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Individual Dopaminergic Neurons of Lamprey SNc/VTA Project to Both the Striatum and Optic Tectum, But Restrict Co-Release of Glutamate to Striatum Only

34 Pages Posted: 10 Sep 2018 Publication Status: Review Complete

See all articles by Arndt von Twickel

Arndt von Twickel

University of Cologne - Biocenter Cologne

Daniel Kowatschew

University of Cologne - Institute for Genetics

Mehmet Saltürk

University of Cologne - Institute for Genetics

Maria Schauer

University of Cologne - Biocenter Cologne

Brita Robertson

Karolinska Institutet - The Nobel Institute for Neurophysiology

Sigrun Korsching

University of Cologne - Institute for Genetics

Wolfgang Walkowiak

University of Cologne - Biocenter Cologne

Sten Grillner

Karolinska Institutet - The Nobel Institute for Neurophysiology

Juan Pérez-Fernández

Karolinska Institutet - The Nobel Institute for Neurophysiology

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Abstract

Dopaminergic neurons in the substantia nigra (SNc) innervate both striatum and the superior colliculus in mammals, as well as lampreys, belonging to the oldest group of living vertebrates. In the lamprey, we have previously shown that the same neuron sends axonal branches to both striatum and the superior colliculus, the optic tectum in lower vertebrates. Here, we show that most SNc neurons in lamprey express not only tyrosine hydroxylase (TH) as an indicator of dopamine, but also the vesicular glutamate transporter (vGluT), suggesting that glutamate is a co-transmitter. Remarkably, the axonal branches that project to striatum elicit both dopaminergic and glutamatergic synaptic effects on striatal neurons, whereas the axonal projections to the optic tectum only evoke dopaminergic effects. Thus, axonal branches from the same neuron can use two transmitters in one branch and only one in the other.Previous studies suggest that along an individual dopaminergic axon there can be microdomains of either TH or vGluT. In contrast, the present results demonstrate that entire axonal branches to one target structure can differ from that of branches to another target, both originating from the same dopamine neuron. This implies that a given dopamine neuron can exert different effects on two different target structures. The combined release of dopamine and glutamate may be appropriate in striatum, whereas the effects exerted on the tectal motor center may be better served with a selective dopaminergic modulation.

Suggested Citation

Twickel, Arndt von and Kowatschew, Daniel and Saltürk, Mehmet and Schauer, Maria and Robertson, Brita and Korsching, Sigrun and Walkowiak, Wolfgang and Grillner, Sten and Pérez-Fernández, Juan, Individual Dopaminergic Neurons of Lamprey SNc/VTA Project to Both the Striatum and Optic Tectum, But Restrict Co-Release of Glutamate to Striatum Only (September 6, 2018). Available at SSRN: https://ssrn.com/abstract=3245527 or http://dx.doi.org/10.2139/ssrn.3245527
This version of the paper has not been formally peer reviewed.

Arndt von Twickel (Contact Author)

University of Cologne - Biocenter Cologne

Albertus-Magnus-Platz
Cologne, 50923
Germany

Daniel Kowatschew

University of Cologne - Institute for Genetics

Albertus-Magnus-Platz
Cologne, 50923
Germany

Mehmet Saltürk

University of Cologne - Institute for Genetics

Albertus-Magnus-Platz
Cologne, 50923
Germany

Maria Schauer

University of Cologne - Biocenter Cologne

Albertus-Magnus-Platz
Cologne, 50923
Germany

Brita Robertson

Karolinska Institutet - The Nobel Institute for Neurophysiology

Granits väg 4
SE-171 77 Stockholm, Stockholm 17171
Sweden

Sigrun Korsching

University of Cologne - Institute for Genetics

Albertus-Magnus-Platz
Cologne, 50923
Germany

Wolfgang Walkowiak

University of Cologne - Biocenter Cologne

Albertus-Magnus-Platz
Cologne, 50923
Germany

Sten Grillner

Karolinska Institutet - The Nobel Institute for Neurophysiology ( email )

Granits väg 4
SE-171 77 Stockholm, Stockholm 17171
Sweden

Juan Pérez-Fernández

Karolinska Institutet - The Nobel Institute for Neurophysiology

Granits väg 4
SE-171 77 Stockholm, Stockholm 17171
Sweden

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