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The Journal of Neuroscience, September 15, 2002, 22(18):8158-8169
Synaptic Convergence of Motor and Somatosensory Cortical
Afferents onto GABAergic Interneurons in the Rat Striatum
Sankari
Ramanathan1,
Jason J.
Hanley1,
Jean-Michel
Deniau2, and
J.
Paul
Bolam1
1 Medical Research Council Anatomical Neuropharmacology
Unit, Department of Pharmacology, Oxford, OX1 3TH, United Kingdom,
and 2 Institut National de la Santé et de la
Recherche Médicale U114, Collège de France, 75321 Paris
Cedex 05, France
Cortical afferents to the basal ganglia, and in particular the
corticostriatal projections, are critical in the expression of basal
ganglia function in health and disease. The corticostriatal projections
are topographically organized but also partially overlap and
interdigitate. To determine whether projections from distinct cortical
areas converge at the level of single interneurons in the striatum,
double anterograde labeling from the primary motor (M1) and primary
somatosensory (S1) cortices in the rat, was combined with
immunolabeling for parvalbumin (PV), to identify one population of
striatal GABAergic interneurons.
Cortical afferents from M1 and S1 gave rise to distinct, but partially
overlapping, arbors of varicose axons in the striatum. PV-positive
neurons were often apposed by cortical terminals and, in many
instances, apposed by terminals from both cortical areas. Frequently,
individual cortical axons formed multiple varicosities apposed to the
same PV-positive neuron. Electron microscopy confirmed that the
cortical terminals formed asymmetric synapses with the dendrites and
perikarya of PV-positive neurons as well as unlabelled dendritic
spines. Correlated light and electron microscopy revealed that
individual PV-positive neurons received synaptic input from axon
terminals derived from both motor and somatosensory cortices.
These results demonstrate that, within areas of overlap of functionally
distinct projections, there is synaptic convergence at the single cell
level. Sensorimotor integration in the basal ganglia is thus likely to
be mediated, at least in part, by striatal GABAergic interneurons.
Furthermore, our findings suggest that the pattern of innervation of
GABAergic interneurons by cortical afferents is different from the
cortical innervation of spiny projection neurons.
Key words:
GABA; striatum; corticostriatal; parvalbumin; cortex; basal ganglia
Copyright © 2002 Society for Neuroscience 0270-6474/02/22188158-12$05.00/0
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