Cross-frequency coupling in cortico-hippocampal networks supports the maintenance of sequential auditory information in short-term memory.

Arthur Borderie, Anne Caclin, Jean-Philippe Lachaux, Marcela Perrone-Bertollotti, Roxane S Hoyer, Philippe Kahane, Hélène Catenoix, Barbara Tillmann, Philippe Albouy
Author Information
  1. Arthur Borderie: CERVO Brain Research Center, School of Psychology, Laval University, Québec, Canada.
  2. Anne Caclin: Université Claude Bernard Lyon 1, CNRS, INSERM, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Bron, France.
  3. Jean-Philippe Lachaux: Université Claude Bernard Lyon 1, CNRS, INSERM, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Bron, France.
  4. Marcela Perrone-Bertollotti: Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, LPNC, Grenoble, France.
  5. Roxane S Hoyer: CERVO Brain Research Center, School of Psychology, Laval University, Québec, Canada.
  6. Philippe Kahane: Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, France.
  7. Hélène Catenoix: Université Claude Bernard Lyon 1, CNRS, INSERM, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Bron, France.
  8. Barbara Tillmann: Université Claude Bernard Lyon 1, CNRS, INSERM, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Bron, France.
  9. Philippe Albouy: CERVO Brain Research Center, School of Psychology, Laval University, Québec, Canada. ORCID

Abstract

It has been suggested that cross-frequency coupling in cortico-hippocampal networks enables the maintenance of multiple visuo-spatial items in working memory. However, whether this mechanism acts as a global neural code for memory retention across sensory modalities remains to be demonstrated. Intracranial EEG data were recorded while drug-resistant patients with epilepsy performed a delayed matched-to-sample task with tone sequences. We manipulated task difficulty by varying the memory load and the duration of the silent retention period between the to-be-compared sequences. We show that the strength of theta-gamma phase amplitude coupling in the superior temporal sulcus, the inferior frontal gyrus, the inferior temporal gyrus, and the hippocampus (i) supports the short-term retention of auditory sequences; (ii) decodes correct and incorrect memory trials as revealed by machine learning analysis; and (iii) is positively correlated with individual short-term memory performance. Specifically, we show that successful task performance is associated with consistent phase coupling in these regions across participants, with gamma bursts restricted to specific theta phase ranges corresponding to higher levels of neural excitability. These findings highlight the role of cortico-hippocampal activity in auditory short-term memory and expand our knowledge about the role of cross-frequency coupling as a global biological mechanism for information processing, integration, and memory in the human brain.

References

  1. Trends Cogn Sci. 1999 Apr;3(4):151-162 [PMID: 10322469]
  2. Ann N Y Acad Sci. 2018 Apr 29;: [PMID: 29707781]
  3. Hippocampus. 2006;16(7):604-16 [PMID: 16770797]
  4. J Cogn Neurosci. 2011 Dec;23(12):3855-61 [PMID: 21671734]
  5. Neuroimage. 2003 Aug;19(4):1417-26 [PMID: 12948699]
  6. Neuron. 2015 Oct 7;88(1):220-35 [PMID: 26447583]
  7. Sci Adv. 2022 Feb 25;8(8):eabj9782 [PMID: 35196074]
  8. Front Neurosci. 2019 Oct 30;13:1165 [PMID: 31736698]
  9. PLoS One. 2010 Apr 22;5(4):e10298 [PMID: 20421978]
  10. J Neurosci. 2022 May 4;42(18):3823-3835 [PMID: 35351829]
  11. Hum Brain Mapp. 2019 Feb 15;40(3):855-867 [PMID: 30381866]
  12. Neurocase. 2001;7(5):357-82 [PMID: 11744778]
  13. Learn Mem. 2011 Dec 16;19(1):15-25 [PMID: 22180053]
  14. Nat Rev Neurosci. 2012 Jan 11;13(2):121-34 [PMID: 22233726]
  15. Neuron. 2013 Mar 20;77(6):1002-16 [PMID: 23522038]
  16. Trends Neurosci. 2019 Jul;42(7):485-499 [PMID: 31178076]
  17. Adv Cogn Psychol. 2010 Apr 26;6:15-22 [PMID: 20689638]
  18. Hippocampus. 1998;8(4):330-9 [PMID: 9744420]
  19. Cell Rep. 2015 Nov 10;13(6):1272-1282 [PMID: 26527004]
  20. Neuron. 2018 Jan 3;97(1):10-13 [PMID: 29301097]
  21. Trends Cogn Sci. 2014 Jan;18(1):16-25 [PMID: 24268290]
  22. J Neurophysiol. 2005 Sep;94(3):1904-11 [PMID: 15901760]
  23. Physiology (Bethesda). 2010 Oct;25(5):319-29 [PMID: 20940437]
  24. J Neurosci. 2016 Apr 20;36(16):4492-505 [PMID: 27098693]
  25. J Cogn Neurosci. 2006 Jul;18(7):1087-97 [PMID: 16839283]
  26. Science. 2004 Jun 25;304(5679):1926-9 [PMID: 15218136]
  27. Neuroimage. 2002 Jan;15(1):273-89 [PMID: 11771995]
  28. Nat Commun. 2014 Sep 02;5:4694 [PMID: 25178489]
  29. Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):3228-33 [PMID: 20133762]
  30. Nat Neurosci. 2017 Jul 26;20(8):1189 [PMID: 28745722]
  31. Curr Biol. 2016 Jun 20;26(12):1513-1521 [PMID: 27238283]
  32. Trends Cogn Sci. 2002 Jan 1;6(1):37-46 [PMID: 11849614]
  33. Neuron. 2018 Jan 3;97(1):221-230.e4 [PMID: 29249289]
  34. J Neurosci. 2007 Jul 18;27(29):7807-16 [PMID: 17634374]
  35. Sci Rep. 2016 Jan 06;6:18861 [PMID: 26732511]
  36. J Neurosci Methods. 2011 Oct 15;201(2):438-43 [PMID: 21871489]
  37. J Neurosci. 2011 Apr 6;31(14):5392-7 [PMID: 21471374]
  38. Science. 1995 Mar 10;267(5203):1512-5 [PMID: 7878473]
  39. Nat Neurosci. 2001 Dec;4(12):1259-64 [PMID: 11694886]
  40. Cogn Neurosci. 2015;6(4):149-57 [PMID: 26101947]
  41. PLoS Biol. 2018 Aug 15;16(8):e2003805 [PMID: 30110320]
  42. BMC Neurosci. 2009 Aug 27;10:106 [PMID: 19712445]
  43. Hippocampus. 2005;15(2):203-15 [PMID: 15390152]
  44. Proc Natl Acad Sci U S A. 2021 Dec 14;118(50): [PMID: 34880133]
  45. J Neurosci. 2010 Feb 17;30(7):2694-9 [PMID: 20164353]
  46. Curr Biol. 2016 Feb 22;26(4):450-7 [PMID: 26832442]
  47. Hippocampus. 1992 Apr;2(2):151-63 [PMID: 1308180]
  48. Trends Cogn Sci. 2013 May;17(5):230-40 [PMID: 23597720]
  49. J Neurol Neurosurg Psychiatry. 1957 Feb;20(1):11-21 [PMID: 13406589]
  50. Curr Biol. 2010 Apr 13;20(7):606-12 [PMID: 20303266]
  51. Brain. 2013 May;136(Pt 5):1639-61 [PMID: 23616587]
  52. Nat Neurosci. 2017 Oct 26;20(11):1434-1447 [PMID: 29073641]
  53. J Neurosci. 2012 Jan 4;32(1):111-23 [PMID: 22219274]
  54. Elife. 2017 Mar 14;6: [PMID: 28288700]
  55. Front Hum Neurosci. 2015 Feb 04;9:20 [PMID: 25698955]
  56. Cereb Cortex. 2005 Mar;15(3):303-16 [PMID: 15342440]
  57. J Neurosci. 1994 Apr;14(4):1908-19 [PMID: 8158246]
  58. Elife. 2015 May 29;4:e06213 [PMID: 26023831]
  59. Prog Neurobiol. 2022 Nov;218:102326 [PMID: 35870677]
  60. Science. 2006 Sep 15;313(5793):1626-8 [PMID: 16973878]
  61. Trends Cogn Sci. 2010 Nov;14(11):506-15 [PMID: 20932795]
  62. Neuron. 2017 Apr 5;94(1):193-206.e5 [PMID: 28343866]
  63. Neuron. 2001 Sep 13;31(5):865-73 [PMID: 11567623]
  64. Nat Rev Neurosci. 2014 Oct;15(10):655-69 [PMID: 25234264]
  65. Sci Adv. 2019 Mar 27;5(3):eaav3687 [PMID: 30944858]
  66. Hippocampus. 2005;15(7):890-900 [PMID: 16114010]
  67. Neuropsychologia. 2017 May;99:48-63 [PMID: 28259771]
  68. Hum Brain Mapp. 2009 Jun;30(6):1758-71 [PMID: 19343801]
  69. Curr Biol. 2017 Apr 3;27(7):1026-1032 [PMID: 28318972]
  70. Cereb Cortex. 2023 Feb 20;33(5):1826-1842 [PMID: 35511687]
  71. Elife. 2022 Aug 12;11: [PMID: 35960169]

MeSH Term

Humans
Memory, Short-Term
Hippocampus
Temporal Lobe
Brain
Caffeine

Chemicals

Caffeine

Word Cloud

Created with Highcharts 10.0.0memorycouplingshort-termcortico-hippocampalretentiontasksequencesphaseauditorycross-frequencynetworksmaintenancemechanismglobalneuralacrossshowtemporalinferiorgyrussupportsperformanceroleinformationsuggestedenablesmultiplevisuo-spatialitemsworkingHoweverwhetheractscodesensorymodalitiesremainsdemonstratedIntracranialEEGdatarecordeddrug-resistantpatientsepilepsyperformeddelayedmatched-to-sampletonemanipulateddifficultyvaryingloaddurationsilentperiodto-be-comparedstrengththeta-gammaamplitudesuperiorsulcusfrontalhippocampusiidecodescorrectincorrecttrialsrevealedmachinelearninganalysisiiipositivelycorrelatedindividualSpecificallysuccessfulassociatedconsistentregionsparticipantsgammaburstsrestrictedspecificthetarangescorrespondinghigherlevelsexcitabilityfindingshighlightactivityexpandknowledgebiologicalprocessingintegrationhumanbrainCross-frequencysequential

Similar Articles

Cited By