Skip to main content
NCBI home page
Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2001 Jan;70(1):88–94. doi: 10.1136/jnnp.70.1.88

Abnormal peripheral auditory asymmetry in schizophrenia

E Veuillet 1, N Georgieff 1, B Philibert 1, J Dalery 1, M Marie-Cardine 1, L Collet 1
PMCID: PMC1763487  PMID: 11118254

Abstract

OBJECTIVE—Auditory processing difficulties have been reported in schizophrenia. This study explores peripheral auditory function in patients with schizophrenia in whom certain early disturbances of auditory message filtering have been found and may be associated with certain abnormalities which are particularly localised in the left temporal lobe.
METHODS—Otoacoustic emissions, including click evoked and spontaneous emissions and measurements of functioning of the medial olivocochlear efferent system were obtained from 12 chronic schizophrenic patients and compared with normative data recorded from 12 normal controls.
RESULTS—Otoacoustic emission amplitudes and medial olivocochlear functioning were similar between the normal controls and schizophrenic patients; the schizophrenic patients did, however, differ from the normal controls in otoacoustic emission intensity and in medial olivocochlear asymmetry. A tendency to a higher number of spontaneous peaks, and a significantly higher click evoked otoacoustic emission response amplitude were found in the right ear compared with the left ear of schizophrenic patients. For the medial olivocochlear system, whereas normal controls showed greater attenuation in the right than in the left ear, schizophrenic patients lacked such an asymmetry.
CONCLUSION—In the absence of any attention task, the findings show disturbed peripheral lateralisation in schizophrenia of mechanisms involved in auditory information filtering. Such a lack of right ear advantage in medial olivocochlear functioning may thus be a peripheral reflection of central lateralisation anomalies.



Full Text

The Full Text of this article is available as a PDF (135.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adler L. E., Pachtman E., Franks R. D., Pecevich M., Waldo M. C., Freedman R. Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biol Psychiatry. 1982 Jun;17(6):639–654. [PubMed] [Google Scholar]
  2. Alain C., Hargrave R., Woods D. L. Processing of auditory stimuli during visual attention in patients with schizophrenia. Biol Psychiatry. 1998 Dec 1;44(11):1151–1159. doi: 10.1016/s0006-3223(97)00478-2. [DOI] [PubMed] [Google Scholar]
  3. Binder J. R., Frost J. A., Hammeke T. A., Rao S. M., Cox R. W. Function of the left planum temporale in auditory and linguistic processing. Brain. 1996 Aug;119(Pt 4):1239–1247. doi: 10.1093/brain/119.4.1239. [DOI] [PubMed] [Google Scholar]
  4. Boutros N. N., Zouridakis G., Overall J. Replication and extension of P50 findings in schizophrenia. Clin Electroencephalogr. 1991 Jan;22(1):40–45. doi: 10.1177/155005949102200109. [DOI] [PubMed] [Google Scholar]
  5. Brownell W. E., Bader C. R., Bertrand D., de Ribaupierre Y. Evoked mechanical responses of isolated cochlear outer hair cells. Science. 1985 Jan 11;227(4683):194–196. doi: 10.1126/science.3966153. [DOI] [PubMed] [Google Scholar]
  6. Bruder G., Rabinowicz E., Towey J., Brown A., Kaufmann C. A., Amador X., Malaspina D., Gorman J. M. Smaller right ear (left hemisphere) advantage for dichotic fused words in patients with schizophrenia. Am J Psychiatry. 1995 Jun;152(6):932–935. doi: 10.1176/ajp.152.6.932. [DOI] [PubMed] [Google Scholar]
  7. Collet L., Kemp D. T., Veuillet E., Duclaux R., Moulin A., Morgon A. Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects. Hear Res. 1990 Jan;43(2-3):251–261. doi: 10.1016/0378-5955(90)90232-e. [DOI] [PubMed] [Google Scholar]
  8. Collet L., Roge B., Descouens D., Moron P., Duverdy F., Urgell H. Objective auditory dysfunction in infantile autism. Lancet. 1993 Oct 9;342(8876):923–924. doi: 10.1016/0140-6736(93)91969-s. [DOI] [PubMed] [Google Scholar]
  9. Collet L., Veuillet E., Bene J., Morgon A. Effects of contralateral white noise on click-evoked emissions in normal and sensorineural ears: towards an exploration of the medial olivocochlear system. Audiology. 1992;31(1):1–7. doi: 10.3109/00206099209072897. [DOI] [PubMed] [Google Scholar]
  10. Crow T. J., Ball J., Bloom S. R., Brown R., Bruton C. J., Colter N., Frith C. D., Johnstone E. C., Owens D. G., Roberts G. W. Schizophrenia as an anomaly of development of cerebral asymmetry. A postmortem study and a proposal concerning the genetic basis of the disease. Arch Gen Psychiatry. 1989 Dec;46(12):1145–1150. doi: 10.1001/archpsyc.1989.01810120087013. [DOI] [PubMed] [Google Scholar]
  11. Crow T. J. Schizophrenia as failure of hemispheric dominance for language. Trends Neurosci. 1997 Aug;20(8):339–343. doi: 10.1016/s0166-2236(97)01071-0. [DOI] [PubMed] [Google Scholar]
  12. Crow T. J. Temporal lobe asymmetries as the key to the etiology of schizophrenia. Schizophr Bull. 1990;16(3):433–443. doi: 10.1093/schbul/16.3.433. [DOI] [PubMed] [Google Scholar]
  13. Dallos P. The active cochlea. J Neurosci. 1992 Dec;12(12):4575–4585. doi: 10.1523/JNEUROSCI.12-12-04575.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Faux S. F., Torello M. W., McCarley R. W., Shenton M. E., Duffy F. H. P300 in schizophrenia: confirmation and statistical validation of temporal region deficit in P300 topography. Biol Psychiatry. 1988 Apr 15;23(8):776–790. doi: 10.1016/0006-3223(88)90066-2. [DOI] [PubMed] [Google Scholar]
  15. Flor-Henry P. Psychosis and temporal lobe epilepsy. A controlled investigation. Epilepsia. 1969 Sep;10(3):363–395. doi: 10.1111/j.1528-1157.1969.tb03853.x. [DOI] [PubMed] [Google Scholar]
  16. Geschwind N., Levitsky W. Human brain: left-right asymmetries in temporal speech region. Science. 1968 Jul 12;161(3837):186–187. doi: 10.1126/science.161.3837.186. [DOI] [PubMed] [Google Scholar]
  17. Giraud A. L., Collet L., Chéry-Croze S., Magnan J., Chays A. Evidence of a medial olivocochlear involvement in contralateral suppression of otoacoustic emissions in humans. Brain Res. 1995 Dec 24;705(1-2):15–23. doi: 10.1016/0006-8993(95)01091-2. [DOI] [PubMed] [Google Scholar]
  18. Gruzelier J. H. Functional neuropsychophysiological asymmetry in schizophrenia: a review and reorientation. Schizophr Bull. 1999;25(1):91–120. doi: 10.1093/oxfordjournals.schbul.a033370. [DOI] [PubMed] [Google Scholar]
  19. Gruzelier J. H., Hammond N. V. Gains, losses and lateral differences in the hearing of schizophrenic patients. Br J Psychol. 1979 May;70(2):319–330. doi: 10.1111/j.2044-8295.1979.tb01689.x. [DOI] [PubMed] [Google Scholar]
  20. Gruzelier J. H. The cardiac responses of schizophrenics to orienting, signal and non-signal tones. Biol Psychol. 1975 Sep;3(2):143–155. doi: 10.1016/0301-0511(75)90016-2. [DOI] [PubMed] [Google Scholar]
  21. Hill H., Weisbrod M. The relation between asymmetry and amplitude of the P300 field in schizophrenia. Clin Neurophysiol. 1999 Sep;110(9):1611–1617. doi: 10.1016/s1388-2457(99)00112-1. [DOI] [PubMed] [Google Scholar]
  22. Hirayasu Y., Potts G. F., O'Donnell B. F., Kwon J. S., Arakaki H., Akdag S. J., Levitt J. J., Shenton M. E., McCarley R. W. Auditory mismatch negativity in schizophrenia: topographic evaluation with a high-density recording montage. Am J Psychiatry. 1998 Sep;155(9):1281–1284. doi: 10.1176/ajp.155.9.1281. [DOI] [PubMed] [Google Scholar]
  23. Huffman R. F., Henson O. W., Jr The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Brain Res Rev. 1990 Sep-Dec;15(3):295–323. doi: 10.1016/0165-0173(90)90005-9. [DOI] [PubMed] [Google Scholar]
  24. Igata M., Ohta M., Hayashida Y., Abe K. Normalization of auditory brainstem responses resulting from improved clinical symptoms in schizophrenia. Schizophr Res. 1995 Jul;16(1):81–82. doi: 10.1016/0920-9964(95)00007-9. [DOI] [PubMed] [Google Scholar]
  25. Javitt D. C., Doneshka P., Grochowski S., Ritter W. Impaired mismatch negativity generation reflects widespread dysfunction of working memory in schizophrenia. Arch Gen Psychiatry. 1995 Jul;52(7):550–558. doi: 10.1001/archpsyc.1995.03950190032005. [DOI] [PubMed] [Google Scholar]
  26. Kemp D. T. Evidence of mechanical nonlinearity and frequency selective wave amplification in the cochlea. Arch Otorhinolaryngol. 1979;224(1-2):37–45. doi: 10.1007/BF00455222. [DOI] [PubMed] [Google Scholar]
  27. Kemp D. T. Otoacoustic emissions, travelling waves and cochlear mechanisms. Hear Res. 1986;22:95–104. doi: 10.1016/0378-5955(86)90087-0. [DOI] [PubMed] [Google Scholar]
  28. Kemp D. T., Ryan S., Bray P. A guide to the effective use of otoacoustic emissions. Ear Hear. 1990 Apr;11(2):93–105. doi: 10.1097/00003446-199004000-00004. [DOI] [PubMed] [Google Scholar]
  29. Kemp D. T. Stimulated acoustic emissions from within the human auditory system. J Acoust Soc Am. 1978 Nov;64(5):1386–1391. doi: 10.1121/1.382104. [DOI] [PubMed] [Google Scholar]
  30. Khalfa S., Collet L. Functional asymmetry of medial olivocochlear system in humans. Towards a peripheral auditory lateralization. Neuroreport. 1996 Apr 10;7(5):993–996. doi: 10.1097/00001756-199604100-00008. [DOI] [PubMed] [Google Scholar]
  31. Khalfa S., Micheyl C., Veuillet E., Collet L. Peripheral auditory lateralization assessment using TEOAEs. Hear Res. 1998 Jul;121(1-2):29–34. doi: 10.1016/s0378-5955(98)00062-8. [DOI] [PubMed] [Google Scholar]
  32. Khalfa S., Veuillet E., Collet L. Influence of handedness on peripheral auditory asymmetry. Eur J Neurosci. 1998 Aug;10(8):2731–2737. doi: 10.1046/j.1460-9568.1998.00286.x. [DOI] [PubMed] [Google Scholar]
  33. MCGHIE A., CHAPMAN J. Disorders of attention and perception in early schizophrenia. Br J Med Psychol. 1961;34:103–116. doi: 10.1111/j.2044-8341.1961.tb00936.x. [DOI] [PubMed] [Google Scholar]
  34. Mathew V. M., Gruzelier J. H., Liddle P. F. Lateral asymmetries in auditory acuity distinguish hallucinating from nonhallucinating schizophrenic patients. Psychiatry Res. 1993 Feb;46(2):127–138. doi: 10.1016/0165-1781(93)90015-9. [DOI] [PubMed] [Google Scholar]
  35. McCarley R. W., Faux S. F., Shenton M. E., Nestor P. G., Adams J. Event-related potentials in schizophrenia: their biological and clinical correlates and a new model of schizophrenic pathophysiology. Schizophr Res. 1991 Mar-Apr;4(2):209–231. doi: 10.1016/0920-9964(91)90034-o. [DOI] [PubMed] [Google Scholar]
  36. McCarley R. W., Shenton M. E., O'Donnell B. F., Faux S. F., Kikinis R., Nestor P. G., Jolesz F. A. Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia. Arch Gen Psychiatry. 1993 Mar;50(3):190–197. doi: 10.1001/archpsyc.1993.01820150036003. [DOI] [PubMed] [Google Scholar]
  37. Micheyl C., Collet L. Involvement of the olivocochlear bundle in the detection of tones in noise. J Acoust Soc Am. 1996 Mar;99(3):1604–1610. doi: 10.1121/1.414734. [DOI] [PubMed] [Google Scholar]
  38. Micheyl C., Morlet T., Giraud A. L., Collet L., Morgon A. Contralateral suppression of evoked otoacoustic emissions and detection of a multi-tone complex in noise. Acta Otolaryngol. 1995 Mar;115(2):178–182. doi: 10.3109/00016489509139286. [DOI] [PubMed] [Google Scholar]
  39. Micheyl C., Perrot X., Collet L. Relationship between auditory intensity discrimination in noise and olivocochlear efferent system activity in humans. Behav Neurosci. 1997 Aug;111(4):801–807. doi: 10.1037//0735-7044.111.4.801. [DOI] [PubMed] [Google Scholar]
  40. Mountain D. C. Changes in endolymphatic potential and crossed olivocochlear bundle stimulation alter cochlear mechanics. Science. 1980 Oct 3;210(4465):71–72. doi: 10.1126/science.7414321. [DOI] [PubMed] [Google Scholar]
  41. Oldfield R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971 Mar;9(1):97–113. doi: 10.1016/0028-3932(71)90067-4. [DOI] [PubMed] [Google Scholar]
  42. Powers N. L., Salvi R. J., Wang J., Spongr V., Qiu C. X. Elevation of auditory thresholds by spontaneous cochlear oscillations. Nature. 1995 Jun 15;375(6532):585–587. doi: 10.1038/375585a0. [DOI] [PubMed] [Google Scholar]
  43. Pritchard W. S. Cognitive event-related potential correlates of schizophrenia. Psychol Bull. 1986 Jul;100(1):43–66. [PubMed] [Google Scholar]
  44. Probst R., Lonsbury-Martin B. L., Martin G. K. A review of otoacoustic emissions. J Acoust Soc Am. 1991 May;89(5):2027–2067. doi: 10.1121/1.400897. [DOI] [PubMed] [Google Scholar]
  45. Puel J. L., Rebillard G. Effect of contralateral sound stimulation on the distortion product 2F1-F2: evidence that the medial efferent system is involved. J Acoust Soc Am. 1990 Apr;87(4):1630–1635. doi: 10.1121/1.399410. [DOI] [PubMed] [Google Scholar]
  46. Ross C. A., Pearlson G. D. Schizophrenia, the heteromodal association neocortex and development: potential for a neurogenetic approach. Trends Neurosci. 1996 May;19(5):171–176. doi: 10.1016/s0166-2236(96)10022-9. [DOI] [PubMed] [Google Scholar]
  47. Shelley A. M., Ward P. B., Catts S. V., Michie P. T., Andrews S., McConaghy N. Mismatch negativity: an index of a preattentive processing deficit in schizophrenia. Biol Psychiatry. 1991 Nov 15;30(10):1059–1062. doi: 10.1016/0006-3223(91)90126-7. [DOI] [PubMed] [Google Scholar]
  48. Siegel J. H., Kim D. O. Efferent neural control of cochlear mechanics? Olivocochlear bundle stimulation affects cochlear biomechanical nonlinearity. Hear Res. 1982 Feb;6(2):171–182. doi: 10.1016/0378-5955(82)90052-1. [DOI] [PubMed] [Google Scholar]
  49. Steinmetz H. Structure, functional and cerebral asymmetry: in vivo morphometry of the planum temporale. Neurosci Biobehav Rev. 1996 Winter;20(4):587–591. doi: 10.1016/0149-7634(95)00071-2. [DOI] [PubMed] [Google Scholar]
  50. VENABLES P. H. INPUT DYSFUNCTION IN SCHIZOPHRENIA. Prog Exp Pers Res. 1964;72:1–47. [PubMed] [Google Scholar]
  51. Veuillet E., Duverdy-Bertholon F., Collet L. Effect of contralateral acoustic stimulation on the growth of click-evoked otoacoustic emissions in humans. Hear Res. 1996 Apr;93(1-2):128–135. doi: 10.1016/0378-5955(95)00212-x. [DOI] [PubMed] [Google Scholar]
  52. Ward P. B., Hoffer L. D., Liebert B. J., Catts S. V., O'Donnell M., Adler L. E. Replication of a P50 auditory gating deficit in Australian patients with schizophrenia. Psychiatry Res. 1996 Sep 27;64(2):121–135. doi: 10.1016/0165-1781(96)02876-4. [DOI] [PubMed] [Google Scholar]
  53. Warren E. H., 3rd, Liberman M. C. Effects of contralateral sound on auditory-nerve responses. I. Contributions of cochlear efferents. Hear Res. 1989 Jan;37(2):89–104. doi: 10.1016/0378-5955(89)90032-4. [DOI] [PubMed] [Google Scholar]
  54. Wexler B. E., Giller E. L., Jr, Southwick S. Cerebral laterality, symptoms, and diagnosis in psychotic patients. Biol Psychiatry. 1991 Jan 15;29(2):103–116. doi: 10.1016/0006-3223(91)90039-o. [DOI] [PubMed] [Google Scholar]
  55. Williams E. A., Brookes G. B., Prasher D. K. Effects of contralateral acoustic stimulation on otoacoustic emissions following vestibular neurectomy. Scand Audiol. 1993;22(3):197–203. doi: 10.3109/01050399309047469. [DOI] [PubMed] [Google Scholar]
  56. Williams E. A., Brookes G. B., Prasher D. K. Effects of olivocochlear bundle section on otoacoustic emissions in humans: efferent effects in comparison with control subjects. Acta Otolaryngol. 1994 Mar;114(2):121–129. doi: 10.3109/00016489409126029. [DOI] [PubMed] [Google Scholar]
  57. Zenner H. P. Motile responses in outer hair cells. Hear Res. 1986;22:83–90. doi: 10.1016/0378-5955(86)90082-1. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Neurology, Neurosurgery, and Psychiatry are provided here courtesy of BMJ Publishing Group

RESOURCES