Dosch, HG

Hauck, M

Patterson, RD

Rupp, A

English

Apollo (Cambridge)

ACTA ACUSTICA UNITED WITH ACUSTICAVol. 104 (2018) 783 – 786DOI 10.3813/AAA.919223The Effect of Age on Huggins’ Pitch Processingand its Location in Auditory CortexAndré Rupp1), Matthias Hauck2), Hans Günter Dosch3), Roy D. Patterson4)1)Department of Neurology, Heidelberg University Hospital, Germany. andre.rupp@uni-heidelberg.de2)Physikalisches Institut, University of Heidelberg, Germany. matthias.hauck@uni-heidelberg.de3)Institut für Theoretische Physik, University of Heidelberg, Germany. h.g.dosch@thphys.uni-heidelberg.de4)Department of Physiology, Development and Neuroscience, University of Cambridge, UK. rdp1@cam.ac.ukSummaryThis paper begins with a description of a behavioural experiment with 72 listeners, 8–84 years of age, whichshows that the upper frequency limit of Huggins’ pitch (HP) decreases steadily with age. Subsequently, transientauditory-evoked-field (AEF) responses to the onset of HP and a change in HP were recorded from a subset of 21of these listeners, 18–75 years of age. These neuromagnetic (MEG) responses were then compared to the onsetand change responses produced by a monaural pitch-producing stimulus, namely, iterated rippled noise (IRN:Yost, 1996), and to a binaural control stimulus composed of broadband noise where a perceptual change wasproduced by inverting the interaural correlation from +1 to −1 or vice versa.Source analyses revealed that the pitch onset responses (PORs) and the pitch change responses (PCRs) were lo-cated in the lateral portion of Heschl’s gyrus (HG), whereas the correlation-change responses (CCRs) associatedwith the control noise were located in planum temporale (PT), along with the energy onset responses (EORs).Correlation analyses of these neuromagnetic responses with age revealed a somewhat complicated pattern of spe-cific effects: The amplitudes of the PORs and PCRs evoked by HP were smaller for increasing age, and the CCRswere smaller in the older listeners. Moreover, the latencies of the POR and PCR to IRN stimuli were longer forthe older listeners. However, the amplitude of the IRN responses did not correlate with age.© 2018 The Author(s). Published by S. Hirzel Verlag · EAA. This is an open access article under the terms of theCreative Commons Attribution (CCBY4.0) license (https://creativecommons.org/licenses/by/4.0/).PACS no. 43.64.-q, 43.66.-x1. IntroductionWhen a diotic white noise is presented to both ears, wehear one source in the middle of the head. If a linear, 2π,phase shift is imposed across a narrow frequency band atone ear, listeners hear a Huggins’ pitch (HP; [1]) in addi-tion to the noise. If the waveform of the noise at one ear isinverted, this interaural correlation of −1 results in the per-ception of a spatially diffuse noise without a pitch. Theseinteraural phase effects grow weaker with age, and there issome evidence to indicate binaural listening tasks are gen-erally more difficult for older listeners [2]. It is assumedthat this reflects an age related-reduction in the accuracy ofphase locking or subsequent time-interval processing. Inan MEG imaging study, Matilainen et al. [3] observed anincrease in the delay of the N100m peak in older listeners,when presented either with tone pips or a speech sound.They did not, however, find corresponding differences inthe amplitudes of these MEG transients. Together, theseReceived 5 May 2018,accepted 17 August 2018.studies prompted us to examine the effect of age on theupper and lower frequency limits of Huggins’ pitch andthe early components of the MEG responses they evoke.For comparison we recorded transient MEG responses toPORs and PCRs produced with diotic IRN, and the CCRproduced by the inversion of the noise waveform at oneear.2. Methods2.1. Experiment 1The first experiment was conducted to assess the upperand lower frequency limit of HP. Seventy-two subjects (32female/40 male; 8–84 years) were included in the study.Listeners younger than 49 years of age had audiometricthresholds better than 25 dBHL between 125 and 8,000Hzwith between ear differences <15 dB. The older listeners(50–84 years) had audiometric thresholds less than 25 dBHL between 125 and 500Hz and less than 40 dB between1,000 and 4,000Hz (between ear differences <15 dB).Both the upper and the lower frequency limits of HP wereassessed using a 3-AFC, 2-up/1-down adaptive procedure© 2018 The Author(s). Published by S. Hirzel Verlag · EAA.This is an open access article under the terms of the CC BY 4.0 license. 783ACTA ACUSTICA UNITED WITH ACUSTICA Rupp et al.: Huggins’ pitch processingVol. 104 (2018)[4]. Listeners were presented with three 800-ms noisebursts and were asked to identify the one which containedthe HP. The HP stimuli were broadband Gaussian noiseswith a 2π-phase transition in the right channel. The band-width of the phase transition was set to 10% of the HPfrequency. The interaural phase difference was centered atf0of HP. The starting f0in the adaptive runs was 400Hzand the change-factor for an increase or decrease in f0was1.5. After two reversals the change-factor was set to 0.75.Fresh noise samples were used on every trial. The adap-tive runs terminated after 15 reversals and threshold wastaken to be the average value of the last six turnarounds.For each condition, we recorded one run. The stimuli werepresented at 65 dB SPL using Etymotic Research (ER-3)earphones equipped with 90 cm plastic tubes.2.2. Experiment 2AEFs were recorded in a subset of 21 adult listeners (16male/5 female; 18–76 years). The differences betweentheir left and right audiometric thresholds were invari-ably less than 10 dB. Measurement of the upper frequencylimit of HP always preceded recoding of their MEG re-sponses. The IRN stimuli were created with 20 iterationsof the delay-and-add manipulation; the delay was adjustedto produce the same set of pitches as for the HP sounds.2.3. MEG recordings and analysisThe neuromagnetic response to the stimuli was measuredwith a Neuromag-122 (Electa Neuromag Oy) gradiome-ter system. Data were sampled at 1000Hz and low-passfiltered at 330Hz. During the passive measurements sub-jects watched a silent video of their own choice to maintainvigilance.In order to separate energy onset responses (EORs)from pitch onset responses (PORs) and pitch change re-sponses (PCRs) the stimulus on each trial was composedof three 750-ms segments. For the IRN- and Huggins’pitch conditions, we always applied a triple composed ofa noise burst without pitch followed by a segment with adistinct f0and a third segment with a different f0. Thef0of the first sound after the initial noise burst was set to220, 880, or 1760Hz. The second sound was either a per-fect 5thup or down from the first. Correlation change re-sponses (CCRs) were measured using trials composed oftwo 750-ms Gaussian noise bursts between which correla-tion changed from +1 to−1 or vice versa. In order to avoidmonaural energy cues at the transitions, crossfading wasaccomplished using square-rooted 10ms Hanning ramps.Stimulus onset and offsets were shaped by a 50ms Han-ning ramp. Each condition was presented 200 times. Theinter-sequence silent interval was randomly chosen fromthe range 800–900ms.Spatio-temporal source analysis [5] was performedoffline using the BESA 5.2 software package (BESAGmbH). After the elimination of artefacts (amplitudes> ±8000 fT/cm and gradients > ±800 fT/cm/ms), sep-arate source models, with one equivalent dipole in eachhemisphere, were created to analyse the transient N100mTalairach X (mm)-50 -40-30-20-10 1020 30 40 50Talairach X (mm)-40-40-50-30-2020304050-30-20-100Huggins PCRIRN PCRHuggins PORIRN PORHuggins EORIRN EORCCR EORCCR -1/+1 +1/-1Talairach x (mm)Talairachy(mm)0 250 500 750 1000 1250 1500 1750 2000 2250 2500025noise pitch 1 pitch 20 250 500 750 1000 1250 1500 1750 2000 2250 2500025noise pitch 1 pitch 20 250 500 750 1000 1250 1500 1750 2000 2250 2500Time (ms)050CCR 1 CCR 242 years> 42 yearsPORPCRN100onCCR-1 +1CCR TransitionHuggins PitchIterated Rippled Noise220 Hzf0pitch 1880 Hz1760 Hz220 Hzf0pitch 1880 Hz1760 Hz+1 -1ABanteriorposteriorHGPT25nAm25nAm25nAmFigure 1. (Colour online) (A) Projection of the 2-dipole sourcelocations onto a standard map of auditory cortex [6]. The errorbars denote the standard error. The POR and PCR sources pro-duced by IRN and HP stimuli are located on, or close to, HG; theenergy onset sources (EOR) and the CCR sources are located be-hind HG in PT. (B) Grand-average source waves (pooled acrosshemispheres) in response to IRN (top panel), HP (middle panel)and correlation-inversion noise (bottom panel), with black wavesfor the younger listeners and red waves for the older listeners.deflections of the EORs at the start of a trial and the PORs,PCRs, and CCRs at stimulus segment transitions. A 1–30Hz bandpass filter was applied to restrict the fits tothe appropriate frequencies in the data. Analysis of vari-ance was employed to search for spatial separation of thetransient EOR, POR, PCR and CCR generators along theanterior-posterior axis. In order to illustrate the effect ofage, we plottet the data from participants below and abovethe median age (<= 42 (mean: 29.1 y) vs > 42 years784Rupp et al.: Huggins’ pitch processing ACTA ACUSTICA UNITED WITH ACUSTICAVol. 104 (2018)000020202020404040406060606080808080100100100100Age (Years)01234Frequency(kHz)r =.79, p<0.0001Age (Years)00.050.10.150.20.25Frequency(kHz)r=.49, p<0.0001Age (Years)01234Frequency(kHz)r=.79, p<0.0001Age (Years)00.050.10.150.20.25Frequency(kHz)r=.39, n.s.A BC DFigure 2. The perceptual upper (A) and lower (B) frequencylimit of Huggins’ pitch as a function of age, for the full set of72 listeners. (C) and (D) depicts the upper and lower frequencylimit for the subset of 21 listeners who participated in the MEG-experiment.20202020202040404040404060606060606080808080808090100110120130140150Latency(ms)IRN POR - Latency-80-60-40-200Amplitude(nAm)IRN POR - Amplitude100150200250Latency(ms)HP POR - Latency-20-15-10-505Amplitude(nAm)HP POR - AmplitudeAge (Years)120140160180200Latency(ms)CCR - LatencyAge (Years)-60-40-200Amplitude(nAm)CCR - Amplituder=.71**r=-.08r=.43*r=.45*r=.58**r=.52*Figure 3. The correlation of age with the latency (left panels)and amplitude (right panels) for the IRN-POR (pooled across allf0-conditions), the HG-POR (the middle f0conditions), and theCCR (pooled across the +1/−1 and −1/+1 transitions).(mean: 60.1 y); see Figure 1B). Pearson correlation co-efficients were used to assess the correspondence betweenage and the latencies and amplitudes of the transient MEG-0.4-0.4-0.2-0.20.00.00.20.20.40.40.60.60.80.81.01.01.21.2Factor 1-0.4-0.200.20.40.60.81Factor3EOR AmpEOR LatIRN Off AmpIRN Off LatCCR AmpCCR LatIRN POR AmpIRN POR LatIRN PCR AmpIRN PCR LatHP POR AmpHP POR LatHP PsyAgeFactor 2-0.4-0.200.20.40.60.81Factor3EOR AmpEOR LatIRN Off AmpIRN Off LatCCR AmpIRN POR AmpIRN POR LatIRN PCR AmpIRN PCR LatHP POR AmpHP POR LatHP PsyAgeCCR LatABFigure 4. Scores of a factor analysis with three factors. Age isassociated with the perceptual upper frequency limit of Hug-gins’ pitch, the latency of the IRN-POR, HP-POR amplitude andCCR amplitude. In contrast, the amplitudes of the IRN-POR andIRN-PCR, as well as the amplitudes of the EOR-onsets and IRN-offsets, are more closely associated with orthogonal Factor 1.responses. Finally, the structure of the correlation matrixwas analysed with the aid of a factor analysis in whichVARIMAX rotation was applied.3. ResultsFigure 2 shows that the upper frequency limit of Huggins’pitch decreases significantly with age, and the reductionbegins at a relatively early age. The correlation coefficientr = .79 is the same for the large group in the behaviouralexperiment (upper left panel) and the subset who partici-pated in the MEG experiment (lower left panel). In con-trast, the lower frequency limit exhibited a small, but sig-nificant, increase with age.The fitting of 2-dipole models was successful for all ofthe onsets and transitions. The PORs and PCRs are foundto originate from Heschl’s gyrus (HG), while the EORsand CCRs come from more posterior regions in planumtemporale (see Figure 1A). An ANOVA revealed thatthe anterior-posterior differences were highly significant(POR-IRN vs EOR-IRN: F (1, 20) = 20.83, p < 0.001;POR-HP vs EOR-HP: F (1, 20) = 20.51, p < 0.001). The785ACTA ACUSTICA UNITED WITH ACUSTICA Rupp et al.: Huggins’ pitch processingVol. 104 (2018)locations of the HP and IRN PORs did not differ signifi-cantly (F (1, 20) = 0.001, p = 0.99).The grand-average source waves are presented in Fig-ure 1B. Since the grand-average waves for all conditionsfrom the left and right hemispheres (not shown) were verysimilar, we averaged the data of both hemispheres. Peak-picking on the AEF waves was successful for all stimulusconditions of all subjects, except for the HP-POR and PCRresponse to high and low f0-conditions. The waves in theupper panel of Figure 1B and the related correlation coeffi-cients in Figure 3 show that the POR and PCR latencies ofolder listeners were greater than those of younger listen-ers, whereas the corresponding amplitudes did not covarywith age. In contrast, HP-POR amplitudes in the mediumf0-range were lower for elderly listeners. Moreover, theCCRs showed both age effects, that is, a significant in-crease in latency and a significant decrease in amplitudewith age (see also Figure 3).Age was significantly correlated with IRN-POR latency,but not with IRN-POR amplitude. In contrast, the latenciesand amplitudes of the HG-POR and the CCR were moder-ately, but significantly, correlated with age. This pattern ofeffects is reflected in the factor analysis which included la-tency and amplitude data for onsets, offsets, PORs, PCRs,CCRs, ’perceptual upper frequency limit of HG’, and age(see Figure 4). The factor pattern shows that factor 3 isassociated with age, the upper limit of HP and the ampli-tudes of binaural responses, whereas factor 1 is associatedwith monaural amplitude. In contrast, factor 2 is associ-ated with latency. Interestingly, the CCR amplitudes ex-hibit medium loading on factors 1 and 3 which is in linewith the scatter plots shown in Fig. 3. Similarly, IRN-PORlatency presents a complex pattern with substantial load-ing on factors 2 and 3.3.1. ConclusionsThe data from the two experiments confirm that age has astrong impact on the upper frequency limit of HP and thereduction of this limit begins before there is pronouncedhearing loss. The MEG data show that the latency of theN100m increases with age and the amplitude decreaseswith age for binaural stimuli. For monaural noise and pitchstimuli, the situation is more complicated; the latency ofthe POR increases but there is no evidence of a reduc-tion in the amplitude. These findings are in line with theobservations of [3] and show that the central effects ofage are more readily observed with binaural phenomena,as might be expected. In order to dissociate central agingeffects from peripheral deterioration, further experimentsneed to include listeners with and without hearing loss ascarried out by Santurette et al. [7] who observed that per-ception of Huggins’ pitch was not strongly associated withaudiometric threshold but with deficits in temporal fine-structure processing. Nevertheless, the strong age-specificcorrelation between psychometric and neuromagnetic re-sponses to HP stimuli, and the observation that AEF re-sponses evoked by onsets and transitions to monaural andbinaural stimuli exhibited a disjunct response pattern, to-gether suggest that neuromagnetic responses to HP stimulicould be employed to separate age-related auditory defi-ciencies from other pathological processes objectively.References[1] E. M. Cramer, W. H. Huggins: Creation of pitch through bin-aural interaction. J Acoust Soc Am 30 (1958) 413–417.[2] B. Ross, T. Fujioka, K. L. Tremblay, T. W. Picton: Aging inbinaural hearing begins in mid-life: evidence from corticalauditory-evoked responses to changes in interaural phase. JNeurosci 27 (2007) 11172–11178.[3] L. E. Matilainen, S. S. Talvitie, E. Pekkonen, P. Alku, P. J.C. May, H. Tiitinen: The effects of healthy aging on audi-tory processing in humans as indexed by transient brain re-sponses. Clinical Neurophysiol 121 (2010) 902–911.[4] H. Levitt: Transformed up-down methods in psychoacou-stics. J Acost Soc Am 49 (1971) 467–477.[5] M. Scherg: Fundamentals of dipole source analysis. In: Au-ditory Evoked Fields and Potentials. Edited by F. Grandori,M. Hoke and G. L. Romani. Basel: Karger, (1990) 40–69.[6] C. M. Leonard, C. Puranik, J. M. Kuldau, L. J. Lombardino:Normal variation in the frequency and location of human au-ditory cortex landmarks. Heschl’s gyrus: where is it? CerebCortex 8 (1998) 397–406.[7] S. Santurette, T. Dau: Relating binaural pitch perceptionto the individual listeners’s profile. J Acoust Soc Am 131(2012) 2968–2986.786

The effect of age on huggins’ pitch processing and its location in auditory cortex

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The effect of age on huggins’ pitch processing and its location in auditory cortex

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