Volume 16, Number 10,
Issue of May 15, 1996
pp. 3412-3426
Copyright ©1996 Society for Neuroscience
Morphological Correlates of Bilateral Synchrony in the Rat
Cerebellar Cortex
Received Jan. 24, 1996; revised Feb. 21, 1996; accepted Feb. 27, 1996.
C. I. De Zeeuw1, 2,
E.
J. Lang1,
I. Sugihara1,
T. J. H. Ruigrok2,
L. M. Eisenman4,
E. Mugnaini3, and
R. Llinás1
1 Department of Physiology and Neuroscience, New York
University Medical School, New York, New York 10016, 2 Department of Anatomy, Erasmus University Rotterdam, The
Netherlands, 3 Institute of Neuroscience, Northwestern
University, Chicago, Illinois 60611, and 4 Daniel Baugh
Institute of Anatomy, Jefferson Medical College, Thomas Jefferson
University, Philadelphia, Pennsylvania 19107
Simultaneous recordings of the left and right crus IIA of the
cerebellar cortex in the rat have demonstrated that Purkinje cells of
both sides can be activated synchronously by their climbing fibers.
Because climbing fibers arise exclusively from the contralateral
inferior olive (IO), this physiological finding seems to contradict the
anatomy. To define the structural basis responsible for the bilateral
synchrony, we examined the possibilities that bilateral common afferent
inputs to the IO and interolivary connections form the underlying
mechanisms.
The bilaterality of the major afferents of the olivary regions that
project to crus IIA was studied using Phaseolus vulgaris
leucoagglutinin as an anterograde tracer. We found that the excitatory
and inhibitory projections from the spinal trigeminal nucleus and
dorsolateral hump of the interposed cerebellar nucleus to the
transition area between the principal olive and dorsal accessory olive
were bilateral.
A second possible mechanism for bilateral synchrony, which is the
possibility that axons of olivary neurons provide collaterals to the
contralateral side, was investigated using biotinylated dextran amine
as an anterograde tracer. Labeled axons were traced and reconstructed
from the principal olive and dorsal and medial accessory olive up to
the entrance of the contralateral restiform body. None of these axons
gave rise to collaterals.
The possibility that neurons in the left and right IO are
electrotonically coupled via dendrodendritic connections was
investigated by examining the midline region of the IO. The neuropil of
the left and right IO is continuous in the dorsomedial cell column.
Examination of Golgi impregnations of this subdivision demonstrated
that (1) many dendrites cross from one side to the other, (2) neurons
close to the midline give rise to dendrites that extend into both
olives, and (3) dendrites of neurons in the dorsomedial cell column
frequently traverse into adjacent olivary subdivisions such as the
medial accessory olive and the transition area between the principal
olive and dorsal accessory olive. Sections immunostained for dendritic
lamellar bodies or GABAergic terminals showed the same pattern: the
neuropils of the dorsomedial cell columns on both sides form a
continuum with each other as well as with the neuropil of other
adjacent olivary subdivisions. Ultrastructural examination of the
dorsomedial cell column demonstrated that the midline area includes
many complex glomeruli that contain dendritic spines linked by gap
junctions.
To verify whether the complex spike synchrony observed between left and
right crus IIA could indeed be mediated in part through coupled neurons
in the dorsomedial cell column, we recorded simultaneously from crus
IIA areas and from left and right vermal lobule IX, which receives
climbing fibers from the dorsomedial cell column. In these experiments
we demonstrated that the climbing fibers of all four areas, i.e., the
left and right crus IIA as well as the left and right lobule IX, can
fire synchronously.
The present results indicate that synchronous climbing fiber activation
of the left and right crus IIA in the rat can be explained by (1)
bilateral inputs to the transition areas between the principal olive
and dorsal accessory olive and (2) dendrodendritic electrotonic
coupling between neurons of the left and right dorsomedial cell column
and between neurons of the dorsomedial cell column and adjacent olivary
subdivisions.
Key words:
inferior olive;
gap junctions;
electrotonic coupling;
complex spikes;
dendritic lamellar bodies;
dorsomedial cell column;
spinal trigeminal nucleus;
cerebellar nuclei;
GABA
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