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The Journal of Neuroscience, September 22, 2004, 24(38):8289-8299; doi:10.1523/JNEUROSCI.1990-04.2004

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Behavioral/Systems/Cognitive
Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

Wanlong Lei, Yun Jiao, Nobel Del Mar, and Anton Reiner

Department of Anatomy and Neurobiology, College of Medicine, The University of Tennessee Health Science Center, Memphis, Tennessee 38163

The two main types of corticostriatal neurons are those that project only intratelencephalically (IT-type), the intrastriatal terminals of which are 0.41 µm in mean diameter, and those that send their main axon into pyramidal tract and have a collateral projection to striatum (PT-type), the intrastriatal terminals of which are 0.82 µm in mean diameter. We used three approaches to examine whether the two striatal projection neuron types (striatonigral direct pathway vs striatopallidal indirect pathway) differ in their input from IT-type and PT-type neurons. First, we retrogradely labeled one striatal projection neuron type or the other with biotinylated dextran amine (BDA)-3000 molecular weight. We found that terminals making asymmetric axospinous contact with striatonigral neurons were 0.43 µm in mean diameter, whereas those making asymmetric axospinous contact with striatopallidal neurons were 0.69 µm. Second, we preferentially immunolabeled striatonigral neurons for D₁ dopamine receptors or striatopallidal neurons for D₂ dopamine receptors and found that axospinous terminals had a smaller mean size (0.45 µm) on D₁+ spines than on D₂+ spines (0.61 µm). Finally, we combined selective BDA labeling of IT-type or PT-type terminals with immunolabeling for D₁ or D₂, and found that IT-type terminals were twice as common as PT-type on D₁+ spines, whereas PT-type terminals were four times as common as IT-type on D₂+ spines. These various results suggest that striatonigral neurons preferentially receive input from IT-type cortical neurons, whereas striatopallidal neurons receive greater input from PT-type cortical neurons. This differential cortical connectivity may further the roles of the direct and indirect pathways in promoting desired movements and suppressing unwanted movements, respectively.

Key words: basal ganglia; cortex; corticostriatal; direct pathway; indirect pathway; striatum

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Received May 21, 2004; revised August 11, 2004; accepted August 11, 2004.

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