New YorkAcademy of Sciences, 769, 3–27.

Dien, J., Tucker, D. M., Potts, G., & Hartry-Speiser, A. (1997).Localization of auditory evoked potentials related to selectiveintermodal attention. Journal of Cognitive Neuroscience, 9,799–823.

Donald,M.W. (1983). Neural selectivity in auditory attention: Sketch ofa theory. In A. W. K. Gaillard & W. Ritter (Eds.), Tutorials in ERP


research: Endogenous components (pp. 37–77). Amsterdam: NorthHolland Publishing Company.

Doyle, A. (1973). Listening to distraction: A developmental study ofselective attention. Journal of Experimental Child Psychology, 15,100–115.

Duff, M., Barnhardt, J., & Gomes, H. (2004). Selective attention, chan-nel separability, and event related potentials in children. Poster pre-sented at the Society for Psychophysiological Research.

Foster, J. K., Eskes, G. A., & Stuss, D. T. (1994). The cognitiveneuroscience of attention: A frontal lobe perspective. Cognitive Neu-ropsychology, 11, 133–147.

Friedman, D. (1991). The endogenous scalp-recorded brain potentialsand their relationship to cognitive development. In J. R. Jennings &M. Coles (Eds.),Handbook of cognitive psychophysiology: Central andautonomic nervous system approaches (pp. 621–656). New York: JohnWiley & Sons.

Geffen, G., & Sexton, M. A. (1978). The development of auditory strat-egies of attention. Developmental Psychology, 14, 11–17.

Gerken, L. (1994). Sentential processes in early child language: Evidencefrom the perception and production of function morphemes. In J. C.Goodman & H. C. Nusbaum (Eds.), The development of speech per-ception (pp. 271–298). Cambridge, MA: MIT Press.

Gibson, E., & Rader, N. (1979). Attention: The perceiver as performer.In G. A. Hale &M. Lewis (Eds.),Attention and cognitive development(pp. 1–21). New York: Plenum Press.

Gomes, H., Molholm, S., Christodoulou, C., Ritter, W., & Cowan, N.(2000). The development of auditory attention in children. Frontiersin Bioscience, 5, 107–120.

Guttentag, R. E., & Ornstein, P. A. (1990). Attentional capacityand children’s memory strategy use. In J. T. Enns (Ed.), Develop-ment of attention: Research and theory (pp. 305–320). Amsterdam:Elsevier.

Halperin, J. M., McKay, K. E., Matier, K., & Sharma, V. (1994). At-tention, response inhibition, and activity level in children: Develop-mental neuropsychological perspectives. In M. G. Tramontana & S.R. Hooper (Eds.), Advances in child neuropsychology (vol. 2, pp.1–54). New York: Springer-Verlag.

Harnishfeger, K. K., & Bjorklund, D. F. (1995). The ontogeny of in-hibition mechanisms: A renewed approach to cognitive development.Annals of the New York Academy of Sciences, 769, 28–49.

Hillyard, S. A., & Hansen, J. C. (1986). Attention: Electrophysiologicalapproaches. In M. G. H. Coles, E. Donchin, & S. W. Porges (Eds.),Psychophysiology: Systems, processes, and applications (pp. 227–243).New York: Guilford Press.

Hillyard, S. A., Mangun, G. R., Woldorff, M. G., & Luck, S. J. (1995).Neural systems mediating selective attention. In M. S. Gazzaniga(Ed.), The cognitive neurosciences (pp. 665–681). Cambridge, MA:MIT Press.

Huttenlocher, P. R., & Dabholkar, A. S. (1997). Regional differences insynaptogenesis in human cerebral cortex. Journal of ComparativeNeurology, 20, 167–178.

Jensen, J. K., & Neff, D. L. (1993). Development of basic auditorydiscrimination in preschool children. Psychological Science, 4, 104–107.

Johnson, R. (1989). Developmental evidence for modality-dependentP300 generators: A normative study. Psychophysiology, 26, 651–667.

Jonkman, L. M., Kemner, C., Verbaten, M. K., Koelega, H. S., Cam-fferman, G., van der Gaag, R. J., et al. (1997). Event-related poten-tials and performance of attention-deficit hyperactivity disorder:Children and normal controls in auditory and visual selective atten-tion tasks. Biological Psychiatry, 41, 595–611.

Kail, R. (1990). The development of memory in children. New York: W.Freeman & Co.

Kasai, K., Nakagome, K., Itoh, K., Koshida, I., Fukuda,M.,Watanabe,A., et al. (1999). Electrophysiological evidence for sequentialactivation of multiple brain regions during the auditory selective at-tention process in humans. NeuroReport, 10, 3837–3842.

Klenberg, L., Korkman, M., & Lahti-Nuuttila, P. (2001). Differentialdevelopment of attention and executive functions in 3- to 12-year-oldFinnish children. Developmental Neuropsychology, 20, 407–428.

Lane, D. M., & Pearson, D. A. (1982). The development of selectiveattention. Merrill-Palmer Quarterly, 28, 317–337.

Loiselle, D. L., Stamm, J. S., Maitinsky, S., & Whipple, S. C. (1980).Evoked potential and behavioral signs of attention dysfunction inhyperactive boys. Psychophysiology, 17, 193–201.

Maatta, S., Paakkonen, A., Saavalainen, P., & Partanen, J. (2005).Selective attention event-related potential effects from auditorynovel stimuli in children and adults. Clinical Neurophysiology, 116,129–141.

Maccoby, E. (1969). The development of stimulus selection. MinnesotaSymposia on Child Psychology, 3, 68–96.

McKay, K. E., Halperin, J. M., Schwartz, S. T., & Sharma, V. (1994).Developmental analysis of three aspects of information processing:Sustained attention, selective attention and response organization.Developmental Neuropsychology, 10, 121–132.

Meehan, S., Singhal, A., & Fowler, B. (2005). The late Nd reflects amemory trace containing amodal spatial information. Psychophysi-ology, 42, 531–539.

Muller-Gass, A., & Campbell, K. (2002). Event-related potential mea-sures of the inhibition of information processing: I. Selective attentionin the waking state. International Journal of Psychophysiology, 46,177–195.

Naatanen, R. (1992). Attention and brain function. Hillsdale, NJ: Law-rence Erlbaum.

Naatanen, R., Alho, K., & Schroger, E. (2001). Electrophysiology ofattention. In H. Pashler (Ed.), Steven’s handbook of experimentalpsychology (3rd ed., (vol. 4, pp. 601–653). New York: John Wiley &Sons.

Parasuraman, R. (1980). Effects of information processing demands onslow negative shift latencies and N100 amplitude in selective and di-vided attention. Biological Psychology, 11, 217–233.

Petkov, C. I., Kang, X., Alho, K., Bertrand, O., Yund, E. W., &Woods,D. L. (2004). Attentional modulation of human auditory cortex. Na-ture Neuroscience, 7, 658–663.

Picton, T. W. (1992). The P300 wave of the human event-related poten-tial. Journal of Clinical Neurophysiology, 9, 456–479.

Plude, D. J., Enns, J. T., & Brodeur, D. (1994). The developmentof selective attention: A life-span overview. Acta Psychologica, 86,227–272.

Posner, M. I., & Rothbart, M. K. (2000). Developing mechanisms of selfregulation. Development and Psychopathology, 12, 427–441.

Rebok, G. W., Smith, C. B., Pascualvaca, D. M., Mirsky, A. F., An-thony, B. J., & Kellam, S. G. (1997). Developmental changes in at-tentional performance in urban children from eight to thirteen years.Child Neuropsychology, 3, 28–46.

Reinvang, I. (1998). Validation of reaction time in continuous per-formance tasks as an index of attention by electrophysiologicalmeasures. Journal of Clinical and Experimental Neuropsychology, 20,885–897.

Ridderinkhof, K. R., & van der Stelt, O. (2000). Attention and selectionin the growing child: Views derived from developmental psychology.Biological Psychology, 54, 55–106.

Rothenberger, A., Banaschewski, T., Heinrich, H., Moll, G. H., Sch-midt, M. H., & van’t Klooster, B. (2000). Comorbidity in ADHD-children: Effects of coexisting conduct disorder or tic disorder onevent-related brain potentials in an auditory selective-attentiontask. European Archives of Psychiatry and Clinical Neuroscience,250, 101–110.

Sanders, L. D., Stevens, C., Coch, D., & Neville, H. J. (2006). Selectiveauditory attention in 3- to 5-year-old children: An event-related po-tential study. Neuropsychologia, 44, 2126–38.

Satterfield, J. H., Schell, A. M., Nicholas, T. W., Satterfield, B. T., &Freese, T. E. (1990). Ontogeny of selective attention effects on eventrelated potentials in attention-deficit hyperactivity disorder and nor-mal boys. Biological Psychiatry, 28, 879–903.

Schreiber, H., Stolz-Born, G., Kornhuber, H. H., & Born, J. (1992).Event-related potential correlates of impaired selective attentionin children at high risk for schizophrenia. Biological Psychiatry, 32,634–651.

Sexton, M. A., & Geffen, G. (1979). Development of three strategiesof attention in dichotic monitoring. Developmental Psychology, 3,299–310.

Sowell, E. R., Thompson, P. M., Tessner, K. D., & Toga, A. W.(2001). Mapping continued brain growth and gray matter densityreduction in dorsal frontal cortex: Inverse relationships duringpostadolescent brain maturation. Journal of Neuroscience, 21,8819–8829.

Van der Molen, M. W., Somsen, R. J. M., & Jennings, J. R. (2000).Developmental change in auditory selective attention as reflected byphasic heart rate changes. Psychophysiology, 37, 626–633.

726 H. Gomes et al.

Van der Stelt, O., Kok, A., Smulders, F. T. Y., Snel, J., &Gunning,W. B.(1998). Cerebral event-related potentials associated with selective at-tention to color: Developmental changes from childhood to adult-hood. Psychophysiology, 35, 227–239.

Wetzel, N., Widmann, A., Berti, S., & Schroger, E. (2006). The devel-opment of involuntary and voluntary attention from childhood toadulthood: A combined behavioral and event-related potential study.Clinical Neurophysiology, 117, 2191–2203.

Woldorff, M. G., & Hillyard, S. A. (1991). Modulation of earlyauditory processing during selective listening to rapidly presentedtones. Electroencephalography and Clinical Neurophysiology, 79,170–191.

(Received January 16, 2007; Accepted April 24, 2007)


Development of auditory selective attention: Event-related potential measures of channel selection...

Documents

Transcript of Development of auditory selective attention: Event-related potential measures of channel selection...