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The Journal of Neuroscience, June 15, 1998, 18(12):4588-4602
Dopamine Neurons Make Glutamatergic Synapses In Vitro
David Sulzer1, 2, 5, Myra P. Joyce1, 5, Ling Lin1, 5, Daron Geldwert1, 5, Suzanne N. Haber6, Toshiaki Hattori7, and Stephen Rayport1, 3, 4, 5 Departments of 1 Psychiatry, 2 Neurology, and 3 Anatomy and Cell Biology and 4 Center for Neurobiology and Behavior, Columbia University, New York, New York 10032, 5 Department of Neuroscience, New York State Psychiatric Institute, New York, New York 10032, 6 Department of Neurobiology and Anatomy, University of Rochester, Rochester, New York 14642, and 7 Department of Anatomy and Cell Biology, University of Toronto, Toronto, Ontario, Canada M5S 1A8
Interactions between dopamine and glutamate play prominent roles in memory, addiction, and schizophrenia. Several lines of evidence have suggested that the ventral midbrain dopamine neurons that give rise to the major CNS dopaminergic projections may also be glutamatergic. To examine this possibility, we double immunostained ventral midbrain sections from rat and monkey for the dopamine-synthetic enzyme tyrosine hydroxylase and for glutamate; we found that most dopamine neurons immunostained for glutamate, both in rat and monkey. We then used postnatal cell culture to examine individual dopamine neurons. Again, most dopamine neurons immunostained for glutamate; they were also immunoreactive for phosphate-activated glutaminase, the major source of neurotransmitter glutamate. Inhibition of glutaminase reduced glutamate staining. In single-cell microculture, dopamine neurons gave rise to varicosities immunoreactive for both tyrosine hydroxylase and glutamate and others immunoreactive mainly for glutamate, which were found near the cell body. At the ultrastructural level, dopamine neurons formed occasional dopaminergic varicosities with symmetric synaptic specializations, but they more commonly formed nondopaminergic varicosities with asymmetric synaptic specializations. Stimulation of individual dopamine neurons evoked a fast glutamatergic autaptic EPSC that showed presynaptic inhibition caused by concomitant dopamine release. Thus, dopamine neurons may exert rapid synaptic actions via their glutamatergic synapses and slower modulatory actions via their dopaminergic synapses. Together with evidence for glutamate cotransmission in serotonergic raphe neurons and noradrenergic locus coeruleus neurons, the present results suggest that glutamatergic cotransmission may be the rule for central monoaminergic neurons.
Key words: glutamate; cotransmission; mesolimbic; nigrostriatal; cell culture; ventral tegmental area
Copyright © 1998 Society for Neuroscience 0270-6474/98/18124588-15$05.00/0
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