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

Abstract

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.

Large-scale model of mammalian thalamocortical systems

“…The waves had a spatial extent of up to a centimeter and a speed of Ϸ0.1 m/s. These measures are similar to propagating neocortical waves observed in vitro (28) and in vivo in visual cortex of anesthetized rats (29). They are slower than those in vivo in primary motor and dorsal premotor cortices of monkeys (30) and in turtle visual cortex (31).…”

Studies of stimulus parameters for seizure disruption using neural network simulations

“…Transit speeds for organized waves of activity within the model range from 13-30 mm/sec, which compares favorably with measured propagating wave speeds in neocortical slice preparations (30-50 mm/sec) (Wu et al 1999;Bao and Wu 2003). Depending on the connectivity pattern used, our model also exhibits organized rhythmic activity within a physiologic range of 3-20 Hz.…”

The Source of Afterdischarge Activity in Neocortical Tonic–Clonic Epilepsy

“…A second issue is timing: their proposed mechanism is likely to be constrained by the time course of the Ca 2ϩ spike, and thus a mechanism that could explain reversal of discharges that are occurring in the theta band (5-12 Hz, as in their disinhibited hippocampal slices) rather than the delta rhythm (0.5-2 Hz) of the afterdischarges in our neocortical slices. Spontaneous changes in wave propagation have been noted previously in both the hippocampus (Finnerty and Jefferys, 2000;Luhmann et al, 2000;Derchansky et al, 2006) and neocortex (Bao and Wu, 2003). Coupled oscillators have been proposed to underlie these spontaneous switches (Bao and Wu, 2003;Derchansky et al, 2006), although once again, this latter mechanism necessarily works at a higher frequency (theta rather than delta) because the latency of activation between oscillators has to be approximately half the period of the oscillation.…”

“…Spontaneous changes in wave propagation have been noted previously in both the hippocampus (Finnerty and Jefferys, 2000;Luhmann et al, 2000;Derchansky et al, 2006) and neocortex (Bao and Wu, 2003). Coupled oscillators have been proposed to underlie these spontaneous switches (Bao and Wu, 2003;Derchansky et al, 2006), although once again, this latter mechanism necessarily works at a higher frequency (theta rather than delta) because the latency of activation between oscillators has to be approximately half the period of the oscillation. It is possible, however, that, although the rhythms we record are ostensibly much slower, at the actual site of reversal the apparent rhythm may be at the requisite theta frequency and, thus, the reversals could indeed be mediated by these previously described mechanisms.…”