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The Journal of Neuroscience, October 1, 2003, 23(26):8931-8940

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Behavioral/Systems/Cognitive
Dopaminergic Modulation of Axon Collaterals Interconnecting Spiny Neurons of the Rat Striatum

Jaime N. Guzmán,1 Adán Hernández,2 Elvira Galarraga,1 Dagoberto Tapia,1 Antonio Laville,1 Ramiro Vergara,1 Jorge Aceves,2 and José Bargas1

1Instituto de Fisiología Celular, Universidad Nacional Autonoma de Mexico, Mexico City DF 04510, Mexico, and 2Departamento de Fisiología, Centro de Investigación y de Estudios Avanzados, Mexico City DF 07000, Mexico

Dopamine is a critical modulator of striatal function; its absence produces Parkinson's disease. Most cellular actions of dopamine are still unknown. This work describes the presynaptic actions of dopaminergic receptor agonists on GABAergic transmission between neostriatal projection neurons. Axon collaterals interconnect projection neurons, the main axons of which project to other basal ganglia nuclei. Most if not all of these projecting axons pass through the globus pallidus. Thus, we lesioned the intrinsic neurons of the globus pallidus and stimulated neostriatal efferent axons antidromically with a bipolar electrode located in this nucleus. This maneuver revealed a bicuculline-sensitive synaptic current while recording in spiny cells. D1 receptor agonists facilitated whereas D2 receptor agonists depressed this synaptic current. In contrast, a bicuculline-sensitive synaptic current evoked by field stimulation inside the neostriatum was not consistently modulated, in agreement with previous studies. The data are discussed in light of the most recent experimental and modeling results. The conclusion was that inhibition of spiny cells by axon collaterals of other spiny cells is quantitatively important; however, to be functionally important, this inhibition might be conditioned to the synchronized firing of spiny neurons. Finally, dopamine exerts a potentially important role regulating the extent of lateral inhibition.

Key words: dopamine; neostriatum; basal ganglia; presynaptic modulation; lateral inhibition; GABA

Received March 21, 2003; revised August 6, 2003; accepted August 11, 2003.




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