Basal ganglia and processing of cortical information: functional interactions between trans-striatal and trans-subthalamic circuits in the substantia nigra pars reticulata

The substantia nigra pars reticulata (SNR), a major output station of basal ganglia, receives information from the cerebral cortex through three main pathways, i.e. a direct inhibitory trans-striatal pathway, an indirect excitatory trans-striatal pathway that involves the pallidum and the subthalamu...

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Bibliographic Details
Published in:Neuroscience 2003-01, Vol.117 (4), p.931-938
Main Authors: Kolomiets, B.P, Deniau, J.M, Glowinski, J, Thierry, A.M
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
auditory cortex
Auditory Cortex - cytology
Auditory Cortex - physiology
Biological and medical sciences
Central nervous system
Cerebral Cortex - cytology
Cerebral Cortex - physiology
Corpus Striatum - cytology
Corpus Striatum - physiology
Electric Stimulation
Electrophysiology
Fundamental and applied biological sciences. Psychology
Male
Models, Neurological
motor cortex
Motor Cortex - cytology
Motor Cortex - physiology
Neural Inhibition - physiology
Neural Pathways - cytology
Neural Pathways - physiology
Neurons - cytology
Neurons - physiology
prefrontal cortex
Prefrontal Cortex - cytology
Prefrontal Cortex - physiology
Rats
Rats, Sprague-Dawley
Substantia Nigra - cytology
Substantia Nigra - physiology
Subthalamic Nucleus - cytology
Subthalamic Nucleus - physiology
Synaptic Transmission - physiology
Vertebrates: nervous system and sense organs
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Summary:The substantia nigra pars reticulata (SNR), a major output station of basal ganglia, receives information from the cerebral cortex through three main pathways, i.e. a direct inhibitory trans-striatal pathway, an indirect excitatory trans-striatal pathway that involves the pallidum and the subthalamus and a direct excitatory trans-subthalamic pathway. In order to determine how cortical information flow originating from functionally distinct cortical areas and processed through the trans-striatal and trans-subthalamic pathways is integrated within the SNR, the responses induced by electrical stimulation of prefrontal, motor and auditory cortex in SNR cells were analyzed in anesthetized rats. Further confirming that direct striato-nigral pathways related to these functionally distinct cortical areas are organized in parallel channels, stimulation of the prefrontal, motor and auditory cortex induced an inhibitory response on distinct subpopulations of SNR cells. Within a given channel, the direct trans-striatal and the trans-subthalamic pathways converge on a large number of nigral cells. In addition, the present study reveals that nigral cells receiving an inhibitory input from a given cortical area through the direct trans-striatal pathway can also receive an excitatory input from a functionally distinct cortical area through the trans-subthalamic pathways. Such a convergence mainly occurred between the direct striato-nigral pathway issued from the auditory cortex and the trans-subthalamic pathways issued from the motor cortex. These data reveal the existence of a converging influence of trans-subthalamic and direct striato-nigral pathways not only within but also across channels. Within a given cortico-basal ganglia channel, the trans-subthalamic pathways likely contribute to the temporal shaping of the striato-nigral inhibition and thus of the disinhibition of the related nigral target nuclei in the thalamus and mesencephalon. Across channels, the specific interactions between trans-subthalamic and direct striato-nigral pathways could contribute to prevent inhibition of subpopulations of nigral cells implicated in competing functions.
ISSN:0306-4522
1873-7544
DOI:10.1016/S0306-4522(02)00824-2