Skip to main content

Binaural Hearing by the Mammalian Auditory Brainstem: Joint Coding of Interaural Level and Time Differences by the Lateral Superior Olive

  • Chapter
  • First Online:
Binaural Hearing

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 73))

Abstract

Two of the cues to sound source location in azimuth are the interaural difference in level (ILD) and time (ITD). ILDs result from the frequency- and direction-dependent modifications of sound by the head and pinnae and are defined as the difference in sound pressure level of sounds at the two ears. ITDs result because the ears are physically separated in space by the head, resulting in direction-dependent differences in acoustic path lengths to the ears. Although it has been known for decades that neurons comprising the lateral (LSO) and medial (MSO) superior olives in the brainstem are the most peripheral in the mammalian ascending auditory pathway to encode ILDs and ITDs, respectively, LSO neurons have recently been demonstrated to also be sensitive to ITDs. Here the mechanisms by which MSO neurons are sensitive to ITDs and LSO neurons can be jointly sensitive to ILD and ITD are reviewed. The physical bases of the ILD and ITD cues themselves are reviewed first. Next, the anatomical, physiological, and biophysical specializations of the circuitry that enable joint encoding of ILDs and ITDs by LSO neurons are examined. Specializations in the input neurons to the LSO permit both the spectral and temporal attributes of the sound arriving at the two ears to be represented accurately, and specializations in LSO neurons themselves allow not only ILDs but also ITDs to be encoded. Comparative studies in mammals that have examined the functional role of the LSO through combined anatomical, physiological, and behavioral observations confirm that the LSO is necessary for sound source localization based on ILDs and also particular kinds of ITDs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ashida G, Kretzberg J, Tollin DJ (2016) Roles for coincidence detection in coding amplitude-modulated sounds. PLoS Comput Biol 12(6):e1004997

    PubMed  PubMed Central  Google Scholar 

  • Ashida G, Tollin DJ, Kretzberg J (2017) Physiological models of the lateral superior olive. PLoS Comput Biol 13(12):e1005903. https://doi.org/10.1371/journal.pcbi.1005903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12(7):2819–2837

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beiderbeck B, Myoga MH, Muller NIC, Callan AR, Friauf E, Grothe B, Pecka M (2018) Precisely timed inhibition facilitates action potential firing for spatial coding in the auditory brainstem. Nat Commun 9(1):1771. https://doi.org/10.1038/s41467-018-04210-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benichoux V, Tollin DJ (2018) These are not the neurons you are looking for. eLife 7:e39244

    PubMed  PubMed Central  Google Scholar 

  • Benichoux V, Rebillat M, Brette R (2016) On the variation of interaural time differences with frequency. J Acoust Soc Am 139(4):1810. https://doi.org/10.1121/1.4944638

    Article  PubMed  Google Scholar 

  • Benichoux V, Brown AD, Anbuhl KL, Tollin DJ (2017) Representation of multidimensional stimuli: quantifying the most informative stimulus dimension from neural responses. J Neurosci 37(31):7332–7346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benichoux V, Ferber AT, Hunt SD, Hughes EG, Tollin DJ (2018) Across species ‘natural ablation’ reveals the brainstem source of a non-invasive biomarker of binaural hearing. J Neurosci 38:1211–1218

    Google Scholar 

  • Bledsoe SC Jr, Snead CR, Helfert RH, Prasad V, Wenthold RJ, Altschuler RA (1990) Immunocytochemical and lesion studies support the hypothesis that the projection from the medial nucleus of the trapezoid body to the lateral superior olive is glycinergic. Brain Res 517(1–2):189–194

    PubMed  Google Scholar 

  • Boudreau JC, Tsuchitani C (1968) Binaural interaction in the cat superior olive S segment. J Neurophysiol 31(3):442–454

    CAS  PubMed  Google Scholar 

  • Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B (2002) Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543–547

    CAS  PubMed  Google Scholar 

  • Bregman AS (1990) Auditory scene analysis: the perceptual organization of sound. Bradford Books, MIT Press, Cambridge, MA

    Google Scholar 

  • Brew HM, Forsythe ID (2005) Systematic variation of potassium current amplitudes across the tonotopic axis of the rat medial nucleus of the trapezoid body. Hear Res 206(1–2):116–132

    CAS  PubMed  Google Scholar 

  • Britt R, Starr A (1976) Synaptic events and discharge patterns of cochlear nucleus cells. I. Steady-frequency tone bursts. J Neurophysiol 39(1):162–178

    CAS  PubMed  Google Scholar 

  • Brown AD, Tollin DJ (2016) Slow temporal integration enables robust neural coding and perception of a cue to sound source location. J Neurosci 36(38):9908–9921

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown AD, Benichoux V, Jones HG, Anbuhl KL, Tollin DJ (2018) Spatial variation in signal and sensory precision both constrain auditory acuity at high frequencies. Hear Res 370:65–73

    PubMed  PubMed Central  Google Scholar 

  • Brownell WE, Manis PB, Ritz LA (1979) Ipsilateral inhibitory responses in the cat lateral superior olive. Brain Res 177(1):189–193

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caird D, Klinke R (1983) Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52(3):385–399

    CAS  PubMed  Google Scholar 

  • Caspary DM, Faingold CL (1989) Non-N-methyl-D-aspartate receptors may mediate ipsilateral excitation at lateral superior olivary synapses. Brain Res 503(1):83–90

    CAS  PubMed  Google Scholar 

  • Dobie RA, Berlin CI (1979) Binaural interaction in brainstem-evoked responses. Arch Otolaryngol 105(7):391–398

    CAS  PubMed  Google Scholar 

  • Finlayson PG, Caspary DM (1989) Synaptic potentials of chinchilla lateral superior olivary neurons. Hear Res 38(3):221–228

    CAS  PubMed  Google Scholar 

  • Ford MC, Alexandrova O, Cossell L, Stange-Marten A, Sinclair J, Kopp-Scheinpflug C, Pecka M, Attwell D, Grothe B (2015) Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing. Nat Commun 6:8073. https://doi.org/10.1038/ncomms9073

    Article  CAS  PubMed  Google Scholar 

  • Franken TP, Roberts MT, Wei L, Golding NL, Joris PX (2015) In vivo coincidence detection in mammalian sound localization generates phase delays. Nat Neurosci 18:444–452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Franken TP, Joris PX, Smith PH (2018) Principal cells of the brainstem's interaural sound level detector are temporal differentiators rather than integrators. eLife 7. https://doi.org/10.7554/eLife.33854

  • Glendenning KK, Masterton RB (1983) Acoustic chiasm: efferent projections of the lateral superior olive. J Neurosci 3(8):1521–1537

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glendenning KK, Masterton RB (1998) Comparative morphometry of mammalian central auditory systems: variation in nuclei and form of the ascending system. Brain Behav Evol 51(2):59–89

    CAS  PubMed  Google Scholar 

  • Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 22:613–636

    Google Scholar 

  • Grantham DW (1984) Discrimination of dynamic interaural intensity differences. J Acoust Soc Am 76(1):71–76

    CAS  PubMed  Google Scholar 

  • Greene NT, Davis KA (2012) Discharge patterns in the lateral superior olive of decerebrate cats. J Neurophysiol 108(7):1942–1953

    PubMed  PubMed Central  Google Scholar 

  • Greene NT, Anbuhl KL, Ferber AT, DeGuzman M, Allen PD, Tollin DJ (2018) Spatial hearing ability of the pigmented guinea pig (Cavia porcellus): minimum audible angle and spatial release from masking in azimuth. Hear Res 365:62–76

    PubMed  PubMed Central  Google Scholar 

  • Grothe B (2003) New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4:540–550

    CAS  PubMed  Google Scholar 

  • Grothe B, Pecka M (2014) The natural history of sound localization in mammals – a story of neural inhibition. Front Neural Circuits 8:116. https://doi.org/10.3389/fncir.2014.00116

  • Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90(3):983–1012

    CAS  PubMed  Google Scholar 

  • Harper NS, McAlpine D (2004) Optimal neural population coding of an auditory spatial cue. Nature 430:682–686

    CAS  PubMed  Google Scholar 

  • Hartmann WM, Constan ZA (2002) Interaural level differences and the level-meter model. J Acoust Soc Am 112:1037–1045

    PubMed  Google Scholar 

  • Helfert RH, Schwartz IR (1986) Morphological evidence for the existence of multiple neuronal classes in the cat lateral superior olivary nucleus. J Comp Neurol 244:533–549

    CAS  PubMed  Google Scholar 

  • Irvine DR (1986) The auditory brainstem: processing of spectral and spatial information. Springer, Berlin

    Google Scholar 

  • Jeffress LA (1948) A place theory of sound localization. J Comp Physiol Psychol 41(1):35–39

    CAS  PubMed  Google Scholar 

  • Jercog PE, Svirskis G, Kotak VC, Sanes DH, Rinzel J (2010) Asymetric excitatory synaptic dynamics underlie interaural time difference processing in the auditory system. PLoS Biol 8(6):e1000406. https://doi.org/10.1371/journal.pbio.1000406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jewett DL, Romano MN, Williston JS (1970) Human auditory evoked potentials: possible brain stem components detected on the scalp. Science 167:1517–1518

    CAS  PubMed  Google Scholar 

  • Johnson DH (1980) The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J Acoust Soc Am 68(4):1115–1122

    CAS  PubMed  Google Scholar 

  • Jones HG, Brown AD, Koka K, Thornton JL, Tollin DJ (2015) Sound frequency-invariant neural coding of a frequency-dependent cue to sound source location. J Neurophysiol 114(1):531–539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joris PX, Trussell LO (2018) The Calyx of held: a hypothesis on the need for reliable timing in an intensity-difference encoder. Neuron 100(3):534–549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joris PX, van der Heijden M (2019) Early binaural hearing: the comparison of temporal differences at the two ears. Annu Rev Neurosci 42:433–457

    CAS  PubMed  Google Scholar 

  • Joris PX, Yin TCT (1992) Responses to amplitude-modulated tones in the auditory nerve of the cat. J Acoust Soc Am 91:215–232

    CAS  PubMed  Google Scholar 

  • Joris PX, Yin TC (1995) Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J Neurophysiol 73(3):1043–1062

    Google Scholar 

  • Joris PX, Yin TCT (1998) Envelope coding in the lateral superior olive. III. Comparison with afferent pathways. J Neurophysiol 79(1):253–269

    CAS  PubMed  Google Scholar 

  • Joris P, Yin TCT (2007) A matter of time: internal delays in binaural processing. Trends Neurosci 30(2):70–78

    CAS  PubMed  Google Scholar 

  • Joris PX, Carney LH, Smith PH, Yin TCT (1994) Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71(3):1022–1036

    CAS  PubMed  Google Scholar 

  • Joris PX, Smith PH, Yin TCT (1998) Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21:1235–1238

    CAS  PubMed  Google Scholar 

  • Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577

    CAS  PubMed  Google Scholar 

  • Joris PX, Van de Sande B, Louage DH, van der Heijden M (2006) Binaural and cochlear disparities. Proc Natl Acad Sci 103:12917–12922

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karino S, Smith PH, Yin TCT, Joris PX (2011) Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re-examination. J Neurosci 31:3016–3031

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koka K, Tollin DJ (2014) Linear coding of complex sound spectra by discharge rate in neurons of the medial nucleus of the trapezoid body (MNTB) and its inputs. Front Neural Circuits 8:144. https://doi.org/10.3389/fncir.2014.00144

    Article  PubMed  PubMed Central  Google Scholar 

  • Koka K, Read HL, Tollin DJ (2008) The acoustical cues to sound location in the rat: measurements of directional transfer functions. J Acoust Soc Am 123(6):4297–4309

    PubMed  PubMed Central  Google Scholar 

  • Kuhn GF, Burnett ED (1977) Acoustic pressure field alongside a manikin's head with a view towards in situ hearing-aid tests. J Acoust Soc Am 62(2):416–423

    CAS  PubMed  Google Scholar 

  • Laback B, Dietz M, Joris PX (2017) Temporal effects in interaural and sequential level difference perception. J Acoust Soc Am 142(5):3267–3283

    PubMed  Google Scholar 

  • Laumen G, Ferber AT, Klump GM, Tollin DJ (2016) The physiological basis and clinical use of the binaural interaction component of the auditory brainstem response. Ear Hear 37(5):e276–e290. https://doi.org/10.1097/AUD.0000000000000301

    Article  PubMed  PubMed Central  Google Scholar 

  • Li K, Chan CHK, Rajendran VG, Meng Q, Rosskothen-Kuhl N, Schnupp JWH (2019) Microsecond sensitivity to envelope interaural time differences in rats. J Acoust Soc Am 145(5):EL341. https://doi.org/10.1121/1.5099164

    Article  PubMed  Google Scholar 

  • Loftus WC, Bishop DC, Saint Marie RL, Oliver DL (2004) Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. J Comp Neurol 472(3):330–344

    PubMed  Google Scholar 

  • Masterton B, Thompson GC, Bechtold JK, RoBards MJ (1975) Neuroanatomical basis of binaural phase-difference analysis for sound localization: a comparative study. J Comp Physiol Psychol 89(5):379–386

    CAS  PubMed  Google Scholar 

  • McAlpine D, Jiang D, Palmer AR (2001) A neural code for low-frequency sound localization in mammals. Nat Neurosci 4:396–401

    CAS  PubMed  Google Scholar 

  • Moore MJ, Caspary DM (1983) Strychnine blocks binaural inhibition in lateral superior olivary neurons. J Neurosci 3(1):237–242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park TJ, Klug A, Oswald JP, Grothe B (1998) A novel circuit in the bat’s midbrain recruits neurons into sound localization processing. Naturwissenschaften 85(4): 176–179

    Google Scholar 

  • Park TJ, Klug A, Holinstat M, Grothe B (2004) Interaural level difference processing in the lateral superior olive and the inferior colliculus. J Neurophysiol 92(1):289–301

    PubMed  Google Scholar 

  • Pecka M, Brand A, Behrend O, Grothe B (2008) Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J Neurosci 28(27):6914–6925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts MT, Seeman SC, Golding NL (2013) A mechanistic understanding of the role of feedforward inhibition in the mammalian sound localization circuitry. Neuron 78(5):923–935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanes DH (1990) An in vitro analysis of sound localization mechanisms in the gerbil lateral superior olive. J Neurosci 10(11):3494–3506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith PH, Joris PX, Yin TCT (1993) Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331:245–260

    CAS  PubMed  Google Scholar 

  • Song P, Yang Y, Barnes-Davies M, Bhattacharjee A, Hamann M, Forsythe ID, Oliver DL, Kaczmarek LK (2005) Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat Neurosci 8(10):1335–1342

    CAS  PubMed  Google Scholar 

  • Rayleigh L (1907) On our perception of sound direction. Philos Mag 6:13–74

    Google Scholar 

  • Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9(2):127–143

    PubMed  Google Scholar 

  • Tollin DJ, Koka K (2009) Postnatal development of sound pressure transformations by the head and pinnae of the cat: binaural characteristics. J Acoust Soc Am 126(6):3125–3136

    PubMed  PubMed Central  Google Scholar 

  • Tollin DJ, Yin TCT (2002a) The coding of spatial location by single units in the lateral superior olive of the cat. I. Spatial receptive fields in azimuth. J Neurosci 22(4):1454–1467

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tollin DJ, Yin TCT (2002b) The coding of spatial location by single units in the lateral superior olive of the cat. II. The determinants of spatial receptive fields in azimuth. J Neurosci 22(4):468–1479

    Google Scholar 

  • Tollin DJ, Yin TCT (2005) Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25:0648–10657

    Google Scholar 

  • Tollin DJ, Koka K, Tsai JJ (2008) Interaural level difference discrimination thresholds for single neurons in the lateral superior olive. J Neurosci 28(19):4848–4860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trussell LO (2002) Modulation of transmitter release at giant synapses of the auditory system. Curr Opin Neurobiol 12(4):400–404

    CAS  PubMed  Google Scholar 

  • Tsai JJ, Koka K, Tollin DJ (2010) Varying overall sound intensity to the two ears impacts interaural level difference discrimination thresholds by single neurons in the lateral superior olive. J Neurophysiol 103(2):875–886

    PubMed  Google Scholar 

  • van der Heijden M, Lorteije JA, Plauska A, Roberts MT, Golding NL, Borst JG (2013) Directional hearing by linear summation of binaural inputs at the medial superior olive. Neuron 78(5):936–948

    PubMed  PubMed Central  Google Scholar 

  • Wesolek CM, Koay G, Heffner RS, Heffner HE (2010) Laboratory rats (Rattus norvegicus) do not use binaural phase differences to localize sound. Hear Res 265(1–2):54–62

    PubMed  Google Scholar 

  • Wu SH, Kelly JB (1991) Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J Neurophysiol 65(2):230–246

    CAS  PubMed  Google Scholar 

  • Wu SH, Kelly JB (1994) Physiological evidence for ipsilateral inhibition in the lateral superior olive: synaptic responses in mouse brain slice. Hear Res 73(1):57–64

    CAS  PubMed  Google Scholar 

  • Yin TCT (2002) Neural mechanisms of encoding binaural localization cues. In: Oertel D, Fay RR, Popper AN (eds) Integrative functions in the mammalian auditory pathway. Springer, New York, pp 99–159

    Google Scholar 

  • Yin TCT, Chan JC (1990) Interaural time sensitivity in medial superior olive of cat. J Neurophysiol 64:465–488

    CAS  PubMed  Google Scholar 

  • Young ED, Davis KA (2002) Circuitry and function of the dorsal Cochlear nucleus. In: Oertel D, Fay RR, Popper AN (eds) Integrative functions in the mammalian auditory pathway. Springer New York, New York, pp 160–206

    Google Scholar 

  • Young ED, Oertel D (2004) Cochlear nucleus. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford University Press, New York, pp 125–163

    Google Scholar 

  • Zhang Y, Wright BA (2009) An influence of amplitude modulation on interaural level difference processing suggested by learning patterns of human adults. J Acoust Soc Am 126(3):1349–1358

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The work during the preparation of this chapter was supported by Grants R01-DC-011555 and R01-DC-017924 from the National Institute of Deafness and Other Communication Disorders (NIDCD), National Institutes of Health. We thank John Peacock and Monica Benson for comments.

Compliance with Ethics Requirements

Zoe L. Owrutsky declares that she has no conflict of interest.

Victor Benichoux declares that he has no conflict of interest.

Daniel J. Tollin declares that he has no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zoe L. Owrutsky .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Owrutsky, Z.L., Benichoux, V., Tollin, D.J. (2021). Binaural Hearing by the Mammalian Auditory Brainstem: Joint Coding of Interaural Level and Time Differences by the Lateral Superior Olive. In: Litovsky, R.Y., Goupell, M.J., Fay, R.R., Popper, A.N. (eds) Binaural Hearing. Springer Handbook of Auditory Research, vol 73. Springer, Cham. https://doi.org/10.1007/978-3-030-57100-9_5

Download citation

Publish with us

Policies and ethics