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The Journal of Neuroscience, June 1, 1999, 19(11):4674-4681
Relationships between the Prefrontal Cortex and the Basal Ganglia
in the Rat: Physiology of the Cortico-Nigral Circuits
Nicolas
Maurice1,
Jean-Michel
Deniau2,
Jacques
Glowinski1, and
Anne-Marie
Thierry1
1 Chaire de Neuropharmacologie, Institut National de la
Santé et de la Recherche Médicale U114, Collège de
France, 75231 Paris Cedex 05, France, and
2 Université Pierre et Marie Curie, Département
de Neurochimie-Neuroanatomie, Institut des Neurosciences, Unité
de Recherche Mixte 7624, 75230 Paris Cedex 05, France
The prelimbic/medial orbital areas (PL/MO) of the rat prefrontal
cortex are connected to substantia nigra pars reticulata (SNR) through
three main circuits: a direct nucleus accumbens (NAcc)-SNR pathway, an
indirect NAcc-SNR pathway involving the ventral pallidum (VP) and the
subthalamic nucleus (STN), and a disynaptic cortico-STN-SNR pathway.
The present study was undertaken to characterize the effect of PL/MO
stimulation on SNR cells and to determine the contribution of these
different pathways. The major pattern of responses observed in the SNR
was an inhibition preceded by an early excitation and followed or not
by a late excitation. The inhibition resulted from the activation of
the direct NAcc-SNR pathway because it disappeared after acute
blockade of the glutamatergic cortico-striatal transmission by CNQX
application into the NAcc. The late excitation resulted from the
activation of the indirect NAcc-VP-STN-SNR pathway via a
disinhibition of the STN because it disappeared after either CNQX
application into the NAcc or blockade of the GABAergic striato-pallidal
transmission by bicuculline application into the VP. The early
excitation, which was markedly decreased after blockade of the
cortico-STN transmission by CNQX application into the STN, resulted
from the activation of the disynaptic cortico-STN-SNR pathway.
Finally, the blockade of the cortico-STN-VP circuit by CNQX
application into STN or VP modified the influence of the trans-striatal
circuits on SNR cells. This study suggests that, in the prefrontal
cortex-basal ganglia circuits, the trans-subthalamic pathways, by
their excitatory effects, participate in the shaping of the inhibitory
influence of the direct striato-nigral pathway on SNR neurons.
Key words:
basal ganglia circuits; prefrontal cortex; subthalamic
nucleus; ventral striatum; nucleus accumbens; ventral pallidum; substantia nigra pars reticulata; in vivo single unit
recordings; rat
Copyright © 1999 Society for Neuroscience 0270-6474/99/19114674-08$05.00/0
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