cross-form conceptual relations between sounds and words: effects on the novelty p3

7
Research report Cross-form conceptual relations between sounds and words: effects on the novelty P3 David Friedman a, * , Yael M. Cycowicz a , Isabel Dziobek b a Cognitive Electrophysiology Laboratory, New York State Psychiatric Institute-Unit 6, 1051 Riverside Drive, New York City, NY 10032, USA b Neuroimaging Laboratory, Center for Brain Health, New York University School of Medicine, 560 First Avenue, New York City, NY 10016, USA Accepted 10 September 2003 Abstract In order for cross-form conceptual priming to occur, the brain must extract an amodal representation of the presented concept. To determine whether the novelty P3 would show such cross-form effects, novel, environmental sounds or their verbal equivalents were repeated two blocks after their first presentation in two cross-form conditions, word–sound (e.g., the word ‘‘pig’’ followed by the sound ‘‘oink’’) or sound – word. Conceptual repetition engendered an asymmetric reduction in novelty P3 amplitude, i.e., amplitude was reduced in the sound – word but not in the word – sound condition. The data suggest that the novelty P3 reflects an evaluative stage of processing in which some semantic information is extracted. However, the lack of amplitude reduction for the word –sound condition implies that, at least at the delays used here, repetition as a conceptually equivalent sound may have failed to make contact with the initial verbal concept. D 2003 Elsevier B.V. All rights reserved. Theme: Neural basis of behavior Topic: Learning and memory Keywords: ERPs; Novelty P3; Orienting response; Conceptual priming 1. Introduction Orienting is a critical aspect of human behavior. The orienting response [28] is an involuntary shift of attention that is a fundamental biological mechanism necessary for survival. The neurocognitive changes engendered by the orienting response enable the organism to respond appro- priately to a variety of familiar and unfamiliar environmen- tal events (see Ref. [19] for a review). The orienting response functions as a what-is-it detector and involves a rapid response to new (never experienced before), unex- pected (out of context) or unpredictable stimuli. The detec- tion of a new or unexpected event precedes the orienting response and induces the involuntary capture of attention, enabling the event to enter consciousness. This permits an evaluation of the salience of the stimulus. If the event is deemed significant, this could lead to appropriate behavioral action. Hence, in addition to sensory analysis, evaluation of a potentially relevant event also appears to involve some kind of semantic analysis to extract meaning (see Ref. [19] for examples). A key characteristic of an orienting response is that it habituates with subsequent presentations of the stimulus or stimuli that initially elicited it. Modulations of the novelty P3 component of the event- related brain potential (ERP) have been interpreted within the rubric of the orienting response. Hence, the novelty P3 has been the subject of intense scrutiny in situations in which the unexpectedness and novelty of stimuli have been shown to engender an orienting response (reviewed in Ref. [13]). This component, which has a latency to peak of about 320 ms, is elicited by infrequently occurring ‘‘novel’’ or unexpected stimuli that are intermixed with frequently occurring events within the context of an ‘‘oddball’’ para- digm. These stimuli can be considered novel on the basis of their unusual characteristics, such as weird, unexpected environmental sounds presented among expected tones, or on the basis of the context in which those events occur, for example, infrequent tones presented for the very first time to the subject [11]. The novelty P3 does not appear to be the brain event that signals the detection of an unexpected 0926-6410/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.cogbrainres.2003.09.002 * Corresponding author. Tel.: +1-212-543-5476; fax: +1-212-543- 6002. E-mail address: [email protected] (D. Friedman). www.elsevier.com/locate/cogbrainres Cognitive Brain Research 18 (2003) 58 – 64

Upload: david-friedman

Post on 05-Sep-2016

212 views

Category:

Documents


0 download

TRANSCRIPT

www.elsevier.com/locate/cogbrainres

Cognitive Brain Research 18 (2003) 58–64

Research report

Cross-form conceptual relations between sounds and words:

effects on the novelty P3

David Friedmana,*, Yael M. Cycowicza, Isabel Dziobekb

aCognitive Electrophysiology Laboratory, New York State Psychiatric Institute-Unit 6, 1051 Riverside Drive, New York City, NY 10032, USAbNeuroimaging Laboratory, Center for Brain Health, New York University School of Medicine, 560 First Avenue, New York City, NY 10016, USA

Accepted 10 September 2003

Abstract

In order for cross-form conceptual priming to occur, the brain must extract an amodal representation of the presented concept. To

determine whether the novelty P3 would show such cross-form effects, novel, environmental sounds or their verbal equivalents were repeated

two blocks after their first presentation in two cross-form conditions, word–sound (e.g., the word ‘‘pig’’ followed by the sound ‘‘oink’’) or

sound–word. Conceptual repetition engendered an asymmetric reduction in novelty P3 amplitude, i.e., amplitude was reduced in the sound–

word but not in the word–sound condition. The data suggest that the novelty P3 reflects an evaluative stage of processing in which some

semantic information is extracted. However, the lack of amplitude reduction for the word–sound condition implies that, at least at the delays

used here, repetition as a conceptually equivalent sound may have failed to make contact with the initial verbal concept.

D 2003 Elsevier B.V. All rights reserved.

Theme: Neural basis of behavior

Topic: Learning and memory

Keywords: ERPs; Novelty P3; Orienting response; Conceptual priming

1. Introduction

Orienting is a critical aspect of human behavior. The

orienting response [28] is an involuntary shift of attention

that is a fundamental biological mechanism necessary for

survival. The neurocognitive changes engendered by the

orienting response enable the organism to respond appro-

priately to a variety of familiar and unfamiliar environmen-

tal events (see Ref. [19] for a review). The orienting

response functions as a what-is-it detector and involves a

rapid response to new (never experienced before), unex-

pected (out of context) or unpredictable stimuli. The detec-

tion of a new or unexpected event precedes the orienting

response and induces the involuntary capture of attention,

enabling the event to enter consciousness. This permits an

evaluation of the salience of the stimulus. If the event is

deemed significant, this could lead to appropriate behavioral

action. Hence, in addition to sensory analysis, evaluation of

0926-6410/$ - see front matter D 2003 Elsevier B.V. All rights reserved.

doi:10.1016/j.cogbrainres.2003.09.002

* Corresponding author. Tel.: +1-212-543-5476; fax: +1-212-543-

6002.

E-mail address: [email protected] (D. Friedman).

a potentially relevant event also appears to involve some

kind of semantic analysis to extract meaning (see Ref. [19]

for examples). A key characteristic of an orienting response

is that it habituates with subsequent presentations of the

stimulus or stimuli that initially elicited it.

Modulations of the novelty P3 component of the event-

related brain potential (ERP) have been interpreted within

the rubric of the orienting response. Hence, the novelty P3

has been the subject of intense scrutiny in situations in

which the unexpectedness and novelty of stimuli have been

shown to engender an orienting response (reviewed in Ref.

[13]). This component, which has a latency to peak of about

320 ms, is elicited by infrequently occurring ‘‘novel’’ or

unexpected stimuli that are intermixed with frequently

occurring events within the context of an ‘‘oddball’’ para-

digm. These stimuli can be considered novel on the basis of

their unusual characteristics, such as weird, unexpected

environmental sounds presented among expected tones, or

on the basis of the context in which those events occur, for

example, infrequent tones presented for the very first time to

the subject [11]. The novelty P3 does not appear to be the

brain event that signals the detection of an unexpected

D. Friedman et al. / Cognitive Brain Research 18 (2003) 58–64 59

event, but rather reflects an evaluation of the novel or

unexpected stimulus. Several studies have demonstrated

habituation at frontal as compared to posterior scalp sites to

be a ubiquitous characteristic of the novelty P3 [4,5,12,16].

These data further support the hypothesis advanced by

Friedman et al. [13] that the novelty P3 reflects aspects of

the orienting response, and that it is comprised of frontal

and posterior subcomponents, each with different func-

tional characteristics (for a somewhat similar view, see

Refs. [10,31]).

Semantic habituation effects, also a characteristic of the

orienting response [19], have been demonstrated on the

novelty P3. For example, Cycowicz and Friedman [6]

presented novel, environmental sounds, along with fre-

quently occurring tones, in an oddball paradigm, in which

many of the environmental sounds repeated two blocks

after their first presentation. These investigators had sub-

jects rate the familiarity of these sounds, and then, based

upon those ratings, categorized the sounds into familiar and

unfamiliar classes. The key findings were that (1) repetition

of familiar sounds led to a reduction of the novelty

P3 over frontal scalp sites, but no significant difference

occurred over posterior scalp sites, and (2) for unfamiliar

sounds, there was no change with repetition over frontal

locations, but over posterior scalp sites, repetition led to an

enhancement of novelty P3 amplitude. Because novelty P3

amplitude appeared to be modulated by the familiarity of

the sound, this was interpreted to suggest that it must

reflect a fairly late stage of information processing, one that

might be close to the extraction of the sound’s semantic

attributes.

The current study was initiated to shed further light on

the issue of semantic habituation effects on the novelty P3.

To more definitively conclude that the novelty P3 is affected

by the semantic attributes of stimuli would require demon-

stration of cross-form habituation effects. That is, a reduc-

tion in novelty P3 amplitude should be demonstrable when

an environmental sound is repeated as its verbal equivalent

(e.g., the sound ‘‘oink’’ repeated as the word ‘‘pig’’) or

when the verbal equivalent is repeated as the conceptually

equivalent sound (the word ‘‘duck’’ followed by the sound

‘‘quack’’). This is not typical cross-form repetition, as for

example, would be represented by the visually presented

word ‘‘tiger’’ followed by the auditory version of ‘‘tiger,’’

which occurs between modalities. Rather, these kinds of

pairings reflect within-modality, conceptual relations be-

tween the word and the environmental sound (see Ref.

[30] for behavioral and ERP examples during tasks other

than the novelty oddball). That is, in order for habituation

effects to occur in these situations, the brain would have to

have access to an amodal, semantic representation of the

auditory concept. Hence, in the experiment reported here,

cross-form conceptual ‘‘repetition’’ of unique environmental

sounds (both word–sound and sound–word pairings) oc-

curred within the context of a novelty oddball paradigm.

Similar to previous studies from this laboratory, subjects

were not informed about the presence of either the sounds or

their verbal counterparts. The observation of cross-form

ERP reductions to conceptually equivalent word–sound or

sound–word pairings would suggest that environmental

sounds do, indeed, engender access to meaning. This would

be the case because an amodal, semantic, representation

would have had to have been generated in order for this kind

of reduction to take place. Because word–sound and

sound–word pairings are not identical in terms of both their

perceptual and semantic attributes, we expected that habit-

uation effects for these two types of pairings would not be

identical.

2. Materials and methods

2.1. Subjects

Sixteen subjects (nine female) between the ages of 20

and 26 (mean age = 21.7) were recruited by notices posted

within the Columbia Presbyterian Medical Center commu-

nity. All subjects reported themselves to be in good health

and to have no major medical, neurological or psychiatric

problems. All subjects signed informed consent, were

native English speakers and received payment for their

participation.

2.2. Stimuli

The stimuli were pure tones, environmental sounds and

their verbal equivalents. The pitches of the pure tones

were 1000 Hz (high tone) and 700 Hz (low tone), and

their duration was 336 ms. In a separate normative study,

65 undergraduates were asked to write down the name of

each of 180 sounds taken from sound effects compact

disks. Of these 180 sounds, 64 unique sound concepts

with the highest name agreements (i.e., the percentage of

the 65 subjects producing the same name) were retained

for the experiment. These sounds and their verbal equiv-

alents were then categorized into four lists, with 16 sounds

per list. There were no reliable differences in name

agreement (which varied from 83% to 91%), or intensity

(matched using the sound and word envelope character-

istics) among the four lists. Mean durations and ranges

were, for the sounds, M = 881 ms, range = 377–1000 ms;

for the words, these values were M = 709 ms, range = 384–

1000 ms. Additionally, the four sets of words and four sets

of sounds did not differ in intensity. Two of the lists were

assigned to the novelty oddball task (see below) to the

sound–word or word–sound repetition conditions, and

the other two were assigned as foils for the recognition

task. These list assignments were counterbalanced across

subjects. The sounds came from several categories, such

as animal, human, musical instrument and artificial

or machine sounds. All stimuli were delivered at 75 dB

SPL.

e Brain Research 18 (2003) 58–64

2.3. Procedure

The experiment consisted of three phases. The first was a

standard auditory oddball task, the second was a novelty

oddball task and the third was a recognition memory test

phase. The data resulting from the recognition phase will not

be reported.

2.3.1. Standard oddball task

Subjects were presented with high and low pure tones in

random order. One tone was presented 88% of the time and

was designated the standard and the other tone was pre-

sented 12% of the time and was designated the target. There

were two blocks of 100 trials each with an inter-stimulus

interval of 1500 ms.

2.3.2. Novelty oddball task

Following the standard oddball task, subjects were pre-

sented with 10 blocks of 80 trials each, again with inter-

stimulus intervals of 1500 ms. Novel stimuli (10%) were

randomly intermixed with standard (80%) and target (10%)

tones. The novels were either environmental sounds or their

verbal equivalents. Subjects were not informed of the

occurrence of the novel stimuli.

There were 32 different non-tonal, environmental sounds

and 32 verbal equivalents. Hence, 16 of each type of novel

event was repeated in its cross-form counterpart (i.e.,

sound1–word2; word1–sound2; these are hereafter referred

to as prime–repeat pairings). Each block contained eight

novel events. In the first two blocks, all of the novel events

were new, while in the rest of the blocks only half were new.

The eight sounds and eight verbal equivalents that did not

repeat (labeled ‘‘unique’’) comprised half of the novel items

in the first two and the last two blocks (four in each block).

These items were taken from environmental sound stimuli

that did not pass the name agreement criterion and are not

analyzed in the data reported below. Conceptual repetition

of the novel stimuli occurred two blocks after their initial

presentation, such that, for example, the novel stimuli

initially presented in the first block were repeated in the

third block. The repetitions were always cross-form. Stimuli

were randomized separately for each subject, with the

restrictions that a target or a novel could not occur as the

first or the last stimulus, and that two targets or novels could

not be presented sequentially.

For both tasks, subjects were instructed to press a button

(emphasizing speed) with the thumb of one hand as soon as

they heard the target tone. Hand of response and target tone

were counterbalanced across subjects. Reaction times be-

tween 200 and 1600 ms were accepted as correct responses.

2.4. EEG recordings

EEG (5-s time constant; 50 Hz upper cutoff; 200 Hz

digitization rate) was recorded (Sensorium amplifiers) con-

tinuously using an Electrocap (Electrocap International)

D. Friedman et al. / Cognitiv60

from 62 extended 10–20 system placements [21], including

left and right mastoids, all referred to nosetip. Vertical EOG

was recorded bipolarly from electrodes placed on the

supraorbital and infraorbital ridges of the right eye, and

horizontal EOG was recorded bipolarly from electrodes

placed on the outer canthi of the two eyes. Trials containing

eye movement artifact were corrected off-line using the

procedure developed by Gratton et al. [14]. Trials were

epoched off-line with 100 ms pre- and 1400 ms post-

stimulus periods.

2.5. Data analyses

The SPSS Version 10 for Windows (repeated-measures

ANOVA) computer program was used for all analyses. The

Greenhouse–Geisser epsilon (e) correction [15] was used

where appropriate. Post hoc testing was performed using the

Tukey Honestly Significant Difference test. Uncorrected

degrees of freedom are reported along with the epsilon

value; the P values reflect the epsilon correction.

3. Results

The data resulting from the standard oddball task were

entirely consistent with previous data recorded from this and

other laboratories. Because they are uninformative with

respect to the novelty P3, they will not be reported.

During the novelty oddball task, subjects were very

accurate in detecting the target (99%) with mean reaction

time of 431 ms, and very occasionally had false alarms to

standard (0.08%) and novel (0.9%) stimuli.

The range of the mean number (F S.D.) of the trials

entering the four depicted waveforms of Fig. 1 varied,

respectively, from 15.4 (0.6) to 15.7 (1.0). The figure

presents the grand mean ERPs associated with first and

second presentations of sounds and words in the two

prime–repeat conditions. The figure depicts the data at the

electrode locations that were analyzed in the ANOVAs

described below. The left three columns of Fig. 1 depict

the sound–word and the right three columns the word–

sound waveforms. The figure suggests that reduction in the

amplitude of the novelty P3 is larger for the sound1–word2

combination of prime and repeat.

A second positivity is also present in the ERPs depicted

in Fig. 1. This component has been observed previously [7]

and is most likely synonymous with the P3b. Because no a

priori predictions were made for this component and its

relation to conceptual repetition, these data will not be

discussed further.

To assess effects on the novelty P3 statistically, planned

comparisons were performed. Novelty P3 amplitude was

measured as an averaged voltage between 280 and 380 ms,

based on inspection of the grand mean ERPs. To capture any

lateralized and/or anterior/posterior effects, the following

electrode sites were considered: on the left, F1, FC1, C1,

Fig. 1. Grand mean ERPs averaged across the 16 subjects for the two cross-form conditions of the experiment: (left) ERPs in the sound1–word2 prime– repeat

pairing recorded at left, midline and right scalp sites; (right) ERPs in the word1–sound2 prime– repeat pairing also recorded at left, midline and right scalp

sites. Arrows mark stimulus onset. The SP and CSD maps for the two prime– repeat pairings are depicted below the corresponding display of waveforms. The

maps are based on the difference in novelty P3 amplitude (measured from 280 to 380 ms) between the first and second presentations in each prime– repeat

condition. The left two maps represent the sound1 minus word2 difference ERPs, and the second two, the word1 minus sound2 difference ERPs. Filled dots

represent the 62 scalp electrode locations. Shading reflects negativity; unshaded areas reflect positivity. SP D= 0.30 AV; CSD D = 0.02 AV/cm2.

Table 1

Results of the sound1–word2 and word1–sound2 ANOVAs

df F P value Epsilon (e)

Sound1–word2

Prime– repeat (P) 1.15 2.843 0.112

Lateral (L) 2.30 28.098 0.000 0.730

Anterior–posterior (A) 4.60 7.014 0.004 0.459

P�L 2.30 3.451 0.048 0.944

P�A 4.60 0.107 0.817 0.333

L�A 8.120 4.404 0.006 0.418

P�L�A 8.120 0.583 0.611 0.335

Word1–sound2

Prime– repeat (P) 1.15 1.385 0.258

Lateral (L) 2.30 21.528 0.000 0.691

Anterior–posterior (A) 4.60 8.886 0.003 0.366

P�L 2.30 0.318 0.701 0.871

P�A 4.60 0.296 0.707 0.418

L�A 8.120 5.614 0.001 0.479

P�L�A 8.120 0.634 0.627 0.460

Italicized F ratios are significant.

D. Friedman et al. / Cognitive Brain Research 18 (2003) 58–64 61

CP1 and P1; at the midline, Fz, FCz, Cz, CPz and Pz; and

on the right, F2, FC2, C2, CP2 and P2. These locations were

chosen based on our previous work, which showed a highly

focal midline scalp distribution and an anteriorly oriented

gradient for the novelty P3 (reviewed in Ref. [13]).

The two ANOVAs that contrasted the factors of Lateral

position on the scalp (left, midline, right), Anterior/Posterior

dimension (frontal, fronto-central, central, centro-parietal

and parietal) and Cross-Form Presentation (first, second—

e.g., sound1–word2) were performed separately on the

sound1–word2 and word1–sound2 prime–repeat condi-

tions. The results of these ANOVAs are presented in Table

1. The sound1–word2 data yielded reliable main effects of

Lateral position and Anterior/Posterior dimension. These

were modulated, however, by a reliable Lateral�Anterior/

Posterior interaction. Post hoc testing indicated that the

novelty P3 was largest at fronto-central scalp sites, with

this gradient steepest at the midline series of electrode sites.

Importantly, the Lateral�Cross-Form Presentation interac-

tion was also reliable. Post hoc testing indicated that,

although the differences between sound1 and word2 were

all reliable at left, midline and right scalp regions, the largest

reduction occurred at the midline (2.6 AV).For the word1–sound2 ANOVA, the Lateral and Ante-

rior/Posterior main effects were, again, reliable, and also

interacted. The Lateral�Anterior/Posterior reflected the

same phenomenon as in the sound1–word2 ANOVA. By

contrast with the sound1–word2 ANOVA, none of the main

or interaction effects involving the Cross-Form Presentation

factor was significant in the word1–sound2 ANOVA.

D. Friedman et al. / Cognitive Brain Research 18 (2003) 58–6462

Fig. 1 also depicts the surface potential (SP) and current

source density (CSD) scalp distributions (computed using a

third-order spherical spline interpolation algorithm [24]) of

the differences in novelty P3 amplitude between the first and

second presentations in the two cross-form conditions. The

left two maps represent the sound1 minus word2 difference

waveforms, and the right two maps, the word1 minus

sound2 difference ERPs. In support of the analysis de-

scribed above, a prefrontal positivity is present in the maps

for sound1–word2 prime–repeat subtraction (in both SP

and CSD distributions) but not in the word1–sound2

subtraction.

To determine if these differences were statistically reli-

able, the current source density difference mean data were

normalized using the root mean square method [20,25]. To be

compatible with the raw data analyses described above, the

waveforms were measured between 280 and 380 ms. The

data from all 62 scalp electrodes were used. The resultant

Condition (sound1–word2, word1–sound2)�Electrode

Location (62 levels) ANOVA on the normalized data returned

a reliable Condition�Electrode Location interaction

[F(61,915) = 4.11, P < 0.001, e= 0.11], indicating that the

scalp distributions of the two subtraction waveforms differed

reliably. Post hoc testing indicated that reliable differences

were obtained primarily over the frontal areas of the scalp.

1 We thank an anonymous reviewer for pointing this out to us.

4. Discussion

One way to ensure that sounds induce access to ‘‘mean-

ing’’ is to demonstrate that an environmental sound can

prime its verbal referent, or that the verbal representation

can prime its sound counterpart. Hence, in order for habit-

uation to have occurred, the brain would have had to have

access to an amodal representation of the concept, and this

would have had to have been available at least by approx-

imately 300 ms or so (the peak of the novelty P3). The

major finding was that reduction in novelty P3 amplitude

occurred only in the case in which a sound concept was

followed by its verbal conceptual equivalent (e.g., ‘‘oink’’

followed by the word ‘‘pig’’). By contrast, the converse,

‘‘pig’’ followed by the sound ‘‘oink,’’ did not lead to a

reduction in the magnitude of the novelty P3. This analysis

based on the raw data was also supported by the topographic

data. This latter analysis indicated that only in the former

situation was a prefrontal positivity present in the prime

minus repeat difference waveforms (see Fig. 1).

One possibility for the lack of reduction in the word–

sound prime–repeat condition is that, much like pictures

(e.g., Ref. [23]), sound concepts require processing on two

levels: perceptual and semantic. Verbal labels, on the other

hand, bear no perceptual relation to their sound equivalents.

Hence, when a verbal label is the conceptual repeat, as in the

sound1–word2 condition (one assumes), the verbal concept

contacts the semantic representation of the previously pre-

sented sound, engendering a reduction in amplitude. How-

ever, when a sound concept is the repeat, as in the word1–

sound2 pairing, both perceptual and semantic analyses must

ensue, leading to a greater amount of processing and hence

no reduction in novelty P3 amplitude.

In one scenario, subjects might intentionally label the

presented sound with its verbal equivalent, e.g., ‘‘pig’’ when

presented with the sound ‘‘oink,’’ or ask the question ‘‘Is

that the sound a pig makes?’’1 However, when the verbal

word ‘‘pig’’ is presented, participants would most likely not

say to themselves, ‘‘What sound does a pig make?’’ On this

view, in the case where the sound was presented first, the

verbal concept would have been activated, making contact

with the actual label when the conceptually equivalent word

was subsequently presented. On the other hand, when the

word was presented first, the equivalent sound concept (e.g.,

‘‘oink’’) would most likely not have been activated. There-

fore, when the conceptually equivalent sound was subse-

quently presented, there would have been a ‘‘mismatch’’ in

activated features (semantic and perceptual for the word–

sound pairing, respectively), thus failing to engender an

amplitude reduction in the novelty P3.

An alternative, but not necessarily contradictory, hypoth-

esis is that the sound in the word1–sound2 pairing does not

contain sufficient information to contact the stored repre-

sentation of the previously heard verbal label. This could be

due to the presumed slowed processing required by the

necessity to incorporate both the perceptual and semantic

characteristics inherent in the sound (see above). Or it could

be due to the possibility that the short durations of the

current sounds did not enable sufficient semantic informa-

tion to be extracted. In either case, the end result would be

the same—a failure to activate the stored representation of

the verbal concept.

Some evidence for these different viewpoints comes

from behavioral studies of environmental sound priming,

although the underlying mechanisms involved may be quite

different from those recruited in the novelty oddball para-

digm presented here. For example, Chiu and Schacter [3]

failed to find cross-form priming in a condition in which

sound labels were studied and sound fragments (the first

second of a 5-s sound) were used as test items. When the

verbal label and the sound were presented together during

the study phase, robust priming by the sound fragment at

test was observed. Similarly, Stuart and Jones [29] reported

that identification of an environmental sound was facilitated

by the repeated presentation of the same sound but not by

the previous presentation of its verbal label.

Although the database on non-linguistic sounds is not

nearly as large as that for verbal stimuli, there is some

evidence suggesting similar processing mechanisms for both

sounds and words. For example, sound familiarity is one

determinant of sound identification, in that commonly heard

sounds are easier to identify than less commonly heard

D. Friedman et al. / Cognitive Brain Research 18 (2003) 58–64 63

sounds [1], an effect that is similar to word frequency. Stuart

and Jones [29] demonstrated an analogy to the word

repetition priming effect using environmental sound stimuli

by demonstrating that the identification of environmental

sounds was facilitated by previous exposure to the same

sound (see also below). Furthermore, Van Petten and

Rheinfelder [30], who used meaningful non-speech sounds

and conceptually related words, demonstrated cross-form

priming of both words and sounds regardless of whether the

non-speech sound or its verbal conceptual equivalent served

as prime or target.

However, although repetition of conceptually similar

items is common to the current novelty oddball investiga-

tion and the sound priming studies mentioned above, there

are key elements that distinguish the two: (1) in the

current investigation, cross-form conceptual repetition oc-

curred at intervals longer than those typically employed in

semantic priming studies (respectively, approximately after

a 3-min lag contrasted with only a few sec); and (2) cross-

form conceptual repetitions occurred within the context of

a novelty oddball task (not a typical semantic priming

paradigm), in which subjects had to detect the infrequent

occurrence of a target event and were not expecting (at

least initially) environmental sounds and their verbal

counterparts. Typically, in behavioral studies of semantic

priming, facilitation in reaction time is short-lived relative

to repetition priming, surviving prime–target intervals of

only a few seconds [9]. Furthermore, the major effect of

semantic priming in ERP studies is to reduce the ampli-

tude of the N400 component [26], an ERP waveform

peaking at approximately 400 ms, about 100 ms later than

the novelty P3 (see Ref. [22]). Together, these findings

suggest that the reductions in amplitude of the novelty P3

observed here reflect an earlier and fundamentally different

mechanism than those observed in semantic priming

studies.

Based on a variety of evidence, the putative neural

mechanism(s) underlying the novelty P3 appears to be

localized to the prefrontal cortex. These studies demonstrate

that the novelty P3 is reduced in patients with dorsolateral

prefrontal lesions when compared to normal controls [8,16],

or patients with lesions elsewhere within the brain [18].

Additional evidence for a prefrontal cortical contribution to

this component comes from intracranial ERP investigations

[2], current source density mapping studies of surface

recorded activity [11,27] and event-related fMRI studies

(see Refs. [17,13] for a review of the latter).

Friedman et al. [13] have argued that the novelty P3 does

not reflect the detection of the deviant event per se, but

rather processes that are activated after the deviant event has

been detected, for example, bringing the event to conscious-

ness for evaluation of its salience and appropriate action. In

the current data, the reduction of the novelty P3 when the

initially presented sound concept is repeated as a verbal

label is consistent with this hypothesis, as processes sub-

sumed under orienting should be called upon to a lesser

extent once a representation of the event has been formed.

The environmental sounds used here are most likely repre-

sented in semantic memory networks similar to those

observed for words and pictures. Although the data are very

limited, some support for this contention has been provided

by experiments in which similar environmental sounds are

embedded within semantic priming and repetition priming

tasks as described earlier for both behavioral [3,29] and ERP

[30] investigations. However, a more complete neurocogni-

tive picture and more definitive conclusions will emerge

only with additional research effort.

Acknowledgements

The research reported here was supported in part by grant

HD14959 (DF) and HD37193 (YMC) from NIH and by the

New York State Department of Mental Hygiene. We thank

Charles L. Brown III for computer programming and

technical assistance, Mr. Martin Duff for technical assistance

and all of the volunteers for generously giving their time.

References

[1] J.A. Ballas, Common factors in the identification of an assortment of

brief everyday sounds, Journal of Experimental Psychology: Human

Perception and Performance 19 (1993) 250–267.

[2] P. Baudena, E. Halgren, G. Heit, J.M. Clarke, Intracerebral potentials

to rare target and distractor auditory and visual stimuli: III. Frontal

cortex, Electroencephalography and Clinical Neurophysiology 94

(1995) 251–264.

[3] C. Chiu, D. Schacter, Auditory priming for nonverbal information:

implicit and explicit memory for environmental sounds, Conscious-

ness and Cognition 4 (1995) 440–458.

[4] E. Courchesne, S.A. Hillyard, R. Galambos, Stimulus novelty, task

relevance, and the visual evoked potential in man, Electroencephalog-

raphy and clinical Neurophysiology 39 (1975) 131–143.

[5] Y.M. Cycowicz, D. Friedman, A developmental study of the effect of

temporal order on the ERPs elicited by novel environmental sounds,

Electroencephalography and clinical Neurophysiology 103 (1997)

304–318.

[6] Y.M. Cycowicz, D. Friedman, Effect of sound familiarity on the

event-related potentials elicited by novel environmental sounds, Brain

and Cognition 36 (1998) 30–51.

[7] Y.M. Cycowicz, D. Friedman, M. Rothstein, An ERP developmental

study of repetition priming by auditory novel stimuli, Psychophysi-

ology 33 (1996) 680–690.

[8] K.R. Daffner, M.M. Mesulam, L.F.M. Scinto, D. Acar, V. Calvo, R.

Fausti, A. Chabrerie, B. Kennedy, P. Holcomb, The central role of the

prefrontal cortex in directing attention to novel events, Brain 123

(2000) 927–939.

[9] G.L. Dannenbring, K. Briand, Semantic priming and the word repe-

tition effect in a lexical decision task, Canadian Journal of Psychology

36 (1982) 435–444.

[10] C. Escera, K. Alho, I. Winkler, R. Naatanen, Neural mechanisms of

involuntary attention to acoustic novelty and change, Journal of Cog-

nitive Neuroscience 10 (1998) 590–604.

[11] M. Fabiani, D. Friedman, Changes in brain activity patterns in aging:

the novelty oddball, Psychophysiology 32 (1995) 579–594.

[12] D. Friedman, G.V. Simpson, ERP amplitude and scalp distribution

to target and novel events: effects of temporal order in young,

D. Friedman et al. / Cognitive Brain Research 18 (2003) 58–6464

middle-aged and older adults, Cognitive Brain Research 2 (1994)

49–63.

[13] D. Friedman, Y.M. Cycowicz, H. Gaeta, The novelty P3: an event-

related brain potential (ERP) sign of the brain’s evaluation of novelty,

Neuroscience and Biobehavioural Reviews 25 (2001) 355–373.

[14] G. Gratton, M.G.H. Coles, E. Donchin, A new method for off-line

removal of ocular artifact, Electroencephalography and Clinical Neu-

rophysiology 55 (1983) 468–484.

[15] J.R. Jennings, C.C. Wood, The q-adjustment procedure for repeated

measures analyses of variance, Psychophysiology 13 (1976) 277–278.

[16] R.T. Knight, Decreased response to novel stimuli after prefrontal

lesions in man, Electroencephalography and Clinical Neurophysiol-

ogy 59 (1984) 9–20.

[17] R.T. Knight, Attention, temporal processing and the human prefrontal

syndrome, Eighth International Conference on Cognitive Neuro-

science, Porquerolles Island, France, 2002.

[18] R.T. Knight, D. Scabini, D.L. Woods, C.C. Calyworth, Contributions

of temporal–parietal junction to the human auditory P3, Brain Re-

search 502 (1989) 109–116.

[19] R. Lynn, Attention, Arousal and the Orientation Reaction, Pergamon,

London, 1966, p. 118.

[20] G. McCarthy, C.C. Wood, Scalp distributions of event-related po-

tentials: an ambiguity associated with analysis of variance models,

Electroencephalography and Clinical Neurophysiology 62 (1985)

203–208.

[21] M.R. Nuwer, D. Lehmann, F. Lopes da Silva, S. Matsuoka, W. Su-

therling, J.F. Vibert, IFCN guidelines for topographic and frequency

analysis of EEGs and EPs. Report of an IFCN committee. Interna-

tional Federation of Clinical Neurophysiology, Electroencephalogra-

phy and Clinical Neurophysiology 91 (1994) 1–5.

[22] B. Opitz, A. Mecklinger, A.D. Friederici, D.Y. von Cramon, The

functional neuroanatomy of novelty processing: integrating ERP

and fMRI results, Cerebral Cortex 9 (1999) 379–391.

[23] A. Paivio, Mental Representations: A Dual Coding Approach, Oxford

Univ. Press, New York, 1986.

[24] F. Perrin, J. Pernier, O. Bertrand, J.F. Echallier, Spherical splines for

scalp potential and current density mapping, Electroencephalography

and Clinical Neurophysiology 72 (1989) 184–187.

[25] D.S. Ruchkin, R. Johnson Jr., D. Friedman, Scaling is necessary

when making comparisons between shapes of event-related potential

topographies: a reply to Haig et al., Psychophysiology 36 (1999)

832–834.

[26] M.D. Rugg, The effects of semantic priming and word repetition on

event-related potentials, Psychophysiology 22 (1985) 642–647.

[27] E. Schroger, M.-H. Giard, C. Wolff, Auditory distraction: event-re-

lated potential and behavioral indices, Clinical Neurophysiology 111

(2000) 1450–1460.

[28] E.N. Sokolov, The orienting response, and future directions of its

development, Pavlovian Journal of Biological Science 25 (1990)

142–150.

[29] G.P. Stuart, D.M. Jones, Priming the identification of environmental

sounds, The Quarterly Journal of Experimental Psychology 48A

(1995) 741–761.

[30] C. Van-Petten, H. Rheinfelder, Conceptual relationships between spo-

ken words and environmental sounds: event-related brain potential

measures, Neuropsychologia 33 (1995) 485–508.

[31] E. Yago, C. Escera, K. Alho, M.H. Giard, J.M. Serra-Grabulosa,

Spatiotemporal dynamics of the auditory novelty-P3 event-related

brain potential, Cognitive Brain Research 16 (2003) 383–390.