© 2018 The Author(s). We have recorded the responses of single units in the superior olivary complex (SOC) of the Guinea pig to simple and complex stimuli. We can readily identify the responses of the four principal ascending nuclei as described in other species and we are therefore confident that the Guinea pig is a suitable model for studying this region. We found single units in the medial superior olive that represent both diotic iterated rippled noise and dichotic repetition pitch in their temporal discharge patterns. Our data demonstrate a use of the SOC beyond sound-source localisation

Alsindi, S

Patterson, RD

Sayles, M

Winter, IM

English

Apollo (Cambridge)

ACTA ACUSTICA UNITED WITH ACUSTICAVol. 104 (2018) 856 – 859DOI 10.3813/AAA.919240The Responses of Single Units to Simple andComplex Sounds from the Superior OlivaryComplex of the Guinea PigSami Alsindi1), Roy D. Patterson1), Mark Sayles2), Ian M. Winter1)1)Department of Physiology, Development and Neuroscience, Downing Street, University of Cambridge,United Kingdom. imw1001@cam.ac.uk2)Brainstem Neurophysiology Laboratory, Weldon School of Biomedical Engineering & Department of Speech,Language and Hearing Sciences, Purdue University, West Lafayette, IN 47907, U.S.A.SummaryWe have recorded the responses of single units in the superior olivary complex (SOC) of the guinea pig to simpleand complex stimuli. We can readily identify the responses of the four principal ascending nuclei as describedin other species and we are therefore confident that the guinea pig is a suitable model for studying this region.We found single units in the medial superior olive that represent both diotic iterated rippled noise and dichoticrepetition pitch in their temporal discharge patterns. Our data demonstrate a use of the SOC beyond sound-sourcelocalisation.© 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. IntroductionThe superior olivary complex consists of a group of audi-tory nuclei in the mammalian brainstem. Two of the largestnuclei, the medial superior olive (MSO) and lateral supe-rior olive (LSO), receive bilateral, direct and/or indirectinputs, from the bushy cells of the ventral cochlear nucleuson both sides and are thus major sites of binaural integra-tion. Not surprisingly, previous physiological studies haveexamined the role of the MSO and LSO in sound localisa-tion. Here we examine, for the first time, the responses ofsingle units in the guinea pig SOC to simple and complexsounds, including stimuli that can evoke a binaural pitchin humans.Human psychoacoustic studies have demonstrated strik-ing “binaural pitch” phenomena. These pitch percepts areproduced by sounds that, presented to either ear on its own,evoked no pitch [1, 2]. One such example is dichotic rep-etition pitch (DRP), consisting of Gaussian noise with asmall inter-aural time difference (ITD) [1]. Neural pro-cessing to combine information from the two ears is essen-tial for this aspect of pitch perception. Here, we demon-strate neural correlates of binaural pitch in the temporaldischarge patterns of single units in the MSO. The MSO iswell known to perform inter-aural computations that repre-sent inter-aural time differences. Analysis of the temporalReceived 4 March 2018,accepted 15 August 2018.discharge patterns of MSO units to diotic iterated ripplednoise, and dichotic repetition pitch reveal a neural corre-late of the pitch of these stimuli. These findings suggest arole for the MSO in the neural machinery underlying bin-aural pitch.2. MethodsOur methods are described in detail elsewhere [3], so onlya brief description is given here. Data were obtained fromnormal-hearing (based on round-window CAP thresh-olds), anaesthetised and normothermic, pigmented guinea-pigs (Cavia porcellus). Experiments were performed inaccordance with the Animals (Scientific Procedures) Act1986 (Amendment Regulations 2012) following ethicalreview by the University of Cambridge Animal Welfareand Ethical Review Body.An estimate of inter-aural crosstalk attenuation was ob-tained from single ventral cochlear nucleus units by mea-suring the difference between monaurally-evoked spikingresponses to BF tones presented ipsi-laterally and contra-laterally. Between 0.10- and 2.00-kHz, the attenuation wasgreater than 50 dB. This, combined with our relatively lowsignal levels, means that the results are unlikely to be con-taminated by inter-aural acoustic crosstalk.Glass-insulated tungsten microelectrodes were posi-tioned at the surface of the dorsal cochlear nucleus (DCN)under operating-microscope control, and advanced para-sagittally through the brainstem at 45◦to the horizontal856© 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.Alsindi et al.: Responses of olivary complex ACTA ACUSTICA UNITED WITH ACUSTICAVol. 104 (2018)plane using a hydraulic microdrive. Signals from the mi-croelectrode were amplified (×1000) and bandpass filtered(0.3–10 kHz) before online spike discrimination and tim-ing. Spike times were stored for offline analysis (10 µs res-olution). Superior olivary complex units were defined asthose found at depths greater than 3.3mm from the surfaceof the DCN. The presence of a neurophonic in response tomonaural or binaural stimulation with low-frequency puretones gave an initial indication that the electrode was closeto the MSO or the low frequency limb of the LSO. Recep-tive fields were measured using 50-ms pure tones, gatedwith 5-ms cos2 ramps. For neurons with BFs <5 kHz, thefrequency range was 3 octaves below unit BF to 2-octavesabove, for units with BFs 5 kHz or above, tone frequen-cies ranged from 2 octaves below BF to 1 octave above.For binaural neurons, receptive fields were measured toipsilateral-only, contralateral-only and diotic tone presen-tations.We collected spike times in response to several pitchstimuli. These included: diotic iterated rippled noise(Gaussian noise delayed and added back to itself [combfiltering], identical in both ears), and dichotic repetitionpitch (Gaussian noise with a small ITD between the twoears).3. ResultsRecordings were made from all main divisions of the SOC:the superior paraolivary nucleus (SPN), the medial nu-cleus of the trapezoid body (MNTB), the lateral supe-rior olive (LSO) and the medial superior olive (MSO).Physiological response properties of the principal cellsof these nuclei have been characterised in other species.However, to our knowledge, responses from such units inthe guinea pig SOC have not been previously reported. Re-sponses to pure tones at unit BF, plotted as post-stimulustime histograms (PSTHs), were used to form an initialclassification. MNTB units showed a “primary-like” (PL)PSTH shape or a “primary-like with notch” (PN) shape,and the characteristic three-component spike-waveformshape reported in other species (Figure 1A). SPN unitsshowed chopper-like responses at stimulus offset (Fig-ure 1B), and sensitivity to gaps between tones. We alsoconfirmed interaural phase difference (IPD)-sensitivity inlow-BF binaurally-responsive cells of the LSO and MSO,using binaural-beat stimuli (Figures 1C and 1D). MSOunits responded weakly to monaural stimulation but morestrongly to diotic stimulation, with many units showingbinaural facilitation. LSO units were sensitive to inter-aural level differences of BF tones (Figure 1F).The microelectrode recording of an MSO unit to stim-ulation with binaural beats is shown in Figure 2A. Thisshows three clusters of spikes during the stimulus pre-sentation, corresponding to the best IPD in each 1 sec-ond beat period. Figure 2B shows an expanded segmentof the same recording to show the presence of the drivenneurophonic, readily identifiable as the approximately si-nusoidal oscillation of the background noise. The oscil-Figure 1. Physiological signatures of the main cell types inthe principal nuclei of the superior olivary complex. A & B)post-stimulus time histograms in response to supra-threshold BFtone bursts from the MNTB (BF = 12.5 kHz) and SPN (BF= 15.64 kHz), respectively. Below each histogram is the cor-responding dot-raster plot. The horizontal bar above each his-togram represents the stimulus duration. C) Response of an MSOunit (BF = 0.13 kHz) to binaural beats at BF and E) an exem-plar composite delay curve. D) Responses of an LSO unit (BF= 0.39 kHz) to binaural beats at BF and F) an exemplar ILDfunction. Average spike waveform shapes are shown as insets forplots A-D. Note the signature three-component shape for MNTBunits (inset in A).lation frequency was quantified by an FFT of the elec-trode trace for two time-windows. The first was in the pres-ence of the driven neurophonic and the second was in thelater 3 seconds of the recording, when the stimulus wasswitched off (the spontaneous neurophonic – Figure 2C).Figure 2D shows a clear peak in the spectrum of the wave-form around the stimulus frequency of the binaural beatstimulus 333/334Hz in the driven neurophonic condition857ACTA ACUSTICA UNITED WITH ACUSTICA Alsindi et al.: Responses of olivary complexVol. 104 (2018)Figure 2. (A) A microelectrode trace showing a single MSO unit responding with a burst of action potentials at the 1s period of abinaural beat stimulus. The duration of the beat stimulus (3 seconds) is shown by the black bar. The driven neurophonic is clearly seenas an amplitude modulation in the second trace [B] which is an expanded section of the waveform in A. The spontaneous neurophonic(in the absence of controlled acoustic stimulation) is shown in C. The frequency of the neurophonic potential is shown in [D] by thepeak just below 350Hz in the spectra of the traces shown in B and C. The carrier frequencies of the binaural beat were 333 and 334Hz.The spectrum shown by the black line is the electrode noise recorded when the stimulus is off (see scale in A). Facilitation in responseto diotic tone bursts for two MSO units is shown in the lower row. In (E) the monaural receptive fields are non-existent while the dioticreceptive field (BF = 0.46 kHz) shows conventional tuning. For comparison, the continuous blue line is the frequency-threshold curveof a similar BF filter recorded from a single unit in the ventral cochlear nucleus of the guinea pig. In (F) we show a unit that showedweak excitatory responses in the monaural receptive fields. BF was estimated as 0.74 kHz.but not in the stimulus-off (spontaneous neurophonic) con-dition.The facilitation to diotic tones is illustrated in Figures2E and F which show ipsi-lateral, contralateral and dioticreceptive fields for two MSO units. In the first unit (Fig-ure 2E) the monaural response, both ipsilateral and con-tralateral, is very weak or non-existent [0, 0] while the di-otic response shows a conventional “V” shaped response.This type of response was observed for 29% of our MSOunit population. In contrast, the second unit (Figure 2F)shows a tuned response to monaural stimulation of eitherear [E, E], with a stronger response to diotic stimulation.This [E, E] pattern was found for 41% of our MSO units.This percentage is lower than seen in the dog (65%, [3]),cat (58%, [4]) and the gerbil (67% [5]).Figure 3 shows the responses of a single MSO unit todiotic iterated rippled noise (IRN) and dichotic repetitionpitch (DRP). The IRNwas generated for one iteration withpositive gain at three delays, 8, 16 and 32ms. There is aclear peak in the all-order inter-spike interval histogramfor each of the delays. It is important to note that the IRNwas presented diotically, and the neural representation ofthe corresponding pitch is available in monaural neural-inputs. In contrast, DRP is generated by presenting broad-band noise to one ear and the same noise, delayed by τms,to the other ear. DRP is a dichotic pitch, requiring binauralinteraction.Humans do not report the pitch corresponding to 1/τto be lateralized; it is heard in the centre of the head. Ifboth the delayed and un-delayed noise waveforms are inFigure 3. (A) The responses of a single MSO unit (BF =0.25 kHz) to IRN with 1 iteration presented diotically for threedifferent IRN delays (but zero ITD). In (B), we see the responsesof the same unit to DRP with the same three delays presentedas ITDs. The all-order interspike interval histograms are plottedwith a binwidth of 0.2ms. The asterisks mark the stimulus delay.phase (DRP+), the pitch is unambiguous at 1/τ. When abroadband phase shift of τ is applied to the delayed noise(DRP–), the DRP is ambiguous, being either ∼ 0.9/τ or∼ 1.1/τ [6].This result is very similar to that of the more familiarmonaural repetition pitch, that is “[iterated] rippled noise”858Alsindi et al.: Responses of olivary complex ACTA ACUSTICA UNITED WITH ACUSTICAVol. 104 (2018)Figure 4. Responses of a single MSO unit (BF = 0.13 kHz) to1 iteration of diotic iterated ripple noise at a delay of 8ms andeither 1 or 16 iterations for both positive and negative gain. Thelack of response by the same cell to positive and negative DRP isalso shown (C). The all-order interspike interval histograms areplotted with a binwidth of 0.2ms.[6]. In Figure 3B, a clear peak can be seen (red asterisks)in the all-order inter-spike interval histograms in responseto the same three delays shown in Figure 3A.It should be noted that only 3 of 11 MSO units in ourdataset showed a clear correlate of DRP in their inter-spikeinterval distributions. In contrast, all of our MSO unitsshowed a clear neural correlate of the pitch of diotic IRN.Figure 4 shows an example of an MSO unit with a cleartemporal representation of the pitch of IRN with 16 itera-tions, but only a weak representation of the pitch of IRNwith 1 iteration. This could be interpreted as reflecting thesalience of IRN pitch. However, this same MSO unit failsto show responses at the delay in the DRP stimulus (4C).4. DiscussionWe have recorded the responses of single units in the su-perior olivary complex (SOC) of the guinea pig to sim-ple and complex stimuli. We can readily identify the re-sponses of the four principal ascending nuclei as describedin other species and we are therefore confident that theguinea pig is a suitable model for studying this region.We also demonstrated that single units in the MSO canrespond to the pitch of diotic IRN, even with a single it-eration. Humans only hear a weak pitch with one itera-tion. A small subset (3/11) of the same units showed aneural correlate to the pitch of DRP. Although DRP pro-duces a rather weak pitch percept, it is currently unknownwhy only a subset of MSO units responded to DRP. Onepossibility is a mismatch in best frequency of the ipsilat-eral and contralateral input filters to the MSO unit. Futurestudies should consider measuring the responses of singleSOC units to sounds which are capable of producing muchstronger binaural pitch percepts, such as dichotic complextones or Huggins pitch.AcknowledgementThis work was supported by an MRC PhD studentship toS. Alsindi.References[1] F. A. Bilsen, J. L. Goldstein: Pitch of dichotically delayednoise and its possible spectral basis. J Acoust Soc Am 55(292-296) 1974.[2] F. A. Bilsen, R. J. Ritsma: Repetition pitch and its implica-tion for hearing theory. Acustica 22 (1969/70) 63–73.[3] J. M. Goldberg, P. B. Brown: Functional organization of thedog superior olivary complex: An anatomical and electro-physiological study. Journal of Neurophysiology 31 (1968)639–656.[4] T. C. T. Yin, J. C. K. Chan: Interaural time sensitivity in themedial superior olive of cat. Journal of Neurophysiology 64(1990) 465–488.[5] A. Brand, O. Behrend, T. Marquardt, D. McAlpine, B.Grothe: Precise inhibition is essential for microsecond inter-aural time difference coding. Nature 417 (2002) 543–547.[6] M. Sayles, I. M. Winter: Ambiguous pitch and the tempo-ral representation of inharmonic iterated rippled noise inthe ventral cochlear nucleus. J Neurosci 28 (2008) 11925–11938.859

The responses of single units to simple and complex sounds from the superior olivary complex of the Guinea pig

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The responses of single units to simple and complex sounds from the superior olivary complex of the Guinea pig

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