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Direct Recording of Theta Oscillations in Primate Prefrontal and Anterior Cingulate Cortices

¹Department of Integrative Brain Science and ²Department of Neurology, Graduate School of Medicine, Kyoto University, Kyoto; ³Center for Brain Experiment, National Institute for Physiological Sciences, Okazaki; ⁴Department of System Neuroscience, Tokyo Metropolitan Institute for Neuroscience, Tokyo; ⁵Department of Neurology, Graduate School of Medicine, Tokushima University, Tokushima; and ⁶Neural Circuit Theory, RIKEN Brain Science Institute, Saitama, Japan

Submitted 11 July 2005; accepted in final form 31 January 2006

Recent evidence has suggested that theta-frequency (4–7 Hz) oscillations around the human anterior cingulate cortex (ACC) and frontal cortex—that is, frontal midline theta (Fm theta) oscillations—may be involved in attentional processes in the brain. However, little is known about the physiological basis of Fm theta oscillations because invasive study in the human is allowed in only limited cases. In the present study, we developed a monkey model for Fm theta oscillations and located the generators of theta waves using electrodes implanted in various cortical areas. Monkeys were engaged in a self-initiated hand-movement task with a waiting period. The theta power in area 9 (the medial prefrontal cortex) and area 32 (the rostral ACC) was gradually increased from a few seconds before the movement and reached a peak immediately after the movement. When the movement was rewarded, the theta power attained a second peak, whereas it swiftly decreased in the unrewarded trials. Theta oscillations in areas 9 and 32 were coherent and phase locked together. This theta activity may be associated with "executive attention" including self-control, internal timing, and assessment of reward. It is probably a homologue of human Fm theta oscillations, as judged from the similar localization, corresponding frequency, and dependency on attentional processes. The monkey model would be useful for studying executive functions in the frontal cortex.

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