Abstract
Auditory spatial processing is an important ability in everyday life and allows the processing of omnidirectional information. In this review, we report and compare data from psychoacoustic and electrophysiological experiments on sound localisation accuracy and auditory spatial discrimination in infants, children, and young and older adults. The ability to process auditory spatial information changes over lifetime: the perception of the acoustic space develops from an initially imprecise representation in infants and young children to a concise representation of spatial positions in young adults and the respective performance declines again in older adults. Localisation accuracy shows a strong deterioration in older adults, presumably due to declined processing of binaural temporal and monaural spectro-temporal cues. When compared to young adults, the thresholds for spatial discrimination were strongly elevated both in young children and older adults. Despite the consistency of the measured values the underlying causes for the impaired performance might be different: (1) the effect is due to reduced cognitive processing ability and is thus task-related; (2) the effect is due to reduced information about the auditory space and caused by declined processing in auditory brain stem circuits; and (3) the auditory space processing regime in young children is still undergoing developmental changes and the interrelation with spatial visual processing is not yet established. In conclusion, we argue that for studying auditory space processing over the life course, it is beneficial to investigate spatial discrimination ability instead of localisation accuracy because it more reliably indicates changes in the processing ability.


Similar content being viewed by others
References
Abel SM, Hay VH (1996) Sound localization the interaction of aging, hearing loss and hearing protection. Scand Audiol 25(1):3–12
Abel SM, Giguere C, Consoli A, Papsin BC (2000) The effect of aging on horizontal plane sound localization. J Acoustic Soc Am 108(2):743–752
Amenedo E, Dıaz F (1998) Aging-related changes in processing of non-target and target stimuli during an auditory oddball task. Biol Psychol 48(3):235–267
Arnott SR, Alain C (2002) Stepping out of the spotlight: MMN attenuation as a function of distance from the attended location. Neuroreport 13(17):2209–2212
Ashmead DH, Clifton RK, Perris EE (1987) Precision of auditory localization in human infants. Dev Psychol 23(5):641–647
Babkoff H, Muchnik C, Ben-David N, Furst M, Even-Zohar S, Hildesheimer M (2002) Mapping lateralization of click trains in younger and older populations. Hear Res 165(1):117–127
Bamiou DE, Sisodiya S, Musiek FE, Luxon LM (2007) The role of the interhemispheric pathway in hearing. Brain Res Rev 56(1):170–182
Banai K, Sabin AT, Wright BA (2011) Separable developmental trajectories for the abilities to detect auditory amplitude and frequency modulation. Hear Res 280(1):219–227
Bennemann J, Freigang C, Schröger E, Rübsamen R, Richter N (2013) Resolution of lateral acoustic space assessed by electroencephalography and psychoacoustics. Front Psychol 4:338
Blauert J (1997) Spatial hearing: the psychophysics of human sound localization. MIT Press, Cambridge
Briley PM, Summerfield AQ (2014) Age-related deterioration of the representation of space in human auditory cortex. Neurobiol Aging 35(3):633–644
Briley PM, Kitterick PT, Summerfield AQ (2013) Evidence for opponent process analysis of sound source location in humans. J Assoc Res Otolaryngol 14(1):83–101
Brunetti M, Belardinelli P, Caulo M, Del Gratta C, Della Penna S, Ferretti A, Lucci G, Moretti A, Pizella V, Tartaro A, Torquati K, Olivetti Belardinelli M, Romani GL (2005) Human brain activation during passive listening to sounds from different locations: an fMRI and MEG study. Hum Brain Mapp 26(4):251–261
Burr D, Binda P, Gori M (2011) Multisensory integration and calibration in adults and in children. In: Trommershauser J, Kording K, Landy MS (eds) Sensory Cue Integration. Oxford University Press, Oxford, pp 173–194
Canlon B, Illing RB, Walton J (2010) Cell biology and physiology of the aging central auditory pathway. In: Gordon-Salant S, Frisina RD, Popper AN (eds) The aging auditory system. Springer, New York, pp 39–74
Chandler DW, Grantham DW (1991) Effects of age on auditory spatial resolution in the horizontal plane. J Acoustic Soc Am 89(4B):1994–1994
Clarey JC, Barone P, Imig TJ (1992) Physiology of thalamus a cortex. In: Popper AN, Fay RR (eds) The mammalian auditory pathway: Neurophysiology. Springer, New York, pp 232–334
Committee on Hearing and Bioacoustics and Biomechanics (CHABA) (1988) Speech understanding and aging. J Acoustic Soc Am 83:856–895
Cooper RJ, Todd J, McGill K, Michie PT (2006) Auditory sensory memory and the aging brain: a mismatch negativity study. Neurobiol Aging 27(5):752–762
Craik FI (2007) The role of cognition in age-related hearing loss. J Am Acad Audiol 18(7):539–547
Cruickshanks KJ, Wiley TL, Tweed TS, Klein BE, Klein R, Mares-Perlman JA, Nondahl DM (1998) Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin the epidemiology of hearing loss study. Am J Epidemiol 148(9):879–886
Czigler I, Csibra G, Csontos A (1992) Age and inter-stimulus interval effects on event-related potentials to frequent and infrequent auditory stimuli. Biol Psychol 33(2):195–206
Dawes P, Bishop DV (2008) Maturation of visual and auditory temporal processing in school-aged children. J Speech Lang Hear Res 51(4):1002–1015
Deouell LY, Bentin S, Soroker N (2000) Electrophysiological evidence for an early (pre-attentive) information processing deficit in patients with right hemisphere damage and unilateral neglect. Brain 123(2):353–365
Deouell LY, Parnes A, Pickard N, Knight RT (2006) Spatial location is accurately tracked by human auditory sensory memory: evidence from the mismatch negativity. Eur J Neurosci 24(5):1488–1494
Deouell LY, Heller AS, Malach R, D’Esposito M, Knight RT (2007) Cerebral responses to change in spatial location of unattended sounds. Neuron 55(6):985–996
Divenyi PL, Stark PB, Haupt KM (2005) Decline of speech understanding and auditory thresholds in the elderly a). J Acoust Soc Am 118(2):1089–1100
Dobreva MS, O’Neill WE, Paige GD (2011) Influence of aging on human sound localization. J Neurophysiol 105(5):2471–2486
Fieger A, Röder B, Teder-Sälejärvi W, Hillyard SA, Neville HJ (2006) Auditory spatial tuning in late-onset blindness in humans. J Cogn Neurosci 18(2):49–157
Fitzgibbons PJ, Gordon-Salant S (1996) Auditory temporal processing in elderly listeners. J Am Acad Audiol 7:183–189
Fitzgibbons PJ, Gordon-Salant S (2010) Behavioral studies with aging humans: Hearing sensitivity and psychoacoustics. In: Gordon-Salant S, Frisina RD, Fay RR, Popper A (eds) The aging auditory system. Springer, New York, pp 111–134
Freigang C, Schmidt L, Wagner J, Eckardt R, Steinhagen-Thiessen E, Ernst A, Rübsamen R (2011) Evaluation of central auditory discrimination abilities in older adults. Front Aging Neurosci 3:6
Freigang C, Schmiedchen K, Nitsche I, Rübsamen R (2014a) Free-field study on auditory localization and discrimination performance in older adults. Exp Brain Res 232(4):1157–1172
Freigang C, Rübsamen R, Richter N (2014b) Pre-attentive cortical processing of behaviorally perceptible spatial changes in older adults—a mismatch negativity study. Front Neurosci 8:146
Gallun FJ, McMillan GP, Molis MR, Kampel SD, Dann SM, Konrad-Martin DL (2014) Relating age and hearing loss to monaural, bilateral, and binaural temporal sensitivity. Front Neurosci 8:172
Gates GA, Mills JH (2005) Presbycusis. Lancet 366(9491):1111–1120
Gordon-Salant S, Fitzgibbons PJ (1993) Temporal factors and speech recognition performance in young and elderly listeners. J Speech Lang Hear Res 36(6):1276–1285
Gori M, Del Viva M, Sandini G, Burr DC (2008) Young children do not integrate visual and haptic form information. Curr Biol 18(9):694–698
Gori M, Sandini G, Burr D (2012) Development of visuo-auditory integration in space and time. Front Integr Neurosci 6:77
Grieco-Calub TM, Litovsky RY (2010) Sound localization skills in children who use bilateral cochlear implants and in children with normal acoustic hearing. Ear Hear 31(5):645–656
Grose JH, Mamo SK (2010) Processing of temporal fine structure as a function of age. Ear Hear 31(6):755
Gunter TC, Jackson JL, Mulder G (1996) Focussing on aging: an electrophysiological exploration of spatial and attentional processing during reading. Biol Psychol 43(2):103–145
Hartley DE, Wright BA, Hogan SC, Moore DR (2000) Age-related improvements in auditory backward and simultaneous masking in 6-to 10-year-old children. J Speech Lang Hear Res 43(6):1402–1415
Hartmann WM (1983) Localization of sound in rooms. J Acoustic Soc Am 74(5):1380–1391
Hartmann WM, Rakerd B (1989) On the minimum audible angle—A decision theory approach. J Acoustic Soc Am 85(5):2031–2041
Häusler R, Colburn S, Marr E (1983) Sound localization in subjects with impaired hearing: spatial-discrimination and interaural-discrimination tests. Acta Otolaryngol 96(S400):1–62
He NJ, Dubno JR, Mills JH (1998) Frequency and intensity discrimination measured in a maximum-likelihood procedure from young and aged normal-hearing subjects. J Acoustic Soc Am 103(1):553–565
Herman GE, Warren LR, Wagener JW (1977) Auditory lateralization: age differences in sensitivity to dichotic time and amplitude cues. J Gerontol 32(2):187–191
Humes LE (1996) Speech understanding in the elderly. J Am Acad Audiol 7:161–167
Humes LE, Christopherson L (1991) Speech identification difficulties of hearing-impaired elderly persons: the contributions of auditory processing deficits. J Speech Lang Hear Res 34(3):686–693
Jerger J (1992) Can age-related decline in speech understanding be explained by peripheral hearing loss. J Am Acad Audiol 3(1):33–38
Kaiser J, Lutzenberger W (2001) Location changes enhance hemispheric asymmetry of magnetic fields evoked by lateralized sounds in humans. Neurosci Lett 314(1):17–20
Kaiser J, Lutzenberger W, Preissl H, Ackermann H, Birbaumer N (2000) Right-hemisphere dominance for the processing of sound-source lateralization. J Neurosci 20(17):6631–6639
Kerber S, Seeber BU (2012) Sound localization in noise by normal-hearing listeners and cochlear implant users. Ear Hear 33(4):445–457
Kirikae I (1969) Auditory function in advanced age with reference to histological changes in the central auditory system. Int J Audiol 8(2–3):221–230
Kühnle S, Ludwig AA, Meuret S, Küttner C, Witte C, Scholbach J, Fuchs M, Rübsamen R (2012) Development of auditory localization accuracy and auditory spatial discrimination in children and adolescents. Audiol Neurotol 18(1):48–62
Lee CC, Middlebrooks JC (2011) Auditory cortex spatial sensitivity sharpens during task performance. Nat Neurosci 14(1):108–114
Lessard N, Lepore F, Poirier P, Villemagne J, Lassonde M (2000) Sound localization in hemispherectomized subjects: the contribution of crossed and uncrossed cortical afferents. Exp Brain Res 134(3):344–352
Lewald J, Dörrscheidt GJ, Ehrenstein WH (2000) Sound localization with eccentric head position. Behav Brain Res 108(2):105–125
Litovsky RY (1997) Developmental changes in the precedence effect: estimates of minimum audible angle. J Acoustic Soc Am 102(3):1739–1745
Litovsky RY (2011) Review of recent work on spatial hearing skills in children with bilateral cochlear implants. Cochlear Implants Int 12(s1):S30–S34
Litovsky RY, Macmillan NA (1994) Sound localization precision under conditions of the precedence effect: effects of azimuth and standard stimuli. J Acoustic Soc Am 96(2):752–758
Litovsky RY, Colburn HS, Yost WA, Guzman SJ (1999) The precedence effect. J Acoustic Soc Am 106(4):1633–1654
Lovett RES, Kitterick PT, Huang S, Summerfield AQ (2012) The developmental trajectory of spatial listening skills in normal-hearing children. J Speech Lang Hear Res 55(3):865–878
Ludwig AA, Rübsamen R, Dörrscheidt GJ, Kotz SA (2012) Age-related dissociation of sensory and decision-based auditory motion processing. Front Hum Neurosci 6:64
Ludwig AA, Fuchs M, Kruse E, Uhlig B, Kotz SA, Rübsamen R (2014) Auditory processing disorders with and without central auditory discrimination deficits. J Assoc Res Otolaryngol 15(3):441–446
Magezi DA, Krumbholz K (2010) Evidence for opponent-channel coding of interaural time differences in human auditory cortex. J Neurophysiol 104(4):1997–2007
Makous JC, Middlebrooks JC (1990) Two‐dimensional sound localization by human listeners. J Acoustic Soc Am 87(5):2188–2200
Mazelová J, Popelar J, Syka J (2003) Auditory function in presbycusis: peripheral vs. central changes. Exp Gerontol 38(1):87–94
McAlpine D, Grothe B (2003) Sound localization and delay lines–do mammals fit the model? Trends Neurosci 26(7):347–350
McFadden D, Pasanen EG (1976) Lateralization at high frequencies based on interaural time differences. J Acoustic Soc Am 59(3):634–639
Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42(1):135–159
Mills AW (1958) On the minimum audible angle. J Acoustic Soc Am 30(4):237–246
Moore JK, Linthicum FH Jr (2007) The human auditory system: a timeline of development. Int J Audiol 46(9):460–478
Moore DR, Ferguson MA, Halliday LF, Riley A (2008) Frequency discrimination in children: Perception, learning and attention. Hear Res 238(1):147–154
Morrongiello BA (1988) Infants’ localization of sounds along the horizontal axis: Estimates of minimum audible angle. Dev Psychol 24(1):8–13
Morrongiello BA, Rocca PT (1987) Infants’ localization of sounds in the horizontal plane: Effects of auditory and visual cues. Child Dev 58(4):918–927
Morrongiello BA, Fenwick KD, Chance G (1990) Sound localization acuity in very young infants: An observer-based testing procedure. Dev Psychol 26(1):75–84
Muir D, Clifton RK (1985) Infants’ orientation to the location of sound sources. In: Gottlieb G, Krasnegor NA (eds) Measurement of audition and vision in the first year of postnatal life: A methodological overview. Ablex, Westport, pp 171–194
Muir D, Field J (1979) Newborn infants orient to sounds. Child Dev 50(2):431–436
Muir D, Hains S (2004) The U-shaped developmental function for auditory localization. J Cogn Dev 5(1):123–130
Muir D, Abraham W, Forbes B, Harris L (1979) The ontogenesis of an auditory localization response from birth to four months of age. Can J Psychol 33(4):320–333
Muir DW, Clifton RK, Clarkson MG (1989) The development of a human auditory localization response: a U-shaped function. Can J Psychol 43(2):199–216
Näätänen R, Paavilainen P, Rinne T, Alho K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118(12):2544–2590
Neher T, Laugesen S, Jensen NS, Kragelund L (2011) Can basic auditory and cognitive measures predict hearing-impaired listeners’ localization and spatial speech recognition abilities? J Acoustic Soc Am 130(3):1542–1558
Noble W, Byrne D, Lepage B (1994) Effects on sound localization of configuration and type of hearing impairment. J Acoustic Soc Am 95(2):992–1005
Otte RJ, Agterberg MJ, Van Wanrooij MM, Snik AF, Van Opstal AJ (2013) Age-related hearing loss and ear morphology affect vertical but not horizontal sound-localization performance. J Assoc Res Otolaryngol 14(2):261–273
Paavilainen P, Karlsson ML, Reinikainen K, Näätänen R (1989) Mismatch negativity to change in spatial location of an auditory stimulus. Electroencephalogr Clin Neurophysiol 73(2):129–141
Pekkonen E (2000) Mismatch negativity in aging and in Alzheimer’s and Parkinson’s disease. Audiol Neurotol 5(3–4):216–224
Perrott DR, Saberi K (1990) Minimum audible angle thresholds for sources varying in both elevation and azimuth. J Acoustic Soc Am 87(4):1728–1731
Phillips DP (2008) A perceptual architecture for sound lateralization in man. Hear Res 238(1):124–132
Phillips DP, Irvine DRF (1981) Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural intensity differences. Hear Res 4:299–307
Pichora-Fuller MK, Schneider BA (1991) Masking-level differences in the elderly: a comparison of antiphasic and time-delay dichotic conditions. J Speech Hear Res 34(6):1410–1422
Pichora-Fuller MK, Schneider BA (1992) The effect of interaural delay of the masker on masking-level differences in young and old adults. J Acoust Soc Am 91(4 Pt 1):2129–2135
Pichora-Fuller MK, Schneider BA (1998) Masking-level differences in older adults: The effect of the level of the masking noise. Percept Psychophys 60(7):1197–1205
Pichora-Fuller MK, Souza PE (2003) Effects of aging on auditory processing of speech. Int J Audiol 42(S2):11–16
Poirier P, Lassonde M, Villemure JG, Geoffroy G, Lepore F (1994) Sound localization in hemispherectomized patients. Neuropsychologia 32(5):541–553
Pulvermüller F, Shtyrov Y, Ilmoniemi RJ, Marslen-Wilson WD (2006) Tracking speech comprehension in space and time. Neuroimage 31(3):1297–1305
Richter N, Schröger E, Rübsamen R (2009) Hemispheric specialization during discrimination of sound sources reflected by MMN. Neuropsychologia 47(12):2652–2659
Richter N, Schröger E, Rübsamen R (2013) Differences in evoked potentials during the active processing of sound location and motion. Neuropsychologia 51(7):1204–1214
Röder B, Rösler F, Hennighausen E, Näcker F (1996) Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. Cogn Brain Res 4(2):77–93
Röder B, Rösler F, Neville HJ (1999) Effects of interstimulus interval on auditory event-related potentials in congenitally blind and normally sighted humans. Neurosci Lett 264(1):53–56
Röder B, Rösler F, Neville HJ (2001) Auditory memory in congenitally blind adults: a behavioral-electrophysiological investigation. Cogn Brain Res 11(2):289–303
Ross B, Fujioka T, Tremblay KL, Picton TW (2007) Aging in binaural hearing begins in mid-life: evidence from cortical auditory-evoked responses to changes in interaural phase. J Neurosci 27(42):11172–11178
Röttger S, Schröger E, Grube M, Grimm S, Rübsamen R (2007) Mismatch negativity on the cone of confusion. Neurosci Lett 414(2):178–182
Ruggles D, Bharadwaj H, Shinn-Cunningham BG (2012) Why Middle-Aged Listeners Have Trouble Hearing in Everyday Settings. Curr Biol 22(19):1858–1858
Salminen NH, May PJ, Alku P, Tiitinen H (2009) A population rate code of auditory space in the human cortex. PLoS ONE 4(10), e7600
Salminen NH, Tiitinen H, Yrttiaho S, May PJ (2010) The neural code for interaural time difference in human auditory cortex. J Acoustic Soc Am 127(2):EL60–EL65
Salminen NH, Tiitinen H, May PJ (2012) Auditory spatial processing in the human cortex. Neuroscientist 18(6):602–612
Salthouse TA (2000) Aging and measures of processing speed. Biol Psychol 54(1):35–54
Savel S (2009) Individual differences and left/right asymmetries in auditory space perception. I. Localization of low-frequency sounds in free field. Hear Res 255(1):142–154
Schmiedchen K, Freigang C, Nitsche I, Rübsamen R (2012) Crossmodal interactions and multisensory integration in the perception of audio-visual motion—A free-field study. Brain Res 1466:99–111
Schmiedchen K, Freigang C, Rübsamen R, Richter N (2013) A comparison of visual and auditory representational momentum in spatial tasks. Atten Percept Psychophys 75(7):1507–1519
Schmiedt RA (2010) The physiology of cochlear presbycusis. In: Gordon-Salant S, Frisina RD, Popper AN (eds) The aging auditory system. Springer, New York, pp 9–38
Schroeder MM, Lipton RB, Ritter W, Giesser BS, Vaughan HG (1995) Event-related potential correlates of early processing in normal aging. Int J Neurosci 80(1–4):371–382
Schröger E (1997) On the detection of auditory deviations: a pre-attentive activation model. Psychophysiology 34:245–257
Schuknecht HF (1955) Presbycusis. Laryngoscope 65:402–419
Seeber BU, Kerber S, Hafter ER (2010) A system to simulate and reproduce audio–visual environments for spatial hearing research. Hear Res 260(1):1–10
Shankweiler DP (1961) Performance of brain-damaged patients on two tests of sound localization. J Comp Physiol Psychol 54(4):375–381
Shtyrov Y, Kujala T, Palva S, Ilmoniemi RJ, Näätänen R (2000) Discrimination of speech and of complex nonspeech sounds of different temporal structure in the left and right cerebral hemispheres. Neuroimage 12(6):657–663
Slugocki C, Trainor LJ (2014) Cortical indices of sound localization mature monotonically in early infancy. Eur J Neurosci 40(11):3608–3619
Sonnadara RR, Alain C, Trainor LJ (2006) Effects of spatial separation and stimulus probability on the event-related potentials elicited by occasional changes in sound location. Brain Res 1071(1):175–185
Stecker GC, Middlebrooks JC (2003) Distributed coding of sound locations in the auditory cortex. Biol Cybern 89(5):341–349
Stecker GC, Harrington IA, Middlebrooks JC (2005) Location coding by opponent neural populations in the auditory cortex. PLoS Biol 3(3), e78
Stevens SS, Newman EB (1936) The localization of actual sources of sound. Am J Psychol :297–306
Strouse A, Ashmead DH, Ohde RN, Grantham DW (1998) Temporal processing in the aging auditory system. J Acoustic Soc Am 104(4):2385–2399
Teder-Sälejärvi WA, Hillyard SA (1998) The gradient of spatial auditory attention in free field: an event-related potential study. Percept Psychophys 60(7):1228–1242
Trainor L, McFadden M, Hodgson L, Darragh L, Barlow J, Matsos L, Sonnadara R (2003) Changes in auditory cortex and the development of mismatch negativity between 2 and 6 months of age. Int J Psychophysiol 51(1):5–15
Tremblay K, Ross B (2007) Effects of age and age-related hearing loss on the brain. J Commun Disord 40(4):305–312
Tremblay KL, Piskosz M, Souza P (2003) Effects of age and age-related hearing loss on the neural representation of speech cues. Clin Neurophysiol 114(7):1332–1343
Van Deun L, Van Wieringen A, Van den Bogaert T, Scherf F, Offeciers FE, Van de Heyning PH, Desloovere C, Dhooge IJ, Deggouj N, Raeve LD, Wouters J (2009) Sound localization, sound lateralization, and binaural masking level differences in young children with normal hearing. Ear Hear 30(2):178–190
Wang M, Wu X, Li L, Schneider BA (2011) The effects of age and interaural delay on detecting a change in interaural correlation: The role of temporal jitter. Hear Res 275(1–2):139–149
Werner-Reiss U, Groh JM (2008) A rate code for sound azimuth in monkey auditory cortex: implications for human neuroimaging studies. J Neurosci 28(14):3747–3758
Wightman FL, Kistler DJ (1992) The dominant role of low‐frequency interaural time differences in sound localization. J Acoustic Soc Am 91(3):1648–1661
Woldorff MG, Tempelmann C, Fell J, Tegeler C, Gaschler-Markefski B, Hinrichs H, Heinze H-J, Scheich H (1999) Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography. Hum Brain Mapp 7(1):49–66
Zatorre RJ, Penhune VB (2001) Spatial localization after excision of human auditory cortex. J Neurosci 21(16):6321–6328
Zatorre RJ, Ptito A, Villemure JG (1995) Preserved auditory spatial localization following cerebral hemispherectomy. Brain 118(4):879–889
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Freigang, C., Richter, N., Rübsamen, R. et al. Age-related changes in sound localisation ability. Cell Tissue Res 361, 371–386 (2015). https://doi.org/10.1007/s00441-015-2230-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-015-2230-8