Spindle Waves are Propagating Synchronized Oscillations in the Ferret LGNd
in vitro.
Kim, Uhnoh, Thierry Bal, and David A. McCormick.
Section of Neurobiology, Yale University School of Medicine, 333 Cedar
Street, New Haven, Connecticut 06510 USA, (203) 785-4577, FAX: (203) 785-
5263.
APStracts 2:0183N, 1995.
SUMMARY AND CONCLUSIONS
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 to 1.5 mm/sec 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 occur spontaneously in any part of the LGNd/PGN. Upon initiation of a
spindle wave, spindle waves propagate away from the site of initiation.
Spindle waves may propagate only locally or 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 and
another. 3. Repetitive electrical stimulation reveals that spindle wave
generation and propagation exhibit a relative refractory period of between 7
and 14 seconds 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-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 prior to
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 following the generation of a spindle wave, but slowly returns
over a 7-14 second 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 co-active, 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 GABAA receptors
with (-)-bicuculline methiodide results in the transformation of spindle waves
into a 3-4 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 seconds, 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 networks.
Received 7 April 1995; accepted in final form 8 June 1995.
APS Manuscript Number J230-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on 6 July 1995.