Perception of the Missing Fundamental by Cats - Psychology

Perception of the missing fundamental by cats*Henry Heffner t and I. C. WhitfieldNeurocommunications Research Unit, University of Birmingham, Birmingham. BI$ 2TJ. England(Received 20 May 1975; revised 20 October 1975)Two cats were testexi on their ability to perceive the missing fundamental through the use of an avoidancetechnique. The an/msia were trained to discriminate between rising and falling pitch sequences first withsingle and then with multiple tones. They were then tested by presenting them with tone triads known toproduce the p•rccption of the missing fundamental in humans. In these traids the pitch of the frequenciescomposing the triad either remained the same or shifted in the direction opposite the shift of the missingfundamental. The result show that the animals' response. to these triads was not in conformity with thatexpected from the 'direction of change of the component frequencies, but could be accounted for if it wereassumed that the cats were respondingthe basis of the missing fundamental. A further test given one ofthe eats indicated that this phenomenon declined progressively as the center frequency was raised, until at6 kHz it was apparently completely absent. A similar decline in the strength of the fundamental pitchoccurs over the same range in humans. Thus, there is reason to believe that cats perceive the missingfundamental.Subject Classification: [.43] 65.75, [43] 65.56, [43] 65.54; [43] 80.50.INTRODUCTIONThe phenomenon of the missing fundamental can bedemonstrated with a complex tone made up of sinusoldswith frequencies such as 1600, 2000, and 2400 Hzwhich, when presented to human subjects, g/yes rise tothe perception of a "fundamental" tone of 400 Hz (e. go,Schouten, 19'/0; Schouten, Ritsma, and Cardozo,1962). The missing fundamental has been consideredto be one example of the more general phenomenon ofperiodicity pitch, in which the ear appears to assignpitch to the signal on the basis c/the periodicity of itsamplitude envelope (for a review, see 1•1omp andSmoorenburg, 1970).Because of the importance of periodicity pitch totheories of hearing, it has become the subiect of physiologicalinvestigations of auditory processing (e. g.,Butler, 1972; Hind, 1972; Klang and Goldstein, 1959;Small and Gross, 1962; Whit/ield, 1970a, b). However,while behavioral investigations of periodicity pitch havebeen carried out with human subjects, the majority of physi-,ological investigations have been carried out with animais.As a result, conclusions concerning the relationof neural activity and behavioral data h•tve been limited.In order to determine if animals could perceive pitchfrom such periodic stimuli, two cats were trained torespond to stimuli which in humans produce the perceptiona[ the missing fundamental. The resttits ofthis work have so far demonstrated that cats behavetowards such stimuli much in the same way as do hu-I. METHODThe basis of the method is that if a tone triad A,A-D, A-2D (e.g., 2400, 2000, 1600 Hz)is repiaced bythe triad A, A-E, A-2E, where E > D (e.g., 2400,1942, 1484 Hz), the apparent pitch--the "missing fundamentai"--rises(from 400 to 458 Hz in our example).However, the actual stimulus frequencies either remainthe same or fall. We tra/n the animal to discrhn-inate between rising and rs/ling pitch sequences firstwith single and then with multiple tones. Finally, wepresent it with the above stimulus situation on the hypothesisthat its response will depend on whether it isassigning pitch on the basis of the harmonics or of the"fundamental." In describing the detailed procedure,we propose to avoid the periphrasis "a pitch equivalentto that of a single tone of__Hz" and to speak simply ofthe "frequency" of the missing fundamental. This ismerely a convenience and we are not addressing ourselvesto the question of whether the perceived pitchdoes or does not have any equivalent frequency representationin the nervous system.A. SubjectsTwo cats were used in the experiment. The animalswere maintained on dry food (Purina Cat Chow), andtheir individual daily water consumptions and drinkingpatterns were recorded. Following this procedure, thetime during which the animals had access to water wasrestricted over a period of five to seven days until theanitasis had one hour to drink--a condition to which theanimals rapidly adjustedø Once this procedure wascompleted, the cats were ready for introduction intothe experiment.B. ApparatusThe animals were tested in a rectangular cage, 30.5cm long, 43 cm high, and 43 cm wide, which had astainless-steel-bar floor and wire-mesh sides andtop. A brass water cup (4 cm diam) was placed onthe floor o• the aa•e at one end and connected with rubbertubing to a water bottle via a solenoid water valve.The entire arrangement was placed in a soundproofchamber and monitored by closed-circuit television.An electronic circuit was connected to the water cupand grid floor in order to detect when the cat lickedthe bowl. A constant-impedance shock source wasused to provide the electric shock, which was administeredthrough the grid floor and controlled by a variabletransformer.The tones used were produced by either one or two915 J. Aeou•. So½. Am.. VoL 59, No. 4, Aiml 1976 Copyright ¸ 1976 by the Acoustical Society of America 915

916 Heffne• and Whitfield: Perception of the missing fundamental by cats 916TABLE I.Stimuli used in the missing fundamental test.OscillatorsMissingA B Frequency fundamental(a) 342 ... 342 None400 ... 400 None458 ..- 458 None•) 342 1942 1600, 1942, 2284 342400 2000 1600, 2000, 2400 400458 2058 1600,2058, 2516 458(c) 342 2058 1716, 2058, 2400 342400 2000 1600,2000, 2400 400458 1942 1484, 1942, 2400 458DirectionFrequencyStandardUpDownStandardUpU pStandardDownof ChangeMissingfundamentalß ß ß'-'DownStandardUpDownStandardU pindependent ascillators and a balanced modulator. Toproduce the three-tone stimulus (triad), the output a/oscillator A was added to and subtracted from the centerfrequency produced by oscillator B and ali threefrequencies were combined. Th e frequency of oscillatorA thus determined the spacing of the three frequenciesof the triad, and hence the frequency of thefundamental. By stepping the two oscillators throughequal increments of frequency, either up or down andin the same or opposite directions, the four types of triedpairs set out below and inTable I couldbe produced.The transducers were a 7.5-cm paper-cone speaker(used only in the initial stage of training) and an ionicloudspeaker (Ionophane 601, Fane Acoustics, Ltd. )which were placed 0.5 m in frontofthe animal and directedtowards its head. The advantages of the latterspeaker are that it has a linear response in the rangeof the frequencies used in this experiment and thatthere is no moving diaphragm to generate distortionproducts. In addition, it is matched to the air by asmall horn such that the system has a high-pass characteristic,giving considerable attenuation for frequenciesin the region below 1 kHz.Sound measurements were made by placing a microphone(Briiel& Kj•er «-in. model 4133) above the watercup in the position previously occupied by the cat's headand with its axis pointing directly at the loudspeaker.The sound level was measured with a Briiel & Kj•ermicrophone amplifier (model 2604) and •-octave filter(model 1614). Readings for the 1600, 2000, 2400 Hztriad were 63, 70, and 65 dB with the filters centeredon 1600, 2000, and 2500 Hz, respectively.Because of their small separation, the three componentsof a triad are not completely resolved by thefilter system, so that adjacent components contributeto each reading.. The readings obtained would correspondto values for the respective components of about62, 68, and 64 dB SPL. In general and on this basis,the intensities of the components of the various triadsall fell within the range 65+3 dB SPL. No output couldbe detected within the band 12.5-1000 Hz.C. StimuliThe stimulus pairs were composed of either singletones or triads in which the "standard" stimulus wasfollowed by a "comparison" stimulus of either higheror lower frequency (Fig. 1)o The tone pairs were presentedat a rate of one pair/sec for 10 sec (290-msecduration, 20-msec rise-decay, with 10 msec betweenmembers of a pair and 410 msec between pairs). Thestimuli used may be divided into three categories (cf.Table I).(a) A standard tone of 400 Hz followed by a comparisontone c• either 342 or 458 Hz [Table I(a)].(b) A standard triad of 1600, 2000, 2400 Hz followedby a comparison triad of either 1600, 1942, and 2284Hz or 1600, 2058, and 2516 Hz [Table I(b)]. In humamthese triads produce the perception of a fundamentaltone (the missing fundamental) c• 400, 342, and458 Hz, respectivelyø It is important to no•e that whenthe standard triad is paired with either of the two comparisontriads, the frequencies of both the triad andthe missing fundamental change in the same directionrelative to the standard.(c) A standard triad of 1600, 2000, and 2400 Hzfollowed by a comparison triad of either 1716, 2058,and 2400 Hz or 1484, 1942, and 2400 Hz [Table I(c)].fTANDARO ]z•JuJu.STANDARD''SAFEI 9 10WARNINGI 9 I0TIME ( sec )FIG. 1. Schematic representation of the tone pairs used in themissing fundamental test. The safe signal consisted of 10 tonepairs in which the second tone of each pair was of lower frequencythan the first or standard tone, The warning signalconsisted of 10 tone pairs in which the second tone was of higherfrequency than the standard. The animals were trained tomake an avoidance response upon presentation of the warningsignal and to ignore the safe signal.'J. Acou•t. So•. Am., VoL Eg, No. 4, April 1976

917 Heffner and Whitfield: Perception of the missing fundamental by c;ts 917•n this case, the frequencies of the triads andthemissingfundamental produced by the triads change in theopposite direction relative to the standard. Thus, forexample, a person who perceived the missing fundamentalwould say that the comparison tone of the pairwas of higher frequency than the standard when in facttwo of the tones in the triad were lower. This stimulnscondition was therefore crucial in determining whethera subject perceived the missing fundamental.During initial training, it was discovered that thecats tended to respond to changes in the absolute frequencyof the tones as well as to the direction of theshift in pitch. To reduce the possibility of an animalresponding to changes in absolute frequency, the settingsof the two oscillators were randomly varied byas much as 10% for the stimuli listed in categories (a)and (b) [but not (c)]. This procedure also served to reducethe possibility that the task could be solved on thebasis of changes in intensity which might have beenassociated with changes in frequency.O. Procedure.Briefly, the cats were trained to maintain contactwith the water cup for a water reward. After a reasonablysteady rate of contact was attained, trials werebegun which consisted of the presentation of one of twotone patterns for 10 sec. - If the tone pattern had arising pitch sequence, the cat had to cease licking within3 sec of tone onset in order to avoid an electricshock which would otherwise be delivered to the ani-mal's feet at tone offset. This conditioning proceduresoon resulted in a cessation of contact with the cupduring such a trial. However, if the tone pattern hada falling pitch sequence, it was never followed by shockand cats soon learned to maintain contact with the cupduring these trials. Evidence that the cats had learnedthe discrimination was provided by demonstrating thatthe animals broke contact when a rising pitch sequencewas presented and maintained contact when a falling ßpitch sequence was presented.1. Details of training and testingThe cats were piaced in the cage for a period of oneho•r and allowed to drink from the water cup. Waterwas delivered into the cup at a rate of 100 drops/turn(00 025 ml/drop) as long as the animal maintained contactwith the cup. If the animal broke contact with thecup for more than 0.25 sec, the flow of water wasautomatically stopped. As a reset, the cats soonlearned that steady contact with the cup would deliverthe maximum amount of water.Once the animal had learned to maintain constantcontact with the water cup, a four-stage training andtesting procedure was begun.First stage: The 400-458-Hz tone pairs were presentedfor 10 sec and, unless the animaI ceased drinkingwithin 3 sec of tone onset, were followed at the endof the 10-sec period by an electric shock deliveredthrough the grill floor. After several such tone-shockpairings, the cats learned to cease drinking when the"warning" stimulus came on and thus were usually ableto avoid the shock. The warning stimulus was presentedat random intervals varying in 15-sec blocksfrom 45 to 180 sec following the previous warning signal.Thus, there were generally 10 intervals in whicha warning signal could occur (i.e., 45, 60, 75 .... ,180 sec) though longer intervals were occasionallyinserted.Second stage: Once the cats had learned to avoidthe 400-458-Hz tone pair, they were trained to ignorethe 400-343-Hz tone pair, the "safe" signal [TableI(a)]. This was accompUshed by presenting this tonepair during the 10-sec intervals in which a warningsignal might have, but did not, occur. Thus, the catswere continuously presented with 10-sec tone pairsseparated by 5 sec of silence, with the warning signalrandomly interspersed among the safe signals. Thisstage of training was completed in approximately 20sessions.Third stage: When the cats had learned to discriminatereliably between the two signals, the triad pairs[Table I(b)] were introduced. The procedure used herewas the same as in stage 2 in that the animals weretrained to avoid the triad pair in which the pitch se~quence of the component frequencies, as well as themissing fundamental, was rising and to ignore thetriads in which the pitch sequence of the componentfrequencies and the missing fundamental were falling.Though the anitasis learned to perform this discriminationwithin three to five sessions, training was continueduntil the animals had received at least 20 train-ing sessions.Fourth stage: When the cats had learnedtodiscriminatethe triad pairs, they were presented with the testfor the perception of the missing fundamental. Thisconsisted of presenting "test" triad pairs iTshie I(c)]in which the pitch sequence of the component frequencieswas in the direction opposite the pitch sequence•g the missing fundamental.The test triads were presented by inserting themwithin sessions consisting primarily of the originaltriads with which the animals had been trained. Sincethe nature of these test triads (i.e., safe or warning)depended upon the cue the animal was using, thesetriads were never followed by shock regardless of theanimal's response. Testing was complete once ananimal had received 10 of each of the two test triadsfor a total of 20 test trials.For comparison, theperformance of the cats on the original training tri•lswas determined on the basis of the 60-80 trials which.they received during the test sessions. A further testwas given cat 2 to determine the range of frequenciesover which the missing fundamental might be perceived.This test consisted of triads in which the center frequencywas 3, 4, 5, or 6 kHz and the upper and lowerfrequencies were the center frequency plus and minus400 Hz. To produce the comparison frequencies, thensciliator outputs were increased and decreased by58 Hz, as in the 2-kHz center frequency test.J. Acoutt. Soc. Am., Vol. 59, No. 4, April 1976

918 Heffner and Whitfield: Perception of the miss'ng fundamental by cats 918TABLE IL Performance on 2-kHz center frequency missingfundamental test, Low scores indicate a cessation of contactwith the water cup in order to avoid electric shock. Theletters "b" and "c" indicate the section of Table I from whichthe stimuli were drawn. Note that the animals showed avoidancebehavior when the missing fundamental warned of possibleshock even though the frequencies of the triad indicated noshock (c).MissingConditionScore (in sec)fundamental Triad Cat 1 Cat 2•o) Safe Safe 9.2 9.7Warning Warning 3.2 3.3(c) Safe Warning 9.6 9.7Warning Safe 4.8 3.02. Analysis of behavioral dataThe amount of time that an animal maintained con-tact with the water cup during the safe and warningintervals was determined to the nearest 0.1 sec. Thus,the time or score for an individual trial could varyfrom 0 to 10.0. To reduce the effects of spuriouspauses, the results of a trial were discarded if theanimal broke contact during the 2 sec preceding atrial, though the trial was presented as usual. Thisprocedure helped reduce variability by eliminatingtrials presented while an animal was pausing to groomor rest, as they occasionally did, without having toresort to modification of the randomized trial presentationssequence. Because this criterion was appliedequally to safe and warning trials, it did not bias theresults. The scores for the safe and warning trialswere compared using the Mann-Whitney U test (Sisgal,1956) to determine the probability that the animalswere successfully performing the discrimination.To compare the performance of cat 2 as the centerfrequency was varied, a unitless measure of detectionwas chosen. This measure is a function of the lengthcf time the animal mainixined contact during the warning(W) and safe (S) signals and is computed as (S- W)/S.The values of the measure vary from + 1 (indicatingcomplete cessation of drinking during the warning signal)to 0 (indicating no cessation of drinking), with intermediatevafues interpreted as indicating that thewarning signal was sometimes detected (e.g., Heffner,H•/fner, and Masterton, 1971).II.RESULTSThe performance of the two cats during the test sessionsis shown in Table llo When both the missing fundamentaland the component frequencies of the triadwere safe signals [Table II(b)] the animals generallycontinued to drink from the water cup with litfie orno pause. Indeed, though on the average the animalsbroke contact with the cup for less than I sec, the catsshowed no break in contact at all on over half of thesafe trials. Thus, the animals had learned not to respondto a falling pitch sequence. In contrast, whenboth the missing fundamental and the component fre-quencies indicated shock, the animais ceased drinkingfrom the water cup in an average time of 3 to 4 sec.In addition, the median score for each animal was lessthan 3 sec, so that on most of the warning trials theanimals did not receive a shock at the end of the 10-sectrial. Thus, the distribution of the animals' scoresindicated that they had learned to distinguish a risingfrom a fallir•g pitch sequence (p < 0.0001, one-taileddistribution).The scores for the triais in which the direction ofthe pitch sequence of the missing fundamental was 09-pusitc to that of the component frequencies are shown.in Table II(c). Note that both animals maintained contactwhen the missing fundamental indicated a safe trialand broke contact when it indicated a warning trial(p < 0.002, two-tailed distribution). Indeed, the performancesof the animals were so consistent that thedistributions of the safe and warning scores did notoverlap. This result suggests that the cats were notresponding to the component frequencies of the triadand may have been responding tothe missingfundamental.The investigation of the missing fundamental in humanshas suggested that the phenomenon does not occurfor center frequencies above about 5 kHz (Schouten,1070). To further explore the ability of cats to respondto these signals, cat 2 was tested using triadswith center frequencies of 3, 4, 5, and 6 kHz.Figure 2 shows the performance of the animal whenthe missing fundamental and the triad signaled the samecondition (i.e., both indicated safe or warning) andwhen they signaled opposite conditions. The decline inperformance in the latter condition indicates that whatevercue the animal was relying an at 2 kHz (the missingfundamental in our hypothesis) is progressivelylost as the center frequency is raised, until at 6 kHzperformance ts not above chance. There was a paralleldecline in performance when the missing fundamentaland triad indicated the same condition, suggesting0-80-4CAT - 20-2 S2 3 4 5 6CENTER FREQUENCY (kHz)FIG. 2. Performance of cat 2 on the missing fundamental testusing center frequencies of 2, 3, 4, 5, and 6 kHz. Scoreswere abtained under two conditions: the missing fundamentaland the frequencies composing the trials shifting in thesame (S) and opposite (O) directions. Note that performancein both conditions declines as center frequency is increased.(ns indicates that performance was not above chance, p > 0.05. ),J. Acoust. Soc. Am., VoL 59, No. 4, April 1976

919 Heftnet and Whitfield: Perception of the missing fundamental by cats 919that the animal does not switch to using the componentfrequencies when the fundamental cue disappears.III.DISCUSSIONThe results of this study strongly suggest that catsexperience something similar to, if not identical with,the perception of the missing fundamental in humans.The response of the animals in the test condition wasnot in conformity with that expected from the directionof change of the component frequencies of the triads,since, contrary to other training, the animals avoidedwhen the direction of the test signal was down and failedto avoid when it was up. However, their performancecould be accounted for if it were assumed that the catswere responding on the basis of a phenomenon in whichthe direction of pitch change was that of the missing fundamental.The additional tests given to cat 2 show a furtherparallel with results in humans. In the "opposition"situation where a correct response requires attentionto the missing fundamental cue, performance declinedprogressively as the center frequency was raised, untilat 6 kHz it was apparently completely absent. Inhumans there is a similar decline in the strength ofthe fundamental pitch over about the same range (e. g.,Sohourea, 1970).The entirely similar decline in performance by cat2 when the triads and the missing fundamental movedin the same direction suggests that the animal was unableto switch from the fundamental to the triad fre-quencies as the former declined. This further suggesisthat the animals were not using the triad frequenciesin any of the experimental situations, but thatthey always heard the pitch in the earlier experimentsas corresponding to that of the missing fundamental.It is necessary, of course, to consider the possibilitythat while there was no detectable external signalbelow 1 kHz, the animals could have been respondingto an intra-aurally generated difference tone. Plomp(1965) found that in man a difference tone of 400 Hz inthe midsing fundamental situation was just detectablewhen the intensity cg the harmonics forming the complexreached a level of about 70 dB SPL, there beinga good deal c• scatter between subjects. It is, however,begging the question to use human data in this contextand some intern,M evidence is to be preferred. Wesuggest that this might come also from the experimentswith higher center frequencies. Had the animals beenresponding to difference tones, they might well havebeen expected to do so whether these were generatedwith a 2- or a 5-kHz centerfrequency. To account fortheir actual behavior in such circumstances, it wouldbe necessary to postulate that the way the cat ear generatesdifference tones happens to decline with generatingfrequency in just the same way that the missingfundamental declines in man. A more realistic conclusionis that the animals were not able to use differ-ence tones to solve the problem.The discovery that cats may be able to perceive themissing fundamental is encouraging for the study ofauditory processing, because it suggests that the auditorysystem of cats is similar in this respect to thehuman auditory system. As a result, it may be possibteto compare the extensive data concerning psriodicitypitch gathered through p•ychophysical studieson humans with the physiological data concerning theauditory system obtained in the cat. Such comparisonscan then be used to determine the physiological mechanismswhich underlie the psychological phenomenaof hearing. Though further investigation is needed toestablish that the phenomenon observed in cats is identicalin every respect to that in man, we have at thistime no reason not to believe that cats do indeed perceivethe missing fundamental.*This work was supported by a grant from the Science ResearchCouncil.tCurreut address: Bureau of Child Research, Parsons StateHospital and Training Center, Parsons, KS 67357.Butler, R. A. (1972). "The auditory evoked response to stimuliproducing periodicity pitch," Psychephysiology 9, 233-237.Heftnor, R., Heftnor, H., and Masterton, B. (1971). "Behavioralmeasurements of absolute and frequency-differencethresholds in guinea pig," J. Acoast. Sec. Am. 49, 1888-1895.Hind, J.E. (1972). "t'hysiological correlates of auditory stimulusperiodicity, "A udiology 11, 42-57.Kiang, N. Y-S., and Goldstein, M. H. (1959). "Tenetopic organizationof the cat auditory cortex for some complex stimuli,"J. Acoust. Sec. Am. 31, 786-790.Pierap, R. (1965). "Detectability threshold for combinationtones," J. Acoust. Sec. Am. 37, 1110-1123.Pierap, R., and Smoorenburg, G. F., Eds. (1970). FrequencyAnalysis and Periodicity Detection in Hearing (Sijthoff, Leizion,The Netherlands).Sohourea, J. ¾., (1979). "The residue revisited," in FrequencyAnalysis and Periodicity Detection in Hearing, editedby R. Plomp and G. F. Smoorenburg (Sijthoff, Leiden, TheNetherlands), pp. 41-54.Schouten, J. F., Ritsma, R. J., and Cardoze, B. L. (1962)."Pitch of the residue," J. Acoust. Sec. Am. 34, 1418-1424.Siegel, S. (1956). Nonpara,r, etric Statistics (McGraw-Hill,New York).Small, A.M. R., and Gross, N. B. (1962). "Response of thecerebral cortex of the cat to repetitive acoustic stimuli," J.Conap. Physio[. Psychol. 55, 445--448.Whitfield, I. C. (1970a). "Neural integration and pitch perception,"in E•cltatory Synal)tic Mechanisms, edited by P. Andersenand J. K. S. Jansen (Universitetsforlaget, Oslo),pp. 277-285.Whitfield, I. C. (1970b). "Can nerve impulse periodicity beused for pitch perception?" in Ciba Foundation Symposium onSe•zsorin½•'al HearingLoss, edited by G. E. W. Wolstenho[meand J. Knight (Churchill, London), pp. 213-223.J. Aooust. Soc. Am., Vol. 59, No. 4, April 1976