Abstract
The cerebral cortex and basal ganglia (BG) form a neural circuit that is disrupted in disorders such as Parkinson’s disease. We found that neuronal activity (c-Fos) in the BG followed cortical activity, i.e., high in arousal state and low in sleep state. To determine if cortical activity is necessary for BG activity, we administered atropine to rats to induce a dissociative state resulting in slow-wave electroencephalography but hyperactive motor behaviors. Atropine blocked c-Fos expression in the cortex and BG, despite high c-Fos expression in the sub-cortical arousal neuronal groups and thalamus, indicating that cortical activity is required for BG activation. To identify which glutamate receptors in the BG that mediate cortical inputs, we injected ketamine [N-methyl-d-aspartate (NMDA) receptor antagonist] and 6-cyano-nitroquinoxaline-2, 3-dione (CNQX, a non-NMDA receptor antagonist). Systemic ketamine and CNQX administration revealed that NMDA receptors mediated subthalamic nucleus (STN) input to internal globus pallidus (GPi) and substantia nigra pars reticulata (SNr), while non-NMDA receptor mediated cortical input to the STN. Both types of glutamate receptors were involved in mediating cortical input to the striatum. Dorsal striatal (caudoputamen, CPu) dopamine depletion by 6-hydroxydopamine resulted in reduced activity of the CPu, globus pallidus externa (GPe), and STN but increased activity of the GPi, SNr, and putative layer V neurons in the motor cortex. Our results reveal that the cortical activity is necessary for BG activity and clarifies the pathways and properties of the BG-cortical network and their putative role in the pathophysiology of BG disorders.
Highlights
The cerebral cortex and basal ganglia (BG), two of the largest forebrain structures, form a dynamic interactive network
Compared to the sleep condition, c-Fos expression was significantly higher in the cerebral cortex in AW rats, especially in the prefrontal and frontal, motor, and sensory cortices (Table 1; Figure 1A) and in all the subunits of the BG, i.e., the dorsal striatum, globus pallidus externa (GPe), globus pallidus (GPi), subthalamic nucleus (STN), and substantia nigra pars reticulata (SNr) (Table 1; Figures 1B–F)
Www.frontiersin.org than spontaneous wakefulness (Vetrivelan et al, 2010). These results indicate that BG neural activity is increased when cortical neuronal activity is increased and likewise decreased when cortical activity is decreased, as in the slow-wave EEG state like sleep
Summary
The cerebral cortex and basal ganglia (BG), two of the largest forebrain structures, form a dynamic interactive network. The BG in turn, with modulation from midbrain dopaminergic system, integrates and processes this cortical information for output, back to the cerebral cortex to shape cortical activity and affect cortical functions such as motor behavior (Yelnik, 2008) This reciprocal regulation is significantly altered after BG dysfunction, as in neurological disorders such as Parkinson’s disease and Huntington’s disease. The glutamatergic subthalamic nucleus (STN) receives cortical inputs (hyper-direct pathway) and in turn projects primarily to the GPe, GPi, and SNr. Midbrain dopaminergic neurons provide the major subcortical input to the BG, especially the striatum. Midbrain dopaminergic neurons provide the major subcortical input to the BG, especially the striatum These projections form the core of the classical model of BG organization that influences current thinking about BG function and dysfunction, as in Parkinson’s and Huntington’s disease
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