Representations of specific acoustic patterns in the auditory cortex and hippocampus.

Sukhbinder Kumar, Heidi M Bonnici, Sundeep Teki, Trevor R Agus, Daniel Pressnitzer, Eleanor A Maguire, Timothy D Griffiths
Author Information
  1. Sukhbinder Kumar: Institute of Neuroscience, Medical School, Newcastle University, Newcastle upon Tyne NE2 4HH, UK Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK sukhbinder.kumar@ncl.ac.uk.
  2. Heidi M Bonnici: Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK.
  3. Sundeep Teki: Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK.
  4. Trevor R Agus: Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, and Ecole Normale Superieure, Paris, France.
  5. Daniel Pressnitzer: Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, and Ecole Normale Superieure, Paris, France.
  6. Eleanor A Maguire: Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK.
  7. Timothy D Griffiths: Institute of Neuroscience, Medical School, Newcastle University, Newcastle upon Tyne NE2 4HH, UK Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK.

Abstract

Previous behavioural studies have shown that repeated presentation of a randomly chosen acoustic pattern leads to the unsupervised learning of some of its specific acoustic features. The objective of our study was to determine the neural substrate for the representation of freshly learnt acoustic patterns. Subjects first performed a behavioural task that resulted in the incidental learning of three different noise-like acoustic patterns. During subsequent high-resolution functional magnetic resonance imaging scanning, subjects were then exposed again to these three learnt patterns and to others that had not been learned. Multi-voxel pattern analysis was used to test if the learnt acoustic patterns could be 'decoded' from the patterns of activity in the auditory cortex and medial temporal lobe. We found that activity in planum temporale and the hippocampus reliably distinguished between the learnt acoustic patterns. Our results demonstrate that these structures are involved in the neural representation of specific acoustic patterns after they have been learnt.

Keywords

References

  1. J Cogn Neurosci. 2008 Dec;20(12):2125-36 [PMID: 18457502]
  2. Proc Natl Acad Sci U S A. 2011 Jan 18;108(3):1188-93 [PMID: 21199948]
  3. Neuroimage. 2005 Feb 15;24(4):1052-7 [PMID: 15670682]
  4. Cereb Cortex. 2015 Jul;25(7):1947-57 [PMID: 24488957]
  5. Cereb Cortex. 1999 Jun;9(4):392-405 [PMID: 10426418]
  6. J Acoust Soc Am. 2013 Jul;134(1):464-73 [PMID: 23862821]
  7. Cereb Cortex. 1996 Sep-Oct;6(5):661-72 [PMID: 8921202]
  8. Hear Res. 2007 Jul;229(1-2):54-68 [PMID: 17344002]
  9. Eur J Neurosci. 2005 Sep;22(5):1135-40 [PMID: 16176355]
  10. AJNR Am J Neuroradiol. 1998 Apr;19(4):659-71 [PMID: 9576651]
  11. Neuroimage. 2005 Oct 15;28(1):132-9 [PMID: 16027008]
  12. J Comput Assist Tomogr. 1989 Nov-Dec;13(6):996-1005 [PMID: 2584512]
  13. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4034-9 [PMID: 10097158]
  14. J Neurosci. 2005 May 25;25(21):5148-58 [PMID: 15917455]
  15. Curr Biol. 2007 Jul 3;17(13):1123-8 [PMID: 17600716]
  16. J Speech Lang Hear Res. 2014 Jun 1;57(3):1069-77 [PMID: 24167235]
  17. Proc Natl Acad Sci U S A. 2006 Mar 7;103(10):3863-8 [PMID: 16537458]
  18. Front Syst Neurosci. 2013 Apr 30;7:11 [PMID: 23641203]
  19. Cereb Cortex. 2004 Sep;14(9):1008-21 [PMID: 15166097]
  20. J Neurosci. 2012 Aug 29;32(35):12251-7 [PMID: 22933806]
  21. Cereb Cortex. 2005 Oct;15(10):1621-31 [PMID: 15703256]
  22. Curr Biol. 2010 Mar 23;20(6):544-7 [PMID: 20226665]
  23. J Neurosci. 2010 Feb 10;30(6):2070-6 [PMID: 20147535]
  24. Trends Neurosci. 2002 Jul;25(7):348-53 [PMID: 12079762]
  25. J Neurosci. 2012 Nov 21;32(47):16982-91 [PMID: 23175849]
  26. Dev Cogn Neurosci. 2012 Oct;2(4):428-36 [PMID: 22652538]
  27. J Neurosci. 2008 Dec 3;28(49):13268-73 [PMID: 19052218]
  28. PLoS Comput Biol. 2007 Jun;3(6):e100 [PMID: 17542641]
  29. Hippocampus. 2008;18(9):909-18 [PMID: 18528855]
  30. Brain Res. 1983 Sep 26;275(2):263-77 [PMID: 6194854]
  31. Neuroscience. 2012 Jul 12;214:49-58 [PMID: 22522473]
  32. Nat Rev Neurosci. 2004 Apr;5(4):279-90 [PMID: 15034553]
  33. Neuroimage. 2004 Jun;22(2):706-19 [PMID: 15193599]
  34. Curr Biol. 2013 Jun 3;23(11):968-74 [PMID: 23664974]
  35. Neuroimage. 2006 Jul 1;31(3):1116-28 [PMID: 16545965]
  36. Neuron. 2010 May 27;66(4):610-8 [PMID: 20510864]
  37. Neuropsychologia. 2012 Nov;50(13):3107-21 [PMID: 22820344]
  38. Neuropsychologia. 2011 Apr;49(5):878-887 [PMID: 21236276]
  39. Curr Biol. 2009 Apr 14;19(7):546-54 [PMID: 19285400]
  40. Neurosci Biobehav Rev. 1996 Winter;20(4):587-91 [PMID: 8994197]
  41. Front Neuroanat. 2010 Oct 08;4:129 [PMID: 20976037]

Grants

  1. 101759/Wellcome Trust
  2. WT091681MA/Wellcome Trust
  3. WT084218/Wellcome Trust
  4. G1002276/Medical Research Council
  5. 091681/Wellcome Trust
  6. 091593/Wellcome Trust

MeSH Term

Acoustic Stimulation
Adult
Auditory Cortex
Auditory Perception
Female
Hippocampus
Humans
Learning
Magnetic Resonance Imaging
Male
Young Adult

Word Cloud

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