Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation.
| Title: | Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation. |
|---|---|
| Authors: | Miller J; Department of Biomedical Engineering, Columbia University, 351 Engineering Terrace, Mail Code 8904, 1210 Amsterdam Avenue, New York, NY, 10027, USA.; Watrous AJ; Department of Biomedical Engineering, Columbia University, 351 Engineering Terrace, Mail Code 8904, 1210 Amsterdam Avenue, New York, NY, 10027, USA.; Tsitsiklis M; Doctoral Program in Neurobiology and Behavior, Columbia University, New York, 10027, NY, USA.; Lee SA; Department of Bio and Brain Engineering, Korea Advanced Institute of Science and Technology, Daejeon, 34141, Korea.; Sheth SA; Department of Neurosurgery, Baylor College of Medicine, Houston, 77030, TX, USA.; Schevon CA; Department of Neurology, Columbia University Medical Center, New York, 10032, NY, USA.; Smith EH; Department of Neurological Surgery, Columbia University Medical Center, New York, 10032, NY, USA.; Sperling MR; Department of Neurology, Thomas Jefferson University, Philadelphia, 19107, PA, USA.; Sharan A; Department of Neurosurgery, Thomas Jefferson University, Philadelphia, 19107, PA, USA.; Asadi-Pooya AA; Department of Neurology, Thomas Jefferson University, Philadelphia, 19107, PA, USA.; Shiraz Neurosciences Research Center, Shiraz University of Medical Sciences, Shiraz, 71348, Iran.; Worrell GA; Department of Neurology, Mayo Clinic, Rochester, 55905, MN, USA.; Meisenhelter S; Department of Neurology, Geisel School of Medicine at Dartmouth, Lebanon, 03756, NH, USA.; Inman CS; Emory University School of Medicine, Atlanta, 30322, GA, USA.; Davis KA; Department of Neurology, Hospital of the University of Pennsylvania, Philadelphia, 19104, PA, USA.; Lega B; University of Texas-Southwestern, Dallas, 75390, TX, USA.; Wanda PA; Department of Psychology, University of Pennsylvania, Philadelphia, 19104, PA, USA.; Das SR; Department of Neurology, Hospital of the University of Pennsylvania, Philadelphia, 19104, PA, USA.; Stein JM; Department of Radiology, Hospital of the University of Pennsylvania, Philadelphia, 19104, PA, USA.; Gorniak R; Department of Radiology, Thomas Jefferson University, Philadelphia, 19107, PA, USA.; Jacobs J; Department of Biomedical Engineering, Columbia University, 351 Engineering Terrace, Mail Code 8904, 1210 Amsterdam Avenue, New York, NY, 10027, USA. joshua.jacobs@columbia.edu. |
| Source: | Nature communications [Nat Commun] 2018 Jun 21; Vol. 9 (1), pp. 2423. Date of Electronic Publication: 2018 Jun 21. |
| Publication Type: | Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: [London] : Nature Pub. Group |
| MeSH Terms: | Hippocampus/*physiology ; Spatial Memory/*physiology ; Spatial Navigation/*physiology; Adult ; Brain Mapping ; Electroencephalography ; Female ; Humans ; Logistic Models ; Male ; Multivariate Analysis |
| Abstract: | The hippocampus plays a vital role in various aspects of cognition including both memory and spatial navigation. To understand electrophysiologically how the hippocampus supports these processes, we recorded intracranial electroencephalographic activity from 46 neurosurgical patients as they performed a spatial memory task. We measure signals from multiple brain regions, including both left and right hippocampi, and we use spectral analysis to identify oscillatory patterns related to memory encoding and navigation. We show that in the left but not right hippocampus, the amplitude of oscillations in the 1-3-Hz "low theta" band increases when viewing subsequently remembered object-location pairs. In contrast, in the right but not left hippocampus, low-theta activity increases during periods of navigation. The frequencies of these hippocampal signals are slower than task-related signals in the neocortex. These results suggest that the human brain includes multiple lateralized oscillatory networks that support different aspects of cognition. |
| Comments: | Comment in: Epilepsy Curr. 2019 Mar-Apr;19(2):126-128. doi: 10.1177/1535759719835662.. (PMID: 30955426) |
| References: | Science. 1978 Jul 14;201(4351):160-3. (PMID: 663646); Front Hum Neurosci. 2008 May 15;2:3. (PMID: 18958204); J Neurosci. 2009 Oct 28;29(43):13613-20. (PMID: 19864573); Front Integr Neurosci. 2010 Mar 10;4:2. (PMID: 20431726); Neuroimage. 2016 May 15;132:534-541. (PMID: 26931816); J Cogn Neurosci. 2013 Jul;25(7):1008-19. (PMID: 23489142); Electroencephalogr Clin Neurophysiol. 1969 Apr;26(4):407-18. (PMID: 4183562); J Neurosci. 2003 Jun 15;23(12):5302-7. (PMID: 12832555); J Cogn Neurosci. 2010 May;22(5):824-36. (PMID: 19400683); Curr Opin Neurobiol. 2006 Dec;16(6):693-700. (PMID: 17097284); J Neurosci. 2003 Jun 1;23(11):4726-36. (PMID: 12805312); J Neurosci. 2011 Apr 6;31(14):5253-61. (PMID: 21471360); J Neurol Neurosurg Psychiatry. 1957 Feb;20(1):11-21. (PMID: 13406589); Neuropsychologia. 1997 Jan;35(1):11-24. (PMID: 8981373); Neuron. 2002 Aug 15;35(4):625-41. (PMID: 12194864); Hippocampus. 2012 Apr;22(4):748-61. (PMID: 21538660); Hippocampus. 2013 Aug;23 (8):656-661. (PMID: 23520039); J Neurosci. 2011 Jan 26;31(4):1238-45. (PMID: 21273408); J Neurophysiol. 2011 Apr;105(4):1747-55. (PMID: 21289136); Neuron. 2008 Nov 26;60(4):683-97. (PMID: 19038224); Nat Neurosci. 2013 Mar;16(3):309-17. (PMID: 23334581); Hippocampus. 1993 Jul;3(3):317-30. (PMID: 8353611); Neuron. 2002 Jan 31;33(3):325-40. (PMID: 11832222); PLoS Biol. 2012;10(2):e1001267. (PMID: 22389627); J Neurosci Methods. 2007 Aug 15;164(1):177-90. (PMID: 17517438); Neuroimage. 2006 Jul 1;31(3):968-80. (PMID: 16530430); Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14466-71. (PMID: 20660746); J Neurosci. 2013 Jan 2;33(1):292-304. (PMID: 23283342); Nature. 2005 Aug 11;436(7052):801-6. (PMID: 15965463); J Neurosci. 1994 Nov;14(11 Pt 2):7040-52. (PMID: 7965097); J Neurophysiol. 2009 Mar;101(3):1192-200. (PMID: 19118111); Med Image Anal. 2008 Feb;12(1):26-41. (PMID: 17659998); J Neurosci. 2008 Jun 4;28(23):5983-90. (PMID: 18524903); Neuroimage. 2014 Jan 1;84:488-94. (PMID: 24012858); Neuron. 2016 Mar 16;89(6):1180-1186. (PMID: 26924436); Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4398-403. (PMID: 10716738); Science. 2013 Nov 29;342(6162):1111-4. (PMID: 24288336); Hippocampus. 2008;18(12):1157-74. (PMID: 19021256); J Neurosci. 2018 Mar 28;38(13):3265-3272. (PMID: 29467145); J Neurosci. 2010 Feb 17;30(7):2694-9. (PMID: 20164353); Hum Brain Mapp. 2015 Jan;36(1):258-87. (PMID: 25181316); Neuroimage. 2016 Nov 15;142:533-543. (PMID: 27521743); Hippocampus. 2008;18(4):340-8. (PMID: 18081172); Curr Biol. 2017 Dec 18;27(24):3743-3751.e3. (PMID: 29199073); Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1616-20. (PMID: 11818559); Philos Trans R Soc Lond B Biol Sci. 2013 Dec 23;369(1635):20130304. (PMID: 24366145); Neuropsychologia. 1998 Nov;36(11):1217-38. (PMID: 9842767); Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5365-70. (PMID: 19289818); J Neurosci. 2003 Nov 26;23(34):10809-14. (PMID: 14645473); Curr Biol. 2017 May 8;27(9):1251-1258. (PMID: 28434860); Neuropsychologia. 1989;27(1):71-81. (PMID: 2496329); J Neurosci. 2007 Apr 4;27(14):3839-44. (PMID: 17409248); Nat Neurosci. 2013 Sep;16(9):1188-90. (PMID: 23912946); Brain. 2001 Dec;124(Pt 12):2476-89. (PMID: 11701601); Proc Natl Acad Sci U S A. 2014 Oct 21;111(42):15238-43. (PMID: 25246561); Nat Commun. 2017 Feb 14;8:14415. (PMID: 28195129); J Neurosci. 2015 Sep 9;35(36):12477-87. (PMID: 26354915); Psychol Rev. 1995 Jul;102(3):419-57. (PMID: 7624455); Proc Natl Acad Sci U S A. 2015 Sep 1;112(35):11078-83. (PMID: 26283350); Hippocampus. 2005;15(7):827-40. (PMID: 16149082); Curr Biol. 2013 Jun 17;23(12):1101-6. (PMID: 23746635); Neuroimage. 2017 Jul 15;155:60-71. (PMID: 28377210); Neuroscience. 2003;116(1):201-11. (PMID: 12535953); Neuroimage. 2014 Jan 15;85 Pt 2:648-55. (PMID: 23769913); Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):12297-12302. (PMID: 29078334); J Neurosci. 2018 May 9;38(19):4471-4481. (PMID: 29636396); Neuron. 1995 Nov;15(5):1053-63. (PMID: 7576649) |
| Grant Information: | T32 NS064928 United States NS NINDS NIH HHS; S10 OD018211 United States OD NIH HHS; Cooperative Agreement N66001-14-2-4032 International DOD | Defense Advanced Research Projects Agency (DARPA); MH104606 International U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH); 1S10OD018211-01 International U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS); R01 MH104606 United States MH NIMH NIH HHS |
| Entry Date(s): | Date Created: 20180623 Date Completed: 20181211 Latest Revision: 20190621 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC6013427 |
| DOI: | 10.1038/s41467-018-04847-9 |
| PMID: | 29930307 |
| Database: | MEDLINE |
Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't