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The Journal of Neuroscience, June 1, 2003, 23(11):4726-4736

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Human {theta} Oscillations Related to Sensorimotor Integration and Spatial Learning

Jeremy B. Caplan,1 Joseph R. Madsen,2,3 Andreas Schulze-Bonhage,4 Richard Aschenbrenner-Scheibe,4 Ehren L. Newman,1 and Michael J. Kahana1,2

1 Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454, 2 Department of Neurosurgery, Children's Hospital, Boston, Massachusetts 02115, 3 Department of Surgery, Harvard Medical School, Boston, Massachusetts 02115, and 4 Neurozentrum, Universität Freiburg, 79106 Freiburg, Germany

{theta} oscillations in the rat hippocampus have been implicated in sensorimotor integration (Bland, 1986), especially during exploratory and wayfinding behavior. We propose that human cortical {theta} activity coordinates sensory information with a motor plan to guide wayfinding behavior to known goal locations. To test this hypothesis, we analyzed invasive recordings from epileptic patients while they performed a spatially immersive, virtual taxi driver task. Consistent with this hypothesis, we found {theta} oscillations during both exploratory search and goal-seeking behavior and, in particular, during virtual movement, when sensory information and motor planning were both in flux, compared with periods of self-initiated stillness. {theta} oscillations had different topographic and spectral characteristics during searching than during goal-seeking, suggesting that different cortical networks exhibit {theta} depending on which cognitive functions are driving behavior (spatial learning during exploration vs orienting to a learned representation during goal-seeking). In contrast, oscillations in the {beta} band appeared to be related to simple motor planning, likely a variant of the Rolandic µ rhythm. These findings suggest that human cortical {theta} oscillations act to coordinate sensory and motor brain activity in various brain regions to facilitate exploratory learning and navigational planning.

Key words: {theta} oscillations; intracranial electroencephalography; spatial navigation; spatial memory; sensorimotor integration; wayfinding


Received Oct. 28, 2002; revised Feb. 21, 2003; accepted Mar. 5, 2003.




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