Mesencephalic dopamine neurons interfacing the shell of nucleus accumbens and the dorsolateral striatum in the rat

Floris G Wouterlood, Angela Engel, Mariah Daal, Gertjan Houwen, Aileen Meinderts, Tomàs Jordà Siquier, Jeroen A M Beliën, Yvette C van Dongen, Jørgen Scheel-Krüger, Anne-Marie Thierry, Henk J Groenewegen, Jean-Michel Deniau

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Parallel corticostriatonigral circuits have been proposed that separately process motor, cognitive, and emotional-motivational information. Functional integration requires that interactions exist between neurons participating in these circuits. This makes it imperative to study the complex anatomical substrate underlying corticostriatonigral circuits. It has previously been proposed that dopaminergic neurons in the ventral mesencephalon may play a role in this circuit interaction. Therefore, we studied in rats convergence of basal ganglia circuits by depositing an anterograde neuroanatomical tracer into the ventral striatum together with a retrograde fluorescent tracer ipsilaterally in the dorsolateral striatum. In the mesencephalon, using confocal microscopy, we looked for possible appositions of anterogradely labeled fibers and retrogradely labeled neurons, "enhancing" the latter via intracellular injection of Lucifer Yellow. Tyrosine hydroxylase (TH) immunofluorescence served to identify dopaminergic neurons. In neurophysiological experiments, we combined orthodromic stimulation in the medial ventral striatum with recording from ventral mesencephalic neurons characterized by antidromic stimulation from the dorsal striatum. We observed terminal fields of anterogradely labeled fibers that overlap populations of retrogradely labeled nigrostriatal cell bodies in the substantia nigra pars compacta and lateral ventral tegmental area (VTA), with numerous close appositions between boutons of anterogradely labeled fibers and nigrostriatal, TH-immunopositive neurons. Neurophysiological stimulation in the medial ventral striatum caused inhibition of dopaminergic nigrostriatal neurons projecting to the ventrolateral striatal territory. Responding nigrostriatal neurons were located in the medial substantia nigra and adjacent VTA. Our results strongly suggest a functional link between ventromedial, emotional-motivational striatum, and the sensorimotor dorsal striatum via dopaminergic nigrostriatal neurons.

Original languageEnglish
Pages (from-to)1518-1542
Number of pages25
JournalJournal of Neuroscience Research
Volume96
Issue number9
DOIs
Publication statusPublished - Sep 2018

Cite this

Wouterlood, F. G., Engel, A., Daal, M., Houwen, G., Meinderts, A., Jordà Siquier, T., ... Deniau, J-M. (2018). Mesencephalic dopamine neurons interfacing the shell of nucleus accumbens and the dorsolateral striatum in the rat. Journal of Neuroscience Research, 96(9), 1518-1542. https://doi.org/10.1002/jnr.24242