neural correlates of auditory repetition priming: reduced fmri activation in the auditory cortex

Neural Correlates of Auditory Repetition Priming:Reduced fMRI Activation in the Auditory Cortex

Dafna Bergerbest, Dara G. Ghahremani, and John D. E. Gabrieli

Abstract

& Repetition priming refers to enhanced or biased perform-ance with repeatedly presented stimuli. Modality-specificperceptual repetition priming has been demonstrated behav-iorally for both visually and auditorily presented stimuli. Infunctional neuroimaging studies, repetition of visual stimuli hasresulted in reduced activation in the visual cortex, as well as inmultimodal frontal and temporal regions. The reductions insensory cortices are thought to reflect plasticity in modality-specific neocortex. Unexpectedly, repetition of auditory stimulihas resulted in reduced activation in multimodal and visualregions, but not in the auditory temporal lobe cortex. Thisfinding puts the coupling of perceptual priming and modality-specific cortical plasticity into question. Here, functionalmagnetic resonance imaging was used with environmental

sounds to reexamine whether auditory priming is associatedwith reduced activation in the auditory cortex. Participantsheard environmental sounds (e.g., animals, machines, musicalinstruments, etc.) in blocks, alternating between initial andrepeated presentations, and decided whether or not eachsound was produced by an animal. Repeated versus initialpresentations of sounds resulted in repetition priming (fasterresponses) and reduced activation in the right superiortemporal gyrus, bilateral superior temporal sulci, and rightinferior prefrontal cortex. The magnitude of behavioral primingcorrelated positively with reduced activation in these regions.This indicates that priming for environmental sounds is asso-ciated with modification of neural activation in modality-specificauditory cortex, as well as in multimodal areas. &

INTRODUCTION

Repetition priming refers to enhanced or biased perfor-mance with repeated presentation of a stimulus. It isclassified as a form of implicit memory because primingis dissociable from performance in explicit memorytests, such as recall or recognition, where participantsare explicitly asked to recollect previously presenteditems from memory (Schacter, 1987; Graf & Schacter,1985). Two lines of evidence suggest that repetitionpriming depends upon different brain structures andmemory processes than does explicit memory. First,amnesic patients with medial temporal lobe or dience-phalic damage show intact priming on implicit memorytests despite impaired explicit memory (reviewed inGabrieli, 1998; Moscovitch, Vriezen, & Goshen-Gottstein,1993). Second, performance on explicit tests in normalpopulations has been dissociated from performance onimplicit tests (reviewed in Roediger & McDermott, 1993).

Repetition priming appears to reflect modification ofneural activity in the neocortex (Schacter, 1992; Tulving& Schacter, 1990). There are different kinds of repetitionpriming, and a fundamental distinction has been madebetween perceptual priming, which is related to the

physical properties of a stimulus, and conceptualpriming, which is related to the amodal meaning ofthe stimulus (Gabrieli, 1998; Schacter & Buckner,1998). Thus, unlike performance on explicit or concep-tual implicit tests, perceptual repetition priming is re-duced or even eliminated when modality of stimuluspresentation (e.g., auditory or visual; Pilotti, Bergman,Gallo, Sommers & Roediger, 2000; McClelland & Pring,1991; Bassili, Smith, & MacLeod, 1989; Jackson & Mor-ton, 1984; Ellis, 1982) or form-specific characteristics(e.g., voice of speaker; Pilotti et al., 2000; Sommers,1999; Church & Schacter, 1994; Schacter & Church,1992) are changed between study and test. The percep-tual basis of repetition priming in the brain is supportedby reports of diminished visual perceptual priming inpatients with focal damage to the occipital cortex (e.g.,Gabrieli, Fleischman, Keane, Reminger, & Morrell, 1995)and by functional imaging studies demonstrating thatrepeated presentation of visual stimuli is accompaniedby reduced activation in visual processing areas, such asthe extrastriate cortex, along with reductions in amodalregions, such as the inferior prefrontal cortex (e.g.,Koutstaal et al., 2000; Wagner, Koutstaal, Maril, Schacter,& Buckner, 2000; Buckner et al., 1998; Wagner, Des-mond, Demb, Glover, & Gabrieli, 1997; Demb et al.,1995). Thus, it has been thought that perceptual primingreflects plasticity in modality-specific neocortex.Stanford University

D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:6, pp. 966–977

Unexpectedly, for auditory stimuli, repetition-relatedreductions have not been demonstrated yet in theauditory cortex. Thus, although perceptually specificauditory priming has been demonstrated behaviorallyfor auditory stimuli (Pilotti et al., 2000; Sommers, 1999;Church & Schacter, 1994; Schacter & Church, 1992;McClelland & Pring, 1991; Bassili et al., 1989; Jackson &Morton, 1984; Ellis, 1982), repetition of auditorily pre-sented words has resulted in reductions in amodalfrontal regions, and even in visual processing regions,but not in the modality-specific auditory cortex (Buck-ner, Koutstaal, Schacter, & Rosen, 2000; Badgaiyan,Schacter, & Alpert, 1999, 2001). Moreover, the only studythat sought repetition-related reductions to auditorystimuli other than words mainly aimed at demonstratingthe brain correlates of explicit memory for environmen-tal sounds (Wheeler, Petersen, & Buckner, 2000). Thisstudy included a subgroup of six participants who per-formed a perceptual task on new and repeated sounds.This produced only nonsignificant reductions for repeat-ed sounds in the superior temporal gyrus. The failure todemonstrate a significant relation between auditorypriming and reduced activation in auditory regions ren-ders uncertain the theory that perceptual priming in-vokes modality-specific plasticity in the human brain.

The lack of evidence for repetition-related reductionsin the auditory cortex could have resulted from the factthat most of the studies that queried repetition-relatedreductions (Buckner et al., 2000; Badgaiyan et al., 1999)used the word-stem completion task. It is possible thatpriming on the auditory word-stem completion task, oreven other auditory word-priming tasks, relies moreheavily on phonological representations than of acousticrepresentations (for the suggestion that acoustic andphonological features of spoken words are stored inanatomically distinct memory systems, see Sommers,1999; Schacter, 1994). With this in mind, we chose todemonstrate repetition-related reductions in the audi-tory cortex using environmental sounds, stimuli whoseprocessing may rely more heavily on acoustic/auditoryrepresentations. Prior behavioral studies document thatrepetition priming for environmental sounds reflectsauditory-perceptual processes rather than amodal-conceptual processes. Hearing or seeing sound namesdid not result in significant cross-modal priming inenvironmental-sound identification tasks (Chiu &Schacter, 1995; Stuart & Jones, 1995). Moreover, semantic(e.g., judgment of frequency-of-occurrence in everydaylife) and nonsemantic (e.g., pitch judgment) encodingtasks led to equivalent levels of auditory priming (Chiu& Schacter, 1995), suggesting that the priming effectfor sounds in these studies relied on the perceptualprocessing of the sounds rather than the conceptualprocessing of their meaning. Finally, repetition of anidentical exemplar sound led to greater priming thandid exposure to a different exemplar (Chiu, 2000; butsee, Stuart & Jones, 1995). This shows that priming

reflects processing of stimulus-specific auditory informa-tion (i.e., priming is associated with the precise auditoryproperties of the stimulus). These findings support theexistence of auditory sound representations, such asword- and object-form representations, that preservemodality-specific stimulus information in memory (Chiu,2000; Schacter, 1994). Repetition-related reductions inauditory regions may reflect plasticity in environmental-sound representations.

In the present study, we used functional magneticresonance imaging (fMRI) to examine whether auditorypriming is associated with reduced activation in theauditory cortex as predicted by its perceptual nature.Participants heard environmental sounds in blocks ofinitial and repeated presentations and performed asound categorization task. Because previous studies ofauditory priming failed to find repetition-related reduc-tions in auditory regions (Buckner et al., 2000; Wheeleret al., 2000; Badgaiyan et al., 1999, 2001), we used ablocked design to maximize the power to find repeti-tion-related reductions in auditory regions.

RESULTS

Behavioral Results

Due to a technical failure of the response box, thebehavioral results of one participant were not recorded.Therefore, behavioral results refer to 13 of the 14participants. Participants responded to most of thesounds (mean = 0.98, SEM = 0.012) and were moder-ately accurate in deciding whether or not sounds weregenerated by an animal (mean = 0.84, SEM = 0.012).Most errors seemed to reflect reasonable alternativeinterpretations of some ambiguous sounds, rather thanfailures of attention. This interpretation was supportedby an analysis of the consistency between the first andsecond decisions for each sound. The consistency be-tween first and second responses (in cases in which bothwere recorded) was high (mean = 0.91, SEM = 0.012).

The critical measure was that of repetition priming,and such priming was evident by both latency andaccuracy analyses. Participants were 97 msec faster torespond to repeated presentations (mean = 1167 msec,SEM = 39.52) than to initial presentation of sounds[mean = 1264 msec, SEM = 50.09; t(12) = 5.82, p <.0001]. Participants were also more accurate in responseto repeated (mean = .96, SEM = .006) than to initialsound presentation [mean = 0.94, SEM = 0.007; t(12) =3.73, p = .003].

Imaging Results

Three types of analyses were performed to characterizethe activation changes associated with repetition prim-ing. First, we contrasted initial and repeated sound

Bergerbest, Ghahremani, and Gabrieli 967

presentations to reveal regions that showed reducedactivation for repeated presentation. Second, we func-tionally defined regions involved in auditory processingof environmental sounds by contrasting activations forenvironmental sounds versus scanner noise in a sepa-rate localizer scan, in which participants alternatedbetween listening to blocks of environmental sounds,blocks of simple tones, and blocks of scanner noisealone. Then, we queried whether regions that showedreduced activation were within the regions that wereindependently identified as responding to environmen-tal sounds. Finally, we examined correlations betweenthe magnitude of activation reductions for repeatedsounds in the regions of interest (ROIs) derived fromthe above analyses and the magnitude of behavioralpriming.

Regions Showing Reduced Activation

Blocks of repeated sound presentations showed re-duced activation, as compared to initial sound presen-tation, mainly in the right superior temporal gyrus (STG;BA 22), bilaterally in the superior temporal sulci (STS;BA 22), in the right inferior prefrontal cortex (RIPC; BA47/45), and in the right putamen (p< .001, uncorrected;see Figure 1 and Table 1). The cluster in the STG waslateral and posterior to Heschl’s gyrus (primary auditorycortex; see Figure 2 for two representative participants).The clusters in the STS were focused in two regions, oneposterior to Heschl’s gyrus and the other in the tempo-ral pole. Regions demonstrating increased activationfor repeated versus initial sound presentation includedthe bilateral fusiform gyri (BA 19), bilateral precuneus(BA 7/31), and left middle frontal gyrus (BA 10; Table 2).

To confirm that the priming-related reductions inactivation were occurring in regions that are involvedin auditory processing, regions were defined thatshowed greater response to environmental sounds thanbackground scanner noise in the separate localizer scan(blocks of simple tones were not included in this or anyother analyses reported in this study). These regionsincluded areas in the STG/STS bilaterally, right inferiorfrontal gyrus, left middle frontal gyrus, and medialfrontal gyrus (Table 3). Although regions of activationin the STG/STS were bilateral, the volume of activationwas larger on the right than on the left side [t(13) =3.23, p = .007].

A conjunction analysis demonstrated that regions inthe STG/STS that showed reduced activation for repeat-ed sounds were mostly a subset of the regions that wereactivated by environmental sounds in the localizer scan(Figure 3, Table 4). The only region in the STS thatshowed no overlap with regions that were active forenvironmental sounds was a region in the left anteriorSTS (see Table 1). The only other overlap betweenregions that showed reduced activation for repeatedsounds and regions that were active for environmentalsounds was in the right inferior frontal gyrus (BA 47).

Correlation between Reduction in Activation andBehavioral Priming

In an ROI analysis, we examined the relations, acrossparticipants, between the magnitude of behavioral prim-ing and the magnitude of repetition-related reduction inactivation within the ROIs defined by the auditorylocalizer (Figure 4). The magnitude of reduction in acti-vation correlated positively with behavioral priming inthe right [r= .70, F(1,12) = 10.47, p= .008] and left STG[r= .69, F(1,12) = 10.03, p= .009], right anterior inferiorprefrontal gyrus [r = .68, F(1,12) = 9.31, p = .01], rightposterior inferior prefrontal gyrus [r = .72, F(1,12) =12.13, p = .005], medial frontal gyrus [r = .68, F(1,12) =9.97,p=.01], left precentral gyrus [r=.58,F(1,12)=5.65,p= .04], right putamen [r= .67, F(1,12) = 8.82, p= .01],and left claustrum [r= .64, F(1,12) = 7.83, p= .02].

DISCUSSION

Repetition priming for environmental sounds was asso-ciated with reduced activation in auditory regions in theright STG (BA 22), bilateral regions in the anterior andposterior STS (BA 22), right inferior prefrontal gyrus (BA47/45), and right putamen. Regions of the STG, STS, andRIPC that showed repetition-related reductions partlyoverlapped with regions that were activated by environ-mental sounds. Moreover, behavioral priming correlatedwith repetition-related reductions in both the right andleft superior temporal cortex as well as in the frontalregions. Such a cross-participant correlation betweenmemory performance and activation increases has been

Figure 1. Statistical activation maps for group data showing regions ofsignificantly greater activity for initial compared to repeated soundpresentation in the auditory priming scans (superimposed over groupaverage structural brain images, using a threshold of p = .001,uncorrected). These regions included (a) the right STG, (b) thebilateral posterior STS, (c) the bilateral anterior STS, (d) the rightinferior frontal gyrus, and (e) the anterior part of the left insula. L, left;R, right.

968 Journal of Cognitive Neuroscience Volume 16, Number 6

demonstrated previously for explicit memory (e.g., Ha-mann, Ely, Grafton, & Kilts, 1999; Alkire, Haier, Fallon, &Cahill, 1998; Cahill et al., 1996; Nyberg, McIntosh, Houle,Nilsson, & Tulving, 1996), but to our knowledge, this isthe first observation of such a quantitative link betweenthe magnitudes of repetition priming and activationreduction. These findings demonstrate that modality-specific repetition priming occurs in a modality otherthan vision. As such, they support the idea that modality-specific repetition priming is mediated, at least in part,by reduced activation in the corresponding modality-specific neocortex.

Our findings converge with those in an anatomicallyconstrained magnetoencephalography (aMEG) studyexamining the temporal dynamics of word processingand repetition effects for auditorily and visually pre-sented words (Marinkovic et al., 2003). In that experi-ment, words were seen or heard six times during study,and repeated 39 times during MEG measurement. Re-peated, relative to novel, auditorily presented wordsyielded early differences (225–250 msec) focused inthe superior temporal plane, superior temporal sulcus,and the temporopolar area. Later repetition effects(300–500 msec) included also supramodal regions suchas anterior temporal and inferior prefrontal regions.This MEG study and our fMRI study converge in point-ing to the superior temporal region as showing reducedresponses to repeated auditory stimuli. To maximize thepower to find repetition-related fMRI activation in audi-tory regions, sounds were presented in blocks of initialand repeated presentation. Such blocked designs havethe limitation that they cannot distinguish betweenphasic item-specific effects and tonic block effects

(e.g., differential attention; Buckner & Logan, 2001). Inthe domain of repetition priming, however, blocked andmixed event-related designs have yielded nearly identi-cal findings. For example, visual priming in blocked(Wagner et al., 1997; Demb et al., 1995) and event-related (Buckner et al., 1998) designs have yieldednearly identical results. Only an event-related auditorypriming study can establish this point with certainty, butthe prior literature supports the view that the priming-related reductions in the present study would occur ineither sort of design.

The present study focused on repetition-related re-ductions in an implicit memory test, but it is likely thatincidental explicit memory processes were engaged in

Table 1. Maxima within Regions Demonstrating BOLD Signal Changes When Contrasting Initial > Repeated Sound Presentation

Talairach Coordinates

Region of Activation Left/Right BAa x y z t value Volumeb

Superior temporal gyrus R 22 53 !19 5 4.94 96

Superior temporal sulcus R 22 46 !40 9 6.08 208

R 22 51 !10 !10 6.60 176

L 22 !61 !31 5 4.54 176

L 22 !42 3 !20 4.30 80

Inferior frontal gyrus R 47/45 42 21 !1 6.55 960

Insula L 13 !30 23 !1 5.37 144

Anterior cingulate R 32/24 6 23 28 6.20 176

Putamen R 12 10 !4 5.25 592

Red nucleus L/R !2 !24 !6 4.37 144

Hypothalamus R 8 !2 !10 4.36 80

aBrodmann’s area.bVolume reported in mm3.

Figure 2. Statistical activation maps showing regions of significantlygreater activity for initial compared to repeated sound presentation inthe auditory priming scans for two participants (spatially unnormalizeddata superimposed over individual structural brain images, using athreshold of p = .001, uncorrected). The right nonprimary auditorycortex is activated for both participants (marked with a cross hair).


this experiment. In fact, upon query at the end of theexperiment, participants reported that they becameaware of sound repetition at some point during theexperiment. This awareness may be the behavioral cor-relate of the increased activation for repeated blocks thatwas found, among other regions, in the bilateral precu-neus (BA 7/31) and the left middle frontal gyrus (BA 10).Increased activation for repeated stimuli in these regionshas been reported for old relative to new items in explicitmemory tests (e.g., Donaldson, Petersen, & Buckner,2001; Konishi, Wheeler, Donaldson, & Buckner, 2000;McDermott, Jones, Petersen, Lageman, & Roediger, 2000;

Henson, Rugg, Shallice, Josephs, & Dolan, 1999). There-fore, it is plausible that the increased activation in theseregions reflects explicit recognition of item repetition.However, the fact that auditory regions showed reduc-tions in activation, rather than increases in activationassociated with explicit memory for environmentalsounds (Nyberg, Habib, McIntosh, & Tulving, 2000;Wheeler et al., 2000), suggests that these regions wereinvolved in auditory priming. A similar pattern of repeti-tion-related decreases and increases in activation (pre-cuneus and left middle frontal among other regions) wasreported in two studies that used implicit memory tasks

Table 2. Maxima within Regions Demonstrating BOLD Signal Changes When Contrasting Repeated > Initial Sound Presentation



Fusiform gyrus L 19 !24 !74 !13 6.37 528

R 19 28 !61 !10 5.25 256

R 19 32 !78 !10 4.62 96

Precuneus R 7 12 !62 36 5.33 240

R 31 16 !57 21 5.11 112

L 7 !26 !52 54 4.45 96

L 31 !10 !69 26 4.23 128

Middle frontal gyrus L 10 !32 54 !6 6.25 240

Precentral gyrus L 4 !59 !7 22 5.18 176

Frontal subgyral R 22 !17 52 4.77 96

Claustrum R 32 !13 12 4.98 96


Table 3. Maxima within Regions Demonstrating BOLD Signal Changes When Contrasting Environmental Sounds > Scanner Noise



Superior temporal gyrus R 41/42/22/38 48 !23 9 13.26 19,088

L 41/42/22/38 !44 !29 9 11.05 15,536

Inferior frontal gyrus R 47 48 27 !8 5.67 1424

R 9 44 11 29 6.09 1264

Medial frontal gyrus L/R 8 !2 20 43 6.52 1008

Middle frontal gyrus L 46 !40 16 18 6.23 832

Precentral gyrus L 6 !38 3 29 4.90 416

Putamen R 28 0 !7 5.17 368

Claustrum L !28 10 !4 5.57 368



(Donaldson, Petersen, & Buckner, 2001; Koutstaal et al.,2000). Donaldson, Petersen, and Buckner (2001) sug-gested that participants may have experienced somelevel of explicit memory while performing the implicitmemory task. This may hold true for our participants aswell. For participants with normal memory, incidentalexplicit memory for item repetition likely occurs inparallel with implicit memory in most repetition primingstudies. Importantly, Donaldson et al. showed that areasexhibiting reduced activation for priming were distinctfrom those that showed enhanced activation for explicitmemory. Thus, incidental explicit memory is not associ-ated with the sort of priming-driven reductions observedin the present study.

Repetition Priming—The Caseof the Auditory Cortex

Few imaging studies have used auditory stimuli inmeasuring the brain correlate of repetition priming inimplicit memory tests (Buckner et al., 2000; Wheeleret al., 2000; Badgaiyan et al., 1999, 2001). None of thesestudies found significant reductions in activation in theauditory cortex (a possible reduction in an explicitmemory test is reported in Tulving et al., 1994). Givenclear behavioral evidence that auditory word-stem com-pletion priming is perceptually specific (Pilotti et al.,2000; Sommers, 1999; Church & Schacter, 1994;Schacter & Church, 1992; McClelland & Pring, 1991;Bassili et al., 1989; Jackson & Morton, 1984; Ellis,1982), it is unclear why the prior studies failed to revealmodulation of auditory cortical areas. As suggested inthe Introduction, word-stem completion has more in-volvement of lexical and phonological systems, whereasenvironmental sounds may be processed in a morepurely acoustic or auditory fashion. This greater depen-dence on auditory representations may have enhancedthe activation reduction in auditory regions in our study.

The temporal regions that showed reduced activationare considered part of the secondary (nonprimary)auditory cortex. Studies with primates (e.g., Rauscheck-er, Tian, & Hauser, 1995) and humans (e.g., Wallace,Johnston, & Palmer, 2002; Wessinger et al., 2001; Rivier& Clarke, 1997; for a review, see Hall, Hart, & Johnsrude,2003) define belt regions surrounding the primary audi-tory cortex on the supratemporal plane as nonprimaryauditory cortex. The right STG region activated in thepresent study corresponds to one of the six nonprimaryareas that have been defined on the basis of theirlaminar structure (the lateral area; Rivier & Clarke,1997; although individual participants showed also otherregions). In contrast, the auditory nature of regions inthe STS that showed repetition-related reductions is lessclear because anatomical studies in primates have shownthat the STS is composed of several uni- and multimodal

Figure 3. Statistical activation maps showing regions of greateractivity for environmental sounds compared to scanner noise in thelocalizer scan (in blue), regions of greater activity for initial comparedto repeated sound presentation (in yellow), and regions that overlap(in green; superimposed over average structural brain images, usinga threshold of p = .001, uncorrected), centered at (A) the right STG(53, !21, 4) and (B) the RIPC (41, 23, !4).

Table 4. Maxima within Regions Demonstrating BOLD Signal Changes in a Conjunction Analysis of Regions That Were ActivatedFor Initial Versus Repeated Sound Presentation and Environmental Sounds Versus Scanner Noise



Superior temporal gyrus R 22 53 !19 5 4.94 96

Superior temporal sulcus R 22 46 !40 9 6.08 160

R 22 51 !12 !6 4.62 112

L 22 !61 !31 5 4.54 160

Inferior frontal gyrus R 47/45 38 27 !5 6.50 288



areas (reviewed in Kaas & Hackett, 2000). In humans,activations along the STS were reported in imagingstudies of speech and voice processing (Belin, Zatorre,Lafaille, Ahad, & Pike, 2000; Belin, Zatorre, & Ahad,2002; Binder et al., 2000) and environmental soundprocessing (Adams & Janata, 2002; Giraud & Price,2001) in STS regions similar to ours. This suggests thatregions in the STS that showed reduced activation areindeed auditory regions. Thus, the auditory primingassociated reductions appear to have occurred in non-primary auditory cortices just as visual priming has beenrelated to reductions in nonprimary visual cortices (e.g.,Buckner et al., 1998).

Although we have focused on repetition-related re-ductions in the auditory cortex as a correlate of behav-ioral repetition priming, other regions correlated withpriming as well. These areas may all offer potentialsources of repetition priming involving more than plas-ticity in modality-specific regions. For example, thecorrelation between behavioral priming and repetition-related reduction in activation in the RIPC could berelated to recapitulation of semantic processing in addi-tion to recapitulation of perceptual processing. More-over, because the same classification decision was madefor both initial and repeated presentations, the primingeffects observed may be partially related to repetition ofstimulus–response associations, not only repetition ofthe stimulus per se. The other regions that correlatedwith behavioral priming may be involved in generatingthese associations during initial presentations and rein-voking them during repetition. The similar magnitudes

of correlation for the various regions suggest a functionalnetwork underlying the priming. For example, Buckneret al. (2000) suggested that reductions in posteriorregions during repetition priming could be the result ofa top-down modulation by frontal regions. However,because fMRI has limited temporal resolution, it is diffi-cult to determine causal relationships between activity indifferent regions. Therefore, the present findings do notallow for a more specific characterization of what pro-cesses are mediated by each of the multiple brain regionsthat showed reduced activation and also a correlationbetween the magnitudes of activation and priming.

The Role of the Two Temporal Lobes in ProcessingEnvironmental Sounds

In the present study, regions in the STG were bilaterallyactivated by environmental sounds, but the region ofactivation was larger on the right STG. Repetition-relatedreduction was bilateral in the STS, but right-lateralized inthe STG. Thus, our results suggest that environmental-sound representation in the auditory cortex is relativelyright-lateralized. The design of the present study pre-cludes a differentiation of right- and left-lateralizedauditory activations, but the findings are consistent withevidence that (a) there is right-lateralized dominance forthe processing of environmental sounds, and that (b)there is also a left-lateralized contribution to the seman-tic analysis of environmental sounds. Dichotic listeningstudies indicate a left ear/right hemisphere superiorityfor recognizing environmental sounds (e.g., Curry,

Figure 4. Statistical activationmaps showing regions ofsignificantly greater activity forenvironmental soundscompared to scanner noisein the localizer scan(superimposed over averagestructural brain images, usinga threshold of p = .001,uncorrected) and theregression between behavioralpriming and reduction inactivity within these regions.


1967), and a study that combined dichotic listening withbrain imaging demonstrated that the left ear advantagefor musical instrument sounds corresponds to right-lateralized activation in the STG (Hugdahl et al., 1999).

Neuropsychological research of auditory agnosia, aneurological disorder characterized by a deficit in rec-ognizing sounds despite normal hearing as measured bystandard audiometry, suggests that both hemispheresare involved in sound processing but that they playdifferent roles in that processing. Auditory agnosia fornonverbal material can occur with spared verbal com-prehension, following bilateral or right hemisphere le-sions, or in association with auditory agnosia for verbalmaterial in cases of bilateral or left hemisphere lesions(for reviews, see Saygin, Dick, Wilson, Dronkers, &Bates, 2003; Clarke, Bellmann, De Ribaupierre, & Assal,1996; Clarke, Bellmann, Meuli, Assal, & Steck, 2000).Patients with right hemisphere lesions have difficultydiscriminating between acoustically related sounds,whereas patients with left hemisphere lesions tend toconfuse the actual source of a sound with a semanticallyrelated source (Schnider, Benson, Alexander, & Schnider-Klaus, 1994; Faglioni, Spinnler, & Vignolo, 1969; Vignolo,1969, 1982). These findings led Vignolo (1982) to sug-gest the existence of two forms of auditory agnosia—aperceptual-discriminative form associated mainly withright hemispheric lesions and an associative-semanticform associated mainly with left hemispheric lesions.Support for this idea comes also from a PET studyreporting greater right than left STG activation forpassive listening for sounds, but left-lateralized activa-tion in prefrontal and middle temporal regions forsemantic categorization of the sounds (Engelien et al.,1995). Thus, the left and right temporal lobe activationsin the present study may reflect different kinds ofauditory processing.

The Role of the RIPC in ProcessingEnvironmental Sounds

In the present study, the RIPC showed reduced activa-tion for repeated sounds. Moreover, reduced activationin the RIPC region that was active for sounds wascorrelated with behavioral priming. Reduced activationin the inferior prefrontal cortex in repetition primingstudies is usually left-lateralized for verbal material (e.g.,Buckner et al., 1998; Wagner et al., 1997, 2000). How-ever, these studies that demonstrated repetition-relatedreductions used words. Repeated presentations of non-verbal visual material result in reduced right frontalactivation (Golby et al., 2001; Kirchhoff, Wagner, Maril& Stern, 2000; Gabrieli, Brewer, Desmond, & Glover,1997). Here, we demonstrated the involvement ofthe RIPC for repetition priming of nonverbal auditorymaterial.

Reduced RIPC activity for repeated sounds is in linewith several studies that demonstrated the involvement

of the RIPC in tasks of auditory working memory (Za-torre, Evans, & Meyer, 1994; Zatorre & Samson, 1991; fora review, see Zatorre, 2001; for bilateral activation in aname verification task for sounds, see Adams & Janata,2002). Moreover, a PET study by Zatorre, Evans, Meyer,and Gjedde (1992) demonstrated that laterality of activ-ity in the inferior prefrontal cortex depends on whetherphonological or acoustic processing is required. Makingphonetic judgments about a speech signal led to activa-tion in the left prefrontal cortex, whereas processingchanges in pitch produced activation of the right side.

Conclusions

The neural correlates of auditory repetition priming, orauditory implicit memory, were demonstrated for thefirst time in the auditory cortex, using environmentalsounds. Further, the magnitude of auditory repetitionpriming correlated across participants with the magni-tude of reductions in the auditory cortex as well as otherregions. Thus, we demonstrated that activity of theauditory cortex could be modulated by repetition ofauditory stimuli, as it is in the visual cortex for visualstimuli. Single-unit recordings in primates have shownactivity reductions in the inferior temporal cortex fol-lowing visual stimulus repetition (Desimone, 1996; Miller,Li, & Desimone, 1991). This phenomenon, which hasbeen termed ‘‘repetition suppression,’’ is believed torepresent a learning mechanism that represents familiaras compared to novel items. It has been suggested thatreductions in the fMRI signal, as observed here, are thehuman regional brain expression of repetition suppres-sion. Here, this possible correlate of repetition suppres-sion has been demonstrated for the auditory cortex.

METHODS

Participants

Fourteen right-handed volunteers (five men) participat-ed in this study (ages 19–29 years). They received US$40for participation. Informed consent was obtained in amanner approved by the Human Subjects Panel ofStanford University.

Stimuli and Behavioral Procedure

Materials included 192 environmental sounds (e.g., adog barking, a door slam, a gun shot, etc.), 25% of themgenerated by animals. None of the sounds containedhuman vocal sounds (speech or nonspeech). Soundswere selected from sound effects CDs and edited to last2 sec. The sampling rate of the sounds was 44.1 KHz,with 16-bit quantization.

Two simple high- (520 Hz) and low-pitched (260 Hz)tones, lasting 2 sec each, were generated to be includedin an auditory localizer session. The sounds and tones


were edited using SoundEdit and presented with aPower Macintosh G3 computer (Apple, Cupertino, CA).Psyscope software (Cohen, MacWhinney, Flatt, & Pro-vost, 1993) was used to control stimulus presentationand to collect responses. The sounds were presented tothe participants in the scanner by a pneumatic head-phone system (Resonance Technology, Van Nuys, CA).This headphone system presented auditory stimuli di-rectly to both ears while reducing scanner noise.

A blocked design was employed with two repetitionpriming scans and one auditory localizer scan. Theauditory localizer scan allowed an independent func-tional definition of auditory cortex for an ROI analysis. Ineach repetition priming scan, participants were pre-sented with eight blocks of initial and eight blocks ofrepeated presentations of nine environmental sounds(across the two scans a total of 144 unique sounds wereused, each presented twice). Each block of initial soundpresentation preceded a block containing the same ninesounds but presented in a different pseudorandomorder. Each sound (2 sec) was followed by a 1-secinterstimulus interval (ISI), resulting in a total durationof 27 sec per block. Participants were instructed todecide, for each sound, whether or not it was generatedby an animal. Responses were to be made as quickly andas accurately as possible, using one thumb for ‘‘Animal’’responses and the other for ‘‘Not an animal’’ responses.The mapping of responding hands to responses wascounterbalanced across participants.

In the auditory localizer scan, participants listened tothree types of 20-sec blocks: Six blocks of environmentalsounds, six blocks of simple tones (simple tone datawere not analyzed in this study), and six blocks ofsilence (scanner noise). Blocks were presented in a fixedpseudorandom order, which included all six possibleorders of the three types of blocks, with the restrictionthat two blocks of the same type were not presentedsuccessively. Each of the six blocks of environmentalsounds included eight pseudorandomly mixed sounds(2 sec each, 25% generated by an animal, a total of 48sounds that were not used in the repetition primingscans). Sounds were separated by a 0.5-sec ISI. Eachblock of tones included six low-pitched tones pseudor-andomly mixed with two high-pitched tones. During thescanner noise blocks, no sounds were presented to theparticipants except for the background scanner noise,which was present for all blocks. Participants were askedto simply pay attention to the sounds and tones pre-sented to them. In all sessions, participants were in-structed to keep their eyes closed.

fMRI Procedure

A 1.5-T General Electric Signa scanner was used to ac-quire both T1 anatomical volume images (TE = 14 msec,TR = 600 msec) and T2*-weighted spiral functionalimages. Each whole-brain acquisition consisted of 20

axial slices aligned parallel to the plane of the anteriorcommissure and the posterior commissure (6 mm thick-ness, no gap, 3.75 " 3.75 mm in-plane resolution,240 mm FOV, 64 " 64 matrix, TE = 40 msec, flipangle = 75). A total of 288 volume images per primingscan (TR = 1500 msec) and 180 volume images for theauditory localizer scan (TR = 2000 msec) were takencontinuously. Eight additional volumes were collectedand discarded at the beginning of each scan to allow forT1 equilibration. Head motion was minimized throughthe use of a fixed bite-bar formed with each participant’sdental impression.

Data Analysis

SPM99 (Wellcome Department of Cognitive Neurology,London, UK) was used to process and analyze thefunctional data. To correct for differences in acquisitiontime, all slices were resampled in time relative to theacquisition time of the middle slice, using sinc interpo-lation in time. All volumes were then realigned to thefirst volume (using sinc interpolation) to correct formotion. Estimated motion parameters computed bySPM99 were examined on a participant-by-participantbasis; the amount of absolute motion did not exceed1.6 mm for any participant. The T1 structural volumewas co-registered with the mean realigned functionalvolume and segmented to gray and white matter. Thegray matter was then normalized to the MNI graytemplate (based on Montreal Neurological Institutereference brain). The functional volumes were normal-ized using the normalization parameters that weregenerated based on the normalization of the graymatter. Then, the functional volumes were smoothedwith a 6-mm full-width half-maximum isotropic gaussiankernel. Differences between stimulus conditions wereexamined by using the general linear model (GLM;Friston, Jezzard, & Turner, 1994), modeling activationat each voxel as a boxcar (square wave) function con-volved with the expected hemodynamic response func-tion to account for hemodynamic delay. Statisticalanalysis was performed using a mixed-effects model;fixed effects were used for single-subject analyses andrandom effects for group analyses (Holmes & Friston,1998). For group analyses, contrast images werecomputed for each participant, then submitted to aone-sample t test (Friston, Holmes, Price, Buchel, &Worsley, 1999). These t-maps were thresholded atp < .001, uncorrected for multiple comparisons, witha spatial extent threshold of 5 contiguous voxels.Group activation maps from these analyses were over-laid on the mean of all participants’ normalized high-resolution anatomical image for each contrast.

ROI time-series data were averaged across voxels,linearly detrended, high-pass filtered (0.015 Hz), andconverted to percent signal change (using the time-


series mean as the baseline). The data for each condi-tion were averaged across blocks for each partici-pant. The block averaging window was shifted by fourimages (6 sec) to account for the hemodynamic lag (cf.,Donaldson, Petersen, Ollinger, & Buckner, 2001).

Acknowledgments

This work was supported by the National Institute of Healthgrant MH59940. Dafna Bergerbest was supported by postdoc-toral scholarships by the Fulbright Foundation and the Feld-man Foundation. Dara Ghahremani was supported by NationalInstitute of Mental Health Training Grant MH15157-20. Wethank Gary Glover for help with scanner protocol and sounddelivery system, and Susan Gabrieli and Jeff Cooper for helpwith data analyses. Portions of this article were reported atthe Society for Neuroscience meeting in Orlando (2002).

Reprint requests should be sent to Dafna Bergerbest, PhD,Department of Psychology, 420 Serra Mall, Stanford, CA 94305-2130, or via e-mail: [email protected].

The data reported in this experiment have been deposited inThe fMRI Data Center (http://www.fmridc.org). The accessionnumber is 2-2003-115KR.

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