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

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Human 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. Kahana^1,2

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

oscillations in the rat hippocampus have been implicated in sensorimotor integration (Bland, 1986), especially during exploratory and wayfinding behavior. We propose that human cortical 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 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. oscillations had different topographic and spectral characteristics during searching than during goal-seeking, suggesting that different cortical networks exhibit 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 band appeared to be related to simple motor planning, likely a variant of the Rolandic µ rhythm. These findings suggest that human cortical oscillations act to coordinate sensory and motor brain activity in various brain regions to facilitate exploratory learning and navigational planning.

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

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

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