Two separate codes for missing-fundamental pitch in the human auditory cortex

Two separate codes for missing-fundamental pitch in the humanauditory cortex

I. Winklera)

Department of Psychophysiology, Institute for Psychology, Hungarian Academy of Sciences, P.O. Box 398,Szondi u. 83/85, H-1394 Budapest, Hungary and Cognitive Brain Research Unit, Department ofPsychology, University of Helsinki, P.O. Box 13, FIN-00014 University of Helsinki, Finland

M. Tervaniemi and R. NaatanenCognitive Brain Research Unit, Department of Psychology, University of Helsinki, P.O. Box 13,FIN-00014 University of Helsinki, Finland

~Received 19 November 1996; revised 3 March 1997; accepted 20 April 1997!

Two auditory event-related potential components, the supratemporal N1 and the mismatchnegativity ~MMN !, index traces encoding the missing-fundamental pitch. The present resultssuggest that these two codes derive from separate pitch extraction processes. Frequent 300-Hz andinfrequent 600-Hz missing-fundamental tones were presented, in some stimulus blocks with short~150 ms!, in others, with long~500 ms! stimulus durations. MMN, reflecting a preattentive changedetection process, was elicited by infrequent missing-fundamental tones only in the long-durationcondition. Correspondingly, subjects were able to detect these high-pitch missing-fundamental tonesamongst similar low-pitch ones only when the stimulus duration was long. In addition, the MMNresponse peaked ca. 120 ms later for missing-fundamental tones than for pure tones of thefundamental frequency suggesting that missing-fundamental pitch resolving took substantiallylonger than extracting the spectral pitch. In contrast, a differential N1 response to themissing-fundamental pitch was found for both stimulus durations, with no substantial difference inpeak latency between the pure and missing-fundamental tones. The contrasting features found forthe two auditory cortical missing-fundamental pitch codes support the notion of two separatemissing-fundamental pitch resolving mechanisms. ©1997 Acoustical Society of America.@S0001-4966~97!05208-9#

PACS numbers: 43.64.Ri, 43.66.Fe, 43.66.Hg@RDF#

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INTRODUCTION

The perceived pitch of complex tones consisting of seral partials corresponds to that of the fundamental wheor not the fundamental itself is present in the sound. Tutility of resolving the missing-fundamental pitch in naturenvironments is stressed by the presence of this abilityanimals~e.g., Tomlinson and Schwarz, 1988! and by its earlyappearance in the course of human ontogenesis~Clarksonand Clifton, 1985!. The importance of the missingfundamental pitch phenomenon~Seebeck, 1841; for recenreviews, see de Boer, 1976; Scharf and Houtsma, 1986! forpitch perception theories lies in the fact that it demonstrathat pitch analysis extends beyond the auditory peripherthe pitch experience for complex tones does not fully corspond to what could be expected on the basis of the pereral distortion~Schoutenet al., 1962!. In addition, pitch rec-ognition for missing-fundamental tones does not deteriowhen harmonics are presented dichotically~Houtsma andGoldstein, 1972!. Therefore recent pitch perception theorisuggest that central pattern-recognition processes extracfundamental frequency from the aurally resolved low-ordharmonics ~Goldstein, 1973; Wightman, 1973; Terhard1974!.

Studies showing how pitch information is encoded in t

a!Electronic mail: [email protected]

1072 J. Acoust. Soc. Am. 102 (2), Pt. 1, August 1997 0001-4966/97/1

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first stages of the afferent auditory pathway provided datadetermining the constraints of the subsequent processinthe missing-fundamental pitch. However, signals measufrom 8th-nerve fibers~e.g., Horstet al., 1986!, single cells ofthe cochlear nucleus~e.g., Evans, 1977!, or auditory evokedbrainstem potentials~Galbraith, 1994! are only indirectly re-lated to the perceived pitch of missing-fundamental tonCortically generated auditory event-related potentials~ERP!may provide an important link between neural activity apitch perception.

ERP responses can be decomposed into contributiondistinct generator processes, the ERP components, appein their typical latency range and displaying the scalp disbution characteristic to the underlying generator~Naatanenand Picton, 1987!. Some of these components are associawith perceptual processes. One piece of such evidenceprovided by Pantevet al. ~1989!, who found that the generator location of the magnetic counterpart of the auditory Npotential ~N1m! elicited by complex missing-fundamentatones corresponded to the auditory cortical source activaby pure tones of the fundamental frequency. Pantevet al.~1996! extended the previous results to dichotically prsented missing-fundamental tones: the source location ofN1m component elicited when odd and even harmonicsthe same fundamental frequency were presented to diffeears matched that of the N1m to a pure tone of the funmental frequency.

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The auditory N1 wave is a central negativity typicalpeaking between 80 and 140 ms from stimulus onset~for areview, see Naätanen and Picton, 1987!. The N1m predomi-nantly reflects the contribution of the auditory cortex to telectric N1 wave. This N1 constituent was termed thepratemporal N1 component~cf. Vaughan and Ritter, 1970for a detailed discussion of further N1 subcomponents,Naatanen and Picton, 1987!. The neural elements generatinthe N1m are tonotopically organized in the primary auditocortex, that is, the stimulus frequency is encoded by thecation of the evoked neural activity~Elberling et al., 1982;Romaniet al., 1982; Pantevet al., 1988!. Frequency~pitch!traces are probably preserved by the supratemporal N1rons in the form of refractoriness patterns demonstratedthe frequency-specific decrease of the N1~N1m! amplitudeto sounds of similar frequency presented in short succes~Hari et al., 1982; Naatanenet al., 1988; Sams and Salmelin1994!. This response decrement cannot be reversed byhabituation procedures~Ritter et al., 1968; Barry et al.,1992!. Therefore, Pantevet al.’s ~1989, 1996! results suggesthat a missing-fundamental pitch code is present in the nronal population generating the supratemporal N1 by cams from the stimulus onset~the time the N1m response reflecting the missing-fundamental pitch commences!.

However, there exists a large body of evidence showthat the N1 response does not correspond to auditory pertion ~for reviews, see Naätanen and Picton, 1987; Naätanen,1992!. For example, in terms of the N1 wave, a 1000-Htone amplitude modulated at 200 Hz is more similar to1000-Hz pure tone than a 200-Hz one~Butler, 1972!,whereas the perceived pitch of this complex tone is apprmately equal to that of a 200-Hz tone. In addition, theamplitude does not correlate with pitch recognition~Para-suramanet al., 1982!.

In a recent study, Winkleret al. ~1995! found that infre-quent complex missing-fundamental tones of 600-Hz funmental frequency presented amongst a set of similar tohaving 300 Hz as the missing fundamental elicitedMMNm response, the magnetic counterpart of the mismanegativity ~MMN ! ERP component. The MMN is a frontocentrally negative potential evoked by infrequent chan~deviant stimuli! in a sequence of a repetitive~standard! au-ditory stimulus or stimulus feature~for recent reviews, seeNaatanen, 1992; Ritteret al., 1995!. Because the MMN isnot elicited by frequently presented stimuli or by a rastimulus per se in the absence of a frequent stimulus~Lou-nasmaaet al., 1989; Naatanen et al., 1989!, it appears thatMMN reflects the deviation of the incoming stimulus frothe auditory sensory memory trace of the frequently psented stimulus or stimulus feature~Naatanen et al., 1978;Naatanen, 1992; Cowan, 1995!. The accuracy of the sounrepresentations indexed by the MMN seems to corresponthe perceptual resolution of auditory stimulus features~seeNaatanen and Alho, 1995; Krauset al., 1996!. MMN is elic-ited even when subjects perform some task unrelated toauditory stimulation~like reading a book or performing somvisual task; e.g., Lyytinenet al., 1992!. Therefore the changedetection process reflected by MMN is probably preattentThus MMN provides accurate information about the und

1073 J. Acoust. Soc. Am., Vol. 102, No. 2, Pt. 1, August 1997

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lying memory representations, which is free from tasrelated distortions.

The composition and within-block probabilities of Winkler et al.’s ~1995! missing-fundamental tones was such theach complex tone, as well as each harmonic frequencypresented equiprobably in the stimulus blocks~the virtualpitch conditions of the present experiments I and II usesame design, see below!. This way, the occasional changfrom 300- to 600-Hz virtual pitch was not accompaniedsimilarly infrequent changes in spectral pitch. The MMelicited by the 600-Hz missing-fundamental tone with rspect to the 300-Hz ones demonstrated that the memtraces involved in the process generating this componentresented the virtual pitch of complex tones, not the specpitch of their harmonic components. Infrequent deviationsperiodicity pitch, another typical way of separating spectand virtual pitch, also elicit an MMN~Lu et al., 1989!.

Winkler et al.’s ~1995! MMNm to virtual-pitch deviantsoriginated from the auditory cortex, in accordance with twell-known auditory cortical location of the primary MMNgenerator~Hari et al., 1984; Halgrenet al., 1995; for a re-view, see Alho, 1995!. The peak latency of this pitchMMNm was, however, longer by ca. 120 ms~200–280 ms!than the typical peak latency~100–140 ms! for comparablechanges in the spectral pitch of pure tones~see Naätanen,1992!. This result suggested that resolving the missinfundamental pitch took substantially longer than pitch etraction from pure tones. On the other hand, the orientaof the N1m generator activated by the missing-fundamedeviant stimulus differed from that of the N1m generatorthe standard stimuli. This latter result showed thatmissing-fundamental pitch information was also encodedthe neuronal population underlying the N1m response,was demonstrated by Pantevet al. ~1989, 1996!.

If the missing-fundamental pitch code was completeca. 80 ms after stimulus onset, judging from the onset ofN1m component, why then did preattentive detection ofviance take 120 ms longer for missing fundamental thanpure tones~the latter elicit N1ms of similar onset latencies!?Two alternative explanations can be considered.

~1! Independent codes hypothesis: The missinfundamental pitch information reflected by the N1m aMMNm are determined by two separate pitch-resolving pcesses of different durations.

~2! Common origin hypothesis: The pitch informatioreflected by the N1m and MMNm derives from that sampitch-resolving process. To account for the delayed MMNto missing-fundamental tones compared with that to ptones~Winkler et al., 1995; whereas no such difference wobserved for the N1m; Pantevet al., 1989, 1996!, one shouldassume that the original pitch code undergoes further pcessing before it is stored in the stimulus representationsdexed by the MMNm.1 This latter process takes longer fovirtual than for spectral pitch.

The present study investigated the relationship betwthe above two auditory cortical codes of missinfundamental pitch. The independent codes hypothesisgests that the traces reflected by the supratemporal N1 cponent are established by a fast process capable

1073Winkler et al.: Two separate pitch codes

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TABLE I. Partials ~in Hz! used in composing the complex missing fundamental tones. The frequencieployed in creating the deviant~600 Hz! tone are italicized throughout the table.

Missing fundamentalcomponent

Standards300 Hz

Deviant600 Hz

1 2 3 4 5 6 7 8 9

1 1200 1200 1200 1200 1200 1500 1500 1500 1800 12002 1500 1500 1500 1800 2100 1800 1800 2100 2100 18003 1800 2100 2400 2100 2400 2100 2400 2400 2400 2400

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determining the missing-fundamental pitch from short acotic segments. In contrast, the auditory stimulus represetions indexed by the MMN component result from a slowprocess, one, perhaps, requiring longer acoustic samplesseparate the two assumed pitch-resolving processes,present set of experiments investigated the effects of stilus duration on the pitch discrimination of missinfundamental tones and on the target ERP responses, thand MMN. As the N1 peak latency does not increase wincreasing stimulus durations, the process encodingmissing-fundamental pitch for N1 should not be affectedstimulus durations exceeding the well-known range ofN1 peak latency. Therefore if by employing different stimlus durations~all longer than the N1 latency! the elicitationor the latency of the MMN response can be influenced,should conclude that the pitch-resolving process underlythe auditory stimulus representations of the MMN systproceeds separately from the one whose outcome is refleby the N1. On the other hand, if such stimulus durationsnot produce differential MMN effects, the more parsimonous explanation of common pitch resolving can be matained. In addition, it was expected that voluntary discrimnation performance would parallel the emergence ofpitch code reflected by the MMN as previous investigatiosuggested good correspondence between MMN and votary discrimination performance~for a review, see Na¨atanenand Alho, 1995!.

I. EXPERIMENTS I AND II

A. Procedure

Nine subjects with normal audiological status~five fe-males, 18–29 years, mean age 23.2 years! participated inexperiment I, 12 subjects~eight females, 19–27 years, meaage 22 years, all different from those of experiment I! inexperiment II. Subjects gave informed consent after theture of the study was explained to them. During the EErecordings, the subject was sitting in a reclining chair inacoustically dampened and electrically shielded room reing a book of his/her choice.

Six blocks of 500 short tones were binaurally deliverto subjects via TDH-50p headphones~NeuroStim stimulationsystem! at an intensity level of 75 dB, sound-pressure levHalf of the blocks contained randomized sequences300-Hz ~‘‘low,’’ 90% ! and 600-Hz ~‘‘high,’’ 10% ! puretones~spectral pitch condition!. In the other three stimulusblocks, ten different complex missing-fundamental tonwere equiprobably delivered at 10% probability~virtual pitchcondition!. Nine out of the ten complex tones had i

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missing-fundamental frequency at 300 Hz, the tenth at 6Hz. The missing-fundamental tones were composed of thpartials selected from the range between the 3rd and theovertones of the 300-Hz fundamental~equaling the 1st to 3rdovertones of the 600-Hz fundamental!. Table I gives the fre-quencies used for constructing the complex tones. Eachdividual harmonic frequency was employed in six out of tten missing-fundamental tones~including the 600-Hz one!.In addition, pink noise covering the range of the two fundmentals~200–800 Hz! was added to each complex tone atintensity level of 240 dB relative to the intensity of thesummed partials to prevent the fundamentals from emergin the output signal due to nonlinear distortions of the stimlation equipment. The overall intensity was identical to thin the spectral pitch condition. The order of the stimulblocks was balanced across subjects.

In experiment I~‘‘short duration’’!, tones of 150-ms du-ration were delivered with an interstimulus interval~offset-to-onset; ISI! of 350 ms. In experiment II~‘‘long duration’’!,500-ms tones were presented with 400 ms ISI. Stimulusrations included 5-ms rise and 5-ms fall times.

The electroencephalogram~EEG! was measured withAg/AgCl electrodes from Fpz, Fz, Cz, Pz, and Oz~10-20system!, both mastoids~LM and RM, for the left and rightmastoids, respectively!, and from L1, L2, R1, and R2~theone- and two-third points on the arc connecting Fz withmastoids on both sides!. The horizontal electrooculogram~HEOG! was monitored at the outer canthus of the right eThe common reference electrode was placed on the tip ofnose. The EEG and EOG signals were digitized at a spling rate of 500 Hz with bandpass filtering between 0.1 a100 Hz~23 dB points!. Responses~analysis period: 400 msstarting 50 ms before stimulus onset! were filtered~low-passbandlimit 30 Hz! and separately averaged for each stimutype. Epochs containing an EEG or EOG change exceed100 mV at any lead were omitted from the analysis. Amptude measurements were referred to the mean amplitudthe prestimulus period~‘‘biological zero’’!. Statistical analy-ses,t tests and dependent analyses of variance~ANOVA !,were conducted by the BMDP statistical program packa~Dixon, 1985!.

B. Results

In the spectral pitch condition of both experiments, ifrequent high tones~deviants! were preattentively detecteamongst repetitive sequences of the low tones. Thisdemonstrated by the larger negativity elicited in responsedeviant than standard stimuli in the 100–150-ms inter


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FIG. 1. Experiments I and II, spectral pitch condition: Frontal~Fz! grand-average ERP responses to frequent low~standard, thin line! and infrequent high~deviant, thick line! pure tones in the short~left side! and long~right side! stimulus-duration experiments. The negative difference between the devianstandard responses~deviant-standard! is marked for each stimulus duration. The bar chart at the center of the figure gives the amplitude of the correspomarked difference responses.

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from stimulus onset~Fig. 1, see Figs. 3 and 4, left sidfor individual responses in the spectral pitch condition!.The statistical significance of the mean frontal~Fz! differ-ence between the standard and deviant responses in100–150-ms interval was verified by 1-groupt tests@t(8)55.09, mean difference:d52.46mV, Standard Errorof Mean: SEM50.48, p,0.001 and t(11)57.3,d523.01mV, SEM50.41, p,0.0001, for the short- andlong-duration stimuli, respectively#. The large extra negativity in response to deviant stimuli~compared to that to thestandards! consisted predominantly of the MMN componewhich was only elicited by infrequent stimuli. The scalp dtribution of this additional negativity had a frontocentrmaximum, was slightly larger over the right than left hemsphere appearing with reversed polarity at the mastoid. Tis compatible with the notion that MMN was elicited by thdeviant stimuli~see, Na¨atanen, 1992 for a description of thMMN scalp distribution!. With large~one octave! separationbetween the standard and deviant frequencies, MMNknown to overlap the N1 wave~Scherget al., 1989!. There-fore, part of the difference between the standard and devresponses was probably due to frequency-specific refracness differences in the N1 components. In other words,N1 neurons responding to the 300-Hz stimulus frequecould have become more refractory during the frequent retition of the 300-Hz stimulus than the neurons activaonly by the 600-Hz tone. The central~Cz! N1 peak latency inthe grand-average responses to low standard tones wasand 124 ms for long and short tones, respectively~the over-lap between the N1 and MMN prevented the measurementhe N1 peak latencies for the deviant tones!.

Infrequent high-pitch missing-fundamental tonamongst frequent low-pitch ones were preattentivelytected only at the long stimulus duration~experiment II!.Figure 2~right side! shows the MMN component at the 200260-ms interval of the frontal responses to infrequent hipitch missing-fundamental tones@t(11)54.59, d520.48mV, SEM50.098,p,0.001, for the mean difference in thinterval#, whereas the tiny negative difference appearingthe same interval for the short tones~Fig. 2, left side! was farfrom being significant @t(8)50.97, d50.053mV, SEM


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50.054#. Individual responses~Figs. 3 and 4, right side!demonstrate that the two experiments yielded separate,consistent patterns of results with the expected interinvidual variance. In experiment II, the scalp distribution of tdifference between the deviant and standard responses i200–260-ms interval was supporting the identification of tnegativity as an MMN component@see also Winkleret al.~1995!, where the equivalent current dipole of the corrsponding magnetic response was localized in the audicortex#.

In contrast, with both stimulus durations, low-pitcmissing-fundamental standards elicited a later and somewlarger N1 component than the high-pitch deviant stimu~Fig. 2!. The mean frontal~Fz! amplitudes of the standarand deviant responses differed in the 120–170-ms inte@t(8)52.44, d50.37mV, SEM50.15, p,0.05 andt(11)53.66, d50.65mV, SEM50.18, p,0.01, for experimentsI and II, respectively#. More importantly, the peak latency othe central~Cz! N1 response~measured separately for eacsubject within the 80–140-ms interval! was significantlylonger for the low-pitch than for the high-pitch missingfundamental tones@t(8)53.19, d510.2mV, SEM53.19,p,0.05, and t(11)53.28, d59.0 ms, SEM52.75, p,0.01, for short and long stimulus durations, respective#.The central~Cz! N1 peak latency in the grand-average rsponses was 128 ms for the low-pitch standards of bstimulus durations, 120 and 108 ms for the short- and loduration high-pitch deviants, respectively.

In general, the N1 amplitudes measured in experimenwere higher than those in experiment I. This was due todifference in stimulus onset asynchronies~onset-to-onset in-terval; SOA being 500 vs 900 ms, in experiments I andrespectively!. The N1 amplitude increases with increasinSOAs below ca. 10 s as a consequence of the long recoperiod of the N1-generating neuronal elements~Hari et al.,1982; for a review see Na¨atanen and Picton, 1987!.

The MMN (MMN1N1) responses shown in Figs. 1 an2 were usually followed by an increased positivity in th200–350-ms latency range~see, also Figs. 3 and 4!. Thefrontocentral scalp distribution of this wave suggests tha


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FIG. 2. Experiments I and II, virtual pitch condition: Frontal~Fz! grand-average ERP responses to frequent low-~standard, thin line! and infrequent high-pitch~deviant, thick line! missing-fundamental tones in the short~left side! and long~right side! stimulus-duration experiments. The N1 difference betweendeviant and standard responses~hatched patterns; standard-deviant! and the MMN component~solid shades; deviant-standard! are marked for each stimulusduration. The bar chart at the center of the figure gives the amplitude of the correspondingly marked difference responses.
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C. Discussion

Experiments I and II established that the processflected by the MMN component requires long (.150 ms)acoustic samples of the complex tones to preattentivelytect infrequent high-pitch missing-fundamental tones embded in sequences of similar low-pitch tones. For pure toof the equivalent spectral pitch, stimuli of 150-ms duratiproved to be sufficient. In addition, the MMN to missinfundamental pitch change peaked ca. 120 ms later thanelicited by an equal amount of deviation in spectral pitcThese results suggest that resolving and encoding the vipitch of missing-fundamental tones for the auditory stimurepresentations underlying preattentive change detectakes significantly longer than the processing of specpitch. The alternative explanation that the late MMNmissing-fundamental pitch deviants~compared to that topure-tone ones! was the result of prolonged change detect~rather than of slower pitch resolving for missing fundametal than pure tones! is contrasted by the lack of MMN toshort-duration missing-fundamental pitch deviants. If tMMN latency difference between the long-duration specpitch ~pure tone! and virtual pitch ~missing fundamental!conditions were caused by longer preattentive change detion for missing fundamental than for spectral pitch, shoduration missing-fundamental pitch deviants should ahave elicited the MMN~if only later than the short-durationpure-tone deviants!.

In contrast to the MMN, the N1 response to the twmissing-fundamental tones differed at both stimulus dutions, with the latency of the N1 wave being approximateequal in the responses to pure and missing-fundametones.

Experiment III was designed to test whether the oserved differences in the N1 responses to low- and high-pmissing-fundamental tones reflected the pitch-specific na


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of the N1 wave or whether this difference was rather cauby the unequal probabilities of stimulus presentation~by pro-ducing different refractoriness states in the N1 generaneurons responding to 300- versus 600-Hz pitch!. To elimi-nate the effects of the unequal stimulus probabilities, eacthe ten different missing-fundamental tones were presenin separate~homogeneous! blocks.

II. EXPERIMENT III

A. Procedure

Seven subjects with normal audiological status~four fe-males, 19–25 years, mean age 21.6 years! participated in theexperiment. Subjects gave informed consent after the naof the study was explained to them. The stimuli, proceduEEG/EOG recording, and measurements were identicathose of the virtual pitch condition of experiment II~500-msstimulus duration!, except that all ten different missingfundamental tones were presented in separate blocks,carrying 120 identical stimuli.

B. Results

Figure 5 shows that the N1 response peaked laterlow-pitch than for high-pitch missing-fundamental toncausing an amplitude difference on the downward slopethis wave, similar to that observed in experiments I andThe N1 peak-latency difference was comparable to thaexperiments I and II: the grand-average peak latencies w110, 106, 104, 104, 104, 112, 108, 106, and 106 ms fornine low-pitch complex tones~the order corresponds to thain Table I!, 98 ms for the high-pitch missing-fundamenttone ~the difference between the N1 peak latencies insponse to low- and high-pitch tones was ca. 8 ms, onaverage!. An analysis of variance of all ten responses~onefactor with ten levels for the ten N1 peak-latency measuments conducted separately for each subject within the140-ms interval! confirmed the observed N1 peak lateneffect@F(9,54)53.85,p,0.01, the Huynh–Feldt adjustmenfactor for the degrees of freedom being 0.879#. Thepost-hoccontrast showed that the N1 peak latency to the high-pcomplex tone was significantly shorter than that to the lo


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C. Discussion

The present results demonstrated that the neuronalments generating the N1 response differentially responde

FIG. 3. Experiment I: Frontal~Fz! responses to frequent low-~standard, thinline! and infrequent high-pitch pure~left side! and missing-fundamentatones~right side! separately for each subject. Subjects are identified bycodes S01 through S09.


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the pitch of missing-fundamental tones. The N1 peak lateof all nine 300-Hz pitch missing fundamental tones wlonger than that of the 600-Hz pitch one. The pitch speciity of the N1 response did not depend on the within-bloprobability of stimulus presentation as, in this experimeeach tone was presented alone~i.e., without mixing it withother tones within the stimulus blocks!. A reduction of theN1 peak latency with increased missing-fundamental p~100–330 Hz! has also been observed by Ragot and LepaErcole ~1996!. These authors employed short~200 ms!stimulus durations. In the present study, the N1 peak latewas not affected by the spectral pitch of the complex tocomponents. This was demonstrated by the lack of systatic variation in the pattern of N1 peak latencies~comparingthe spectral composition of the 300-Hz pitch complex tongiven by Table I with the grand-average N1 peak latencmeasured from the corresponding ERP responses, seesults above!. If the N1 peak latency was, at least partialldetermined by the spectral pitch of the tonal componeone should expect the similarity between the N1 peak lacies responding to two complex tones of identical virtupitch to depend on the number of common frequency coponents.

The virtual pitch-specific nature of the N1 neuronsdemonstrated by the latency effect in the electrically recoable N1 wave and by the pitch-dependent generator locaof the N1m ~the magnetic N1! component~Pantevet al.,1989, 1996; Winkleret al., 1995!. The fact that also the pealatency of the N1/N1m elicited by pure tones decreases wincreasing tone frequencies below 1000 Hz~Jacobsonet al.,1992; Roberts and Poeppel, 1996! supports Pantevet al.’s~1989! conclusion that the N1m neurons responding to sptral pitch might also be involved in the N1m responsestones of the corresponding missing-fundamental pitch.

Thus the present results support the notion that the nronal population generating the supratemporal N1 comnent encode the pitch of missing-fundamental stimuli. Tresults of experiment I and those of Ragot and Lepaul-Erc~1996! demonstrated that the missing-fundamental pitchencoded by the auditory cortical N1 neurons even at sstimulus durations.

Experiment IV tested the effects of stimulus duration

FIG. 5. Experiment III: Frontal~Fz! grand-average responses to low- ahigh-pitch missing fundamental tones presented in separate stimulus blResponses to different low-pitch missing fundamental tones were collapThe N1~and the consequent P2! difference between the low- and high-pitctones is marked in the figure by hatched pattern fill.


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III. EXPERIMENT IV

A. Procedure

Twelve subjects of normal audiological status~five fe-males, 20–27 years, mean age 22.3 years! participated in theexperiment. Subjects were instructed to press a reactionton when detecting a high-pitch tone. Four stimulus bloceach corresponding to one of the spectral pitch~pure tone! orvirtual pitch ~missing-fundamental tone! conditions of ex-periments I~150-ms tone duration! or II ~500-ms tone dura-tion!, were presented to subjects. Each stimulus block wpreceded by a short training session. Stimulation paramewere identical to those of the corresponding experimecondition, except that the present blocks consisted ofstimuli. The order of the stimulus blocks was balancacross subjects.

B. Results

Due to the exact octave difference in pitch, the requirdiscrimination of missing-fundamental stimuli was difficufor most subjects~cf. Krumhansel, 1990!. With the shorttone duration, only a few of them managed to detecthigh-pitch missing-fundamental tones above the chance l~mean detection rate 19.33%, with 10% of the tones havhigh missing-fundamental pitch!. However, the discrimina-tion performance for missing-fundamental tones dramaticimproved with the long stimulus duration~mean detectionrate 62.5%!. The discrimination of pure tones was closeperfect at both stimulus durations. Figure 6 shows the groaverage Grier A8 sensitivity values~Grier, 1971; Aaronsonand Walls, 1987! calculated separately for each stimulblock. An ANOVA analysis of these scores@tone type~pure versus missing fundamental!3tone duration ~150versus 500 ms!# revealed an interaction between the two fators @F(1,11)538.85, p,0.0001#. This interaction wascaused by the pattern of results showing significant permance difference between the two tone durations for missfundamental @F(1,11)531.56, p,0.001, A8(150)50.63,A8(500)50.84# but none for pure tones@F(1,11)51.62,A8(150)50.99, A8(500)50.95#. There was a main effect othe tone-type factor confirming that it was easier to discrimnate pure than missing-fundamental tones@F(1,11)555.15,p,0.0001#. The corresponding bias~Grier’s B9! values werehigher for pure tones than for missing-fundamental tonesfor long tones than for short tones@F(1,11)588.08,p,0.0001 andF(1,11)511.21,p,0.01, for tone type andtone duration, respectively#. No interaction was found between the two factors for the bias values. Reaction timcould only be analyzed for the long tones as the numbedetected short missing-fundamental targets was too smalseveral subjects. The average reaction time~RT! for longmissing-fundamental tones was significantly longer than t

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for the corresponding pure tones~518.12 and 377.08 msrespectively; t(11)56.83, d5141.03 ms, SEM520.66, p,0.001!.

C. Discussion

The present results demonstrated that short samplethe stimuli were insufficient for a reliable discriminationthe low and high missing-fundamental sounds even thopure tones of the corresponding pitches could be easilytinguished with this duration. With the long stimulus durtion, however, also the missing-fundamental tones of onethe other pitch could be discriminated from each other.accordance with the difficulty of the task, RTs were longfor missing-fundamental tones than for pure tones~this wastested only for the long stimuli!.

IV. GENERAL DISCUSSION

The picture emerging from the present experimentsthree salient features:~1! The preattentive change detectio~revealed by the elicitation of the MMN component! paral-lels voluntary discrimination performance. High pure toncould be discriminated from low ones and also the MMcomponent was elicited with both stimulus durations. In cotrast, subjects were able to detect the infrequent high-pmissing-fundamental tones amongst frequent low-pitch oonly with the long stimulus duration. Accordingly, the MMNcomponent only emerged at this stimulus duration, butwhen the short stimulus duration was used.~2! The neuronalpopulation generating the supratemporal N1 componentcoded the pitch of the pure and missing-fundamental tosimilarly ~probably in the form of tonotopy, i.e., by following the place principle!. This code distinguished between thtwo employed pitches for the missing-fundamental tonesboth stimulus durations, even though subjects were unabmake the required voluntary discrimination with the shstimulus duration.~3! The onset latency of the N1 responsuggests that the pitch code reflected by this component mbe complete by ca. 80 ms~for both pure and missingfundamental tones!. Spectral pitch information was accesible by the preattentive change detection at about the s

FIG. 6. Grier’s A8 sensitivity values~grand mean! describing the perfor-mance in discriminating low and high pure tones~hatched patterns! andmissing-fundamental tones~solid shades! for the short~left side, grey shade!and long~right side, black color! stimulus-duration conditions.


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time ~judging from the early onset of the MMNs in the spetral pitch conditions of experiments I and II!. However, thepreattentive detection of the missing-fundamental pitch deants ~emerging only with the long stimulus duration! com-menced ca. 120 ms later than that for the corresponding ptones and the average RT measured when subjects discnated these complex tones was ca. 140 ms longer thanRT for the pure tones.

The above-described pattern of results revealed thattraces reflected by the supratemporal N1 and the MMN coponents encoded the outcome of two separate missfundamental pitch-resolving processes. As was expecprolonging the missing-fundamental stimuli past the typiN1 latency range did not increase the N1 peak latency. Hever, MMN was only elicited with the long, but not with thshort stimulus duration. If the missing-fundamental pitcode underlying the two components derived from a comon pitch-resolving process, the MMN should have beelicited with both stimulus durations. This is becausedifferential N1 response to missing-fundamental pitch atshort stimulus duration demonstrated that a 150-ms sosegment provided sufficient spectral information for the cresponding pitch-resolving process. If the missinfundamental pitch information was accessible by the pretentive change detection process at the short stimuduration, MMN should have been elicited, just as it waspure-tone deviants. Therefore the missing-fundamental pcode involved in preattentive change detection~MMN ! andthe one reflected by the N1 could not have been determby a common pitch-resolving process.

The present conclusion of the existence of two sepapitch-resolving processes might be somewhat surprisHowever, redundant mechanisms have already beenposed to account for the missing-fundamental pitch phenenon. Due to the interference between unresolved higorder partials of a given fundamental frequency atauditory periphery~the residue!, in most situations, the envelope of the cochlear output signal carries sufficient infmation for detecting the frequency of the corresponding fdamental~e.g., Horstet al., 1986!. Thus the auditory systemcould determine the fundamental pitch on the basis ofresidue~Schouten, 1949, 1970!. It has been suggested~deBoer, 1976; Houtsma and Smurzinsky, 1990; Carlyon aShackleton, 1994! that beside the central pattern-recognitiprocesses mentioned in the Introduction a residue-bamechanism might also be involved in perceiving the pitchmissing-fundamental tones. The two pitch codes found inpresent study, however, cannot be regarded as resultingthe above-mentioned two mechanisms~pattern recognitionand residue!, because both of the present missinfundamental pitch codes were observed for tones compoof low-order harmonics.

The correspondence between the elicitation of MMand detection performance suggests that the voluntarycrimination of missing fundamentals~and probably also perception! relies on the same pitch code as the preattenchange detection. A similar correspondence betweenMMN and discrimination performance has been observedauditory recognition masking~Winkler et al., 1993!. In ad-


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dition, the MMN peak latency strongly correlates with threaction time in discrimination tasks and, further, it providthe earliest ERP index to predict the latency of later, tadependent ERP components~such as the N2b and P3; e.gNovaket al., 1992; Tiitinenet al., 1994!. Corroborating evi-dence was obtained in the present study. With the lostimulus duration, the MMN peak latency and the RTtargets in the corresponding active discrimination task wlonger for missing-fundamental tones than for pure tonessimilar amounts of time. In contrast, in the present study,correlation was found between the presence of missfundamental pitch information in the neuronal populatigenerating the N1 potential and voluntary discriminationthese complex tones. This finding supports the view thatN1 generating mechanisms are not a part of the sequencbrain events directly underlying perception~Walter, 1964;Davis and Zerlin, 1966; Naätanen and Picton, 1987; Naä-tanen, 1992!.

It is possible that the missing-fundamental pitch infomation reflected by the supratemporal N1 is establishedsubcortical parts of the afferent auditory system. This notis supported by observations of neural activity related tomissing-fundamental pitch throughout the ascending atory pathway ~Smith et al., 1978; Greenberget al., 1987;Galbraith, 1994!. Furthermore, the subcortical pitch-relateneural activity does not require long acoustic samplesmissing-fundamental tones~e.g., a frequency-following response of the fundamental commences in the brainstemsoon as 15 ms after the onset of a missing-fundamental tSmith et al., 1978; Greenberget al., 1987!. At the corticallevel, tonotopically organized neuronal populations habeen shown to underlie the Pa component~Pantevet al.,1995!, one of the earliest exogenous~‘‘obligatory,’’ stimulusdriven! auditory cortical evoked responses~peaking at about30 ms from stimulus onset!. In addition, the peak latency othis, as well as the other ‘‘middle-latency’’ auditory evokepotentials~Na, Nb, and Pb! was shorter in response to 4-kHthan to 250-Hz tone bursts~Woodset al., 1995!. This resultprovides further evidence linking the observed spectralvirtual pitch specific N1 latency effects to earlier phasespitch processing. Thus there seems to exist an unbrochain of stages along the auditory afferent pathway estabing the pitch of missing-fundamental tones with very shdelay from the onset of stimulation and encoding it by tsame tonotopical code as that for the spectral pitch. The rtively early onset and tonotopical nature of the exogensupratemporal N1 component are compatible with the nothat the supratemporal N1 neurons could receive their infrom this system. The present suggestion does not neceily contradict Pantevet al.’s ~1996! findings demonstratingthe ‘‘central’’ origin of the missing-fundamental pitch codreflected by the N1m as the auditory pathways from theears converge already in the medial superior olive, the sond ‘‘relay station’’ of ascending auditory information in thbrainstem~see, e.g., Harrison, 1978!.

The missing-fundamental pitch-extraction process sserving the auditory stimulus representations of the MMsystem requires considerably longer~longer than 150 ms!acoustic samples than that needed for preattentively discr


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nating pure tones of even only slightly differing frequenci~30 ms in Paavilainenet al., 1993!. The relatively long du-ration of this process is also suggested by the long~ca. 250ms! peak latency of the MMN to missing-fundamental pitcdeviants~see also Winkleret al., 1995!. These features arecompatible with the assumption that the missinfundamental pitch is resolved by some central patterecognition process for subsequent storage in auditorysory memory.

V. CONCLUSIONS

The problem of resolving the missing-fundamental pithas important implications for the theory of pitch perceptioThe present study demonstrated that two separate codethe missing-fundamental pitch exist in the auditory corteThese codes are determined by different pitch-extraction pcesses. The auditory stimulus representations involvedpreattentive change detection~reflected by the MMN com-ponent! seem to correspond to those subserving voluntdiscrimination. Establishing this code takes consideratime and requires long samples of the acoustic input. Tpresence of missing-fundamental pitch information in ttonotopically organized neuronal population generatingsupratemporal N1 did not correspond to the voluntary dcrimination of missing-fundamental tones. The pitch infomation reflected by the supratemporal N1 is probably eslished by subcortical mechanisms in the early phaseauditory processing shortly after the stimulus onset. Thefore, the present results suggest the existence of redunmechanisms in resolving the missing-fundamental pitch.

ACKNOWLEDGMENTS

This study was supported by the National Scientific Rsearch Fund of Hungary~OTKA T006967!, the Academy oFinland, and the Finnish Psychological Society. The auththank Dr. Istvań Czigler, Dr. Mark Molnar, Dr. Walter Rit-ter, and Dr. Hannu Tiitinen for their helpful comments asuggestions.

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Two separate codes for missing-fundamental pitch in the human auditory cortex

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