Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze

Journal of Neuroscience

Volumn 28, Issue 23, 2008, Pages 5983-5990

  Cornwell, Brian R ^a   Johnson, Linda L ^a   Holroyd, Tom ^a   Carver, Frederick W ^a   Grillon, Christian ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Hippocampus; Magnetoencephalography; Morris water maze; Spatial memory; Synthetic aperture magnetometry; Theta rhythm

Indexed keywords

ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; HIPPOCAMPUS THETA RHYTHM; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; MAZE TEST; MENTAL PERFORMANCE; NORMAL HUMAN; OSCILLATION; PRIORITY JOURNAL; SUBICULUM; TEMPORAL CORTEX; VIRTUAL REALITY; ADULT; BEHAVIOR; COMPARATIVE STUDY; COMPUTER INTERFACE; HIPPOCAMPUS; METHODOLOGY; MOTIVATION; PHOTOSTIMULATION; PHYSIOLOGY; PREDICTION AND FORECASTING; PSYCHOMOTOR PERFORMANCE; THETA RHYTHM;

ADULT; FEMALE; GOALS; HIPPOCAMPUS; HUMANS; MALE; MAZE LEARNING; PARAHIPPOCAMPAL GYRUS; PHOTIC STIMULATION; PREDICTIVE VALUE OF TESTS; PSYCHOMOTOR PERFORMANCE; SPATIAL BEHAVIOR; THETA RHYTHM; USER-COMPUTER INTERFACE;

EID: 44949242629     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5001-07.2008     Document Type: Article

References (50)

1. Astur RS, Ortiz ML, Sutherland RJ (1998) A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav Brain Res 93:185-190.
2. Astur RS, Taylor LB, Mamelak AN, Philpott L, Sutherland RJ (2002) Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav Brain Res 132:77-84.
3. Bohbot VD, Kalina M, Stephankova K, Spackova N, Petrides M, Nadel L (1998) Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 36:1217-1238.
4. Burgess N, Maguire EA, O'Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
5. Buzsaki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15:827-840.
6. Caplan JB, Madsen JR, Raghavachari S, Kahana MJ (2001) Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. J Neurophysiol 86:368-380.
7. Caplan JB, Madsen JR, Schulze-Bonhage A, Aschenbrenner-Scheibe R, Kahana MJ (2003) Human theta oscillations related to sensorimotor integration and spatial learning. J Neurosci 23:4726-4736.
8. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162-173.
9. de Araujo DB, Baffa O, Wakai RT (2002) Theta oscillations and human navigation: a magnetoencephalography study. J Cogn Neurosci 14:70-78.
10. Driscoll I, Hamilton DA, Petropoulos H, Yeo RA, Brooks WM, Baumgartner RN, Sutherland RJ (2003) The aging hippocampus: cognitive, biochemical and structural findings. Cereb Cortex 13:1344-1351.
11. Duncko R, Cornwell B, Cui L, Merikangas KR, Grillon C (2007) Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learn Mem 14:329-335.
12. Ekstrom AD, Caplan JB, Ho E, Shattuck K, Fried I, Kahana MJ (2005) Human hippocampal theta activity during virtual navigation. Hippocampus 15:881-889.
13. First MB, Spitzer RI, Williams JBW, Gibbon M (1995) Structured clinical interview fro DSM-IV (SCID). Washington, DC: American Psychiatric Association.
14. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using false discovery rates. NeuroImage 15:772-786.
15. Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 7:374-385.
16. Ghaem O, Mellet E, Crivello F, Tzourio N, Mazoyer B, Berthoz A, Denis M (1997) Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. NeuroReport 8:739-744.
17. Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37:877-888.
18. Hillebrand A, Singh KD, Holliday IE, Furlong PL, Barnes GR (2005) A new approach to neuroimaging with magnetoencephalography. Hum Brain Mapp 25:199-211.
19. Jacobs J, Kahana MJ, Ekstrom AD, Fried I (2007) Brain oscillations control timing of single-neuron activity in humans. J Neurosci 27:3839-3844.
20. Jacobs WJ, Laurance HE, Thomas KGF (1998a) Place learning in virtual space. I. Acquisition, overshadowing, and transfer. Learn Motiv 28:521-541.
21. Jacobs WJ, Thomas KGF, Laurance HE, Nadel L (1998b) Place learning in virtual space. II. Topographical relations as one dimension of stimulus control. Learn Motiv 29:288-308.
22. Jensen O, Tesche CD (2002) Frontal theta activity in humans increases with memory load in a working memory task. Eur J Neurosci 15:1395-1399.
23. Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madsen JR (1999) Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399:781-784.
24. Kelemen E, Moron I, Fenton AA (2005) Is the hippocampus theta rhythm related to cognition in a non-locomotor place recognition task? Hippocampus 15:472-479.
25. Kessels RPC, Hendriks MPH, Schouten J, van Asselen M, Postma A (2004) Spatial memory deficits in patients after unilateral selective amygdalohippocampectomy. J Int Neuropsychol Soc 10:907-912.
26. Klimesch W, Doppelmayr M, Russegger H, Pachinger T (1996) Theta band power in the human scalp EEG and the encoding of new information. NeuroReport 7:1235-1240.
27. Klimesch W, Doppelmayr M, Schimke H, Ripper B (1997) Theta synchronization and alpha desynchronization in a memory task. Psychophysiology 34:169-176.
28. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120-131.
29. Maguire EA, Burgess N, Donnett JG, Frackowiak RSJ, Frith CD, O'Keefe J (1998) Knowing where, and getting there: a human navigation network. Science 280:921-924.
30. Maguire EA, Burgess N, O'Keefe J (1999) Human spatial navigation: cognitive maps, sexual dimorphism, and neural substrates. Cur Opin Neurobiol 9:171-177.
31. Mehta MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741-746.
32. Mitchell KJ, Johnson MK, Raye CL, D'Esposito M (2000) fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. Cogn Brain Res 10:197-206.
33. Morris RGM (1981) Spatial localization does not require the presence of local cues. Learn Motiv 12:239-260.
34. Morris RGM, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
35. Ohnishi T, Matsuda H, Hirakata M, Ugawa Y (2006) Navigation ability dependent neural activation in the human brain: an fMRI study. Neurosci Res 55:361-369.
36. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
37. Olvera-Cortes E, Guevara MA, Gonzalez-Burgos I (2004) Increase of the hippocampal theta activity in the Morris water maze reflects learning rather than motor activity. Brain Res Bull 62:379-384.
38. Robinson SE, Vrba J (1999) Functional neuroimaging by synthetic aperture magnetometry (SAM). In: Recent advances in biomagnetism (Yoshimoto T, Kotani M, Kuriki S, Karibe, H, Nakasato N, eds), pp 302-305. Sendai, Japan: Tohoku UP.
39. Samsonovich AV, Ascoli GA (2005) A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval. Learn Mem 12:193-208.
40. Schultz M, Chau W, Graham SJ, McIntosh AR, Ross B, Ishii R, Pantev C (2004) An integrative MEG-fMRI study of the primary somatosensory cortex using crossmodal correspondence analysis. NeuroImage 22:120-133.
41. Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR (2003) Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 23:10809-10814.
42. Singh KD, Barnes GR, Hillebrand A, Forde EM, Williams AL (2002) Task-related changes in cortical synchronization are spatially coincident with the hemodynamic response. NeuroImage 16:103-114.
43. Skaggs WE, McNaughton BL, Wilson MA, Barnes C (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
44. Spiers HJ, Burgess N, Maguire EA, Baxendale SA, Hartley T, Thompson P, O'Keefe J (2001) Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain 124:2476-2489.
45. Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279-306.
46. Stockwell RG, Mansinha L, Lowe RP (1996) Localization of the complex spectrum: the S transform. IEEE Trans Signal Process 44:998-1000.
47. Tesche CD, Karhu J (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci USA 97:919-924.
48. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578-598.
49. Vrba J, Robinson SE (1999) Signal processing in magnetoencephalography. Methods 25:249-271.
50. Wolbers T, Buchel C (2005) Dissociable retrospenial and hippocampal contributions to successful formation of survey representations. J Neurosci 25:3333-3340.