SPINDLE WAVES ARE PROPAGATING SYNCHRONIZED OSCILLATIONS IN THE FERRET LGND IN-VITRO

1. The cellular features of propagation of spindle waves and a bicuculline-induced slow oscillation through sagittal slices of the ferret dorsal lateral geniculate nucleus (LGNd) maintained in vitro were examined with simultaneous extracellular and intracellular recordings from up to eight sites. Spindle waves typically propagated along the long axis (dorsal-ventral) of the sagital slice at a speed of 0.3-1.5 mm/s and were synchronized along the line of projection between the perigeniculate nucleus (PGN) and the A, A1, and C laminae. 2. Spindle waves can be initiated with local electrical stimulation or can occur spontaneously in any part of the LGNd/PGN. On initiation of a spindle wave, spindle waves propagate away from the site of initiation. Spindle waves may propagate only locally or may collide with other spindle waves. Collision of spindle waves is associated with synchronization of the two network oscillations, and the spindle waves do not propagate past one another. 3. Repetitive electrical stimulation reveals that spindle wave generation and propagation exhibit a relative refractory period of between 7 and 14 s in vitro. Stimulation at rates of less than the refractory period results in the generation of abbreviated local spindle waves at the stimulation site, but not in the propagation of this spindle wave into adjacent regions of the slice. 4. Local block of non-N-methyl-D-aspartate (non-NMDA) excitatory amino acid receptors in the PGN with 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) prevents the propagation of spindle waves across the point of application, indicating that the excitation of PGN neurons by thalamocortical cells is essential to the propagation of these oscillations. The local antagonism of non-NMDA receptors in the PGN results in the dorsal and ventral aspects of the LGNd slice behaving as independent spindle wave generators, even if before application of CNQX they were not. 5. Activation of a burst discharge in a single PGN neuron can result in the generation of a full spindle wave and the propagation of this spindle wave both dorsally and ventrally through the slice away from the activated PGN neuron. The ability of a burst of action potentials in a PGN neuron to generate a spindle wave is suppressed immediately after the generation of a spindle wave, but slowly returns over a 7- to 14-s period corresponding to the relative spindle wave refractory period. 6. The degree of synchrony between two recording sites, as well as the percentage of time these two sites are coactive, decreases as the distance between the recording sites increases. Phase lags and leads between different recording sites appear to be related to differences in the intraspindle frequency between recording sites. 7. Block of gamma-aminobutyric acid-A (GABA(A)) receptors with (-)-bicuculline methiodide results in the transformation of spindle waves into a 3- to 4-Hz slow oscillation characterized by pronounced burst firing in thalamocortical and PGN neurons. This bicuculline-induced slow oscillation exhibits the same properties as spindle waves, including dorsal-ventral travel, a refractory period of 20-30 s, and relative synchronization across active portions of the slice. This oscillation, however, could not be initiated by burst firing in a single PGN neuron. 8. We suggest that spindle waves and the bicuculline-induced slow oscillation propagate through the thalamus by progressive recruitment of neighboring neurons into the oscillation and that synchrony of neuronal activity results from a large degree of overlap in efferent and afferent connections. Owing to a relative refractory period, these network oscillations can be organized into relatively stable and repeating patterns of activity, which may be useful for the maintenance and regulation of thalamocortical synaptic net-works.