Propagating Wave and Irregular Dynamics: Spatiotemporal Patterns of Cholinergic Theta Oscillations in Neocortex In Vitro

Department of Physiology and Biophysics, Georgetown University, Washington DC, 20057-1421 Submitted 31 December 2002; accepted in final form 18 February 2003 Neocortical "theta" oscillation (5–12 Hz) has been observed in animals and human subjects but little is known about how the oscillation is organized in the cortical intrinsic networks. Here we use voltage-sensitive dye and optical imaging to study a carbachol/bicuculline induced theta ( 8 Hz) oscillation in rat neocortical slices. The imaging has large signal-to-noise ratio, allowing us to map the phase distribution over the neocortical tissue during the oscillation. The oscillation was organized as spontaneous epochs and each epoch was composed of a "first spike," a "regular" period (with relatively stable frequency and amplitude), and an "irregular" period (with variable frequency and amplitude) of oscillations. During each cycle of the regular oscillation, one wave of activation propagated horizontally (parallel to the cortical lamina) across the cortical section at a velocity of 50 mm/s. Vertically the activity was synchronized through all cortical layers. This pattern of one propagating wave associated with one oscillation cycle was seen during all the regular cycles. The oscillation frequency varied noticeably at two neighboring horizontal locations (330 µm apart), suggesting that the oscillation is locally organized and each local oscillator is about ≤300 µm wide horizontally. During irregular oscillations, the spatiotemporal patterns were complex and sometimes the vertical synchronization decomposed, suggesting a de-coupling among local oscillators. Our data suggested that neocortical theta oscillation is sustained by multiple local oscillators. The coupling regime among the oscillators may determine the spatiotemporal pattern and switching between propagating waves and irregular patterns. Address for reprint requests: J.-Y. Wu, Georgetown University, Rm 247, Basic Science Building, 3900 Reservoir Rd. NW, Washington, DC 20057 (E-mail: wuj{at}georgetown.edu ).