Abstract
Theta oscillations (electroencephalographic activity with a frequency of 4â8âHz) have long been implicated in spatial navigation in rodents1,2,3,; however, the role of theta oscillators in human spatial navigation has not been explored. Here we describe subdural recordings from epileptic patients learning to navigate computer-generated mazes. Visual inspection of the raw intracranial signal revealed striking episodes of high-amplitude slow-wave oscillations at a number of areas of the cortex, including temporal cortex. Spectral analysis showed that these oscillations were in the theta band. These episodes of theta activity, which typically last several cycles, are dependent on task characteristics. Theta oscillations occur more frequently in more complex mazes; they are also more frequent during recall trials than during learning trials.
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References
Winson, J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201, 160â163 (1978).
O'Keefe, J. & Recce, M. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317â330 (1993).
Skaggs, W. E., McNaughton, B. L., Wilson, M. A. & Barnes, C. A. Theta phase precision in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149â172 (1996).
Bland, B. H. The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol. 26, 1â54 (1986).
Stewart, M. & Fox, S. E. Hippocampal theta activity in monkeys. Brain Res. 538, 59â63 (1991).
Huerta, P. T. & Lisman, J. E. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364, 723â725 (1993).
Buzsaki, G. Two-stage model of memory trace formation: role for ânoisyâ brain states. Neuroscience 31, 551â570 (1989).
Sohal, V. S. & Hasselmo, M. E. GABA(B) modulation improves sequence disambiguation in computational models of hippocampal region CA3. Hippocampus 8, 171â193 (1998).
Buzsaki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81â92 (1996).
Lisman, J. E. & Idiart, M. A. Storage of 7+/â2 short-term memories in oscillatory subcycles. Science 267, 1512â1515 (1995).
Buzsaki, G. Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res. 7, 17â23 (1998).
Jensen, O. & Lisman, J. E. An oscillatory short-term memory buffer model can account for data on the Sternberg task. J. Neurosci. 18, 10688â10699 (1998).
Borst, J. G., Leung, L. W. & MacFabe, D. F. Electrical activity of the cingulate cortex. II. Cholinergic modulation. Brain Res. 407, 81â93 (1987).
Slawinska, U. & Kasicki, S. Theta-like rhythm in depth EEG activity of hypothalamic areas during spontaneous or electrically induced locomotion in the rat. Brain Res. 678, 117â126 (1995).
Routtenberg, A. & Taub, F. Hippocampus and superior colliculus: congruent EEG activity demonstrated by a simple measure. Behav. Biol. 8, 801â805 (1973).
Halgren, E., Babb, T. L. & Crandall, P. H. Human hippocampal formation EEG desynchronizes during attentiveness and movement. Electroencephalograph. Clin. Neurophysiol. 44, 778â781 (1978).
Arnolds, D. E. A. T., Lopes Da Silva, F. H., Aitink, J. W., Kamp, A. & Boeijinga, P. The spectral properties of hippocampal EEG related to behaviour in man. Electroencephalogr. Clin. Neurophysiol. 50, 324â328 (1980).
Tesche, C. D. Non-invasive detection of ongoing neuronal population activity in normal human hippocampus. Brain Res. 749, 53â60 (1997).
Aguirre, G. K., Detre, J. A., Alsop, D. C. & D'Esposito, M. The parahippocampus subserves topographical learning in man. Cerebral Cortex 6, 823â829 (1996).
Maguire, E. A. et al. Knowing where and getting there: a human navigation network. Science 280, 921â924 (1998).
Epstein, R. & Kanwisher, N. Acortical representation of the local visual environment. Nature 392, 598â601 (1998).
Maguire, E. A., Frackowiak, S. J. & Frith, C. D. Learning to find your way: a role for the human hippocampal formation. Proc. R. Soc. Lond. B 263, 1745â1750 (1996).
Maguire, E. A., Frackowiak, S. J. & Frith, C. J. Recalling routes around London: activation of the right hippocampus in taxi drivers. J. Neurosci. 17, 7103â7110 (1997).
Sperling, M. R. Clinical challenges in invasive monitoring in epilepsy surgery. Epilepsia (Suppl.) 38, S6âS12 (1997).
Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain(Verlag, Stuttgart, 1988).
Tulving, E. Elements of Episodic Memory(Oxford Univ. Press, New York, 1983).
Grossmann, A. & Morlet, J. Mathematics + Physics Vol. 1(World Scientific, Singapore, 1985).
Acknowledgements
This work was supported by NIH. We thank J. Lisman for encouraging our search for theta; J. Lisman and O. Jensen for helpful discussions during the course of this research; and E. Tulving, E. Marder, L. Abbott and E. Menschik for helpful comments on a previous version of this manuscript. Weacknowledge the cooperation of colleagues in the Children's Hospital Epilepsy program including P.M. Black, B. Bourgeois, F. Duffy and L. Kull. Finally, we thank the patients and their families for their participation and support.
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Kahana, M., Sekuler, R., Caplan, J. et al. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399, 781â784 (1999). https://doi.org/10.1038/21645
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DOI: https://doi.org/10.1038/21645
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