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Topography and collateralization of dopaminergic projections to primary motor cortex in rats

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Abstract

Dopaminergic signaling within the primary motor cortex (M1) is necessary for successful motor skill learning. Dopaminergic neurons projecting to M1 are located in the ventral tegmental area (VTA, nucleus A10) of the midbrain. It is unknown which behavioral correlates are encoded by these neurons. The objective here is to investigate whether VTA-M1 fibers are collaterals of projections to prefrontal cortex (PFC) or nucleus accumbens (NAc) or if they form a distinct pathway. In rats, multiple-site retrograde fluorescent tracers were injected into M1, PFC and the core region of the NAc and VTA sections investigated for concomitant labeling of different tracers. Dopaminergic neurons projecting to M1, PFC and NAc were found in nucleus A10 and to a lesser degree in the medial nucleus A9. Neurons show high target specificity, minimal collateral branching to other than their target area and hardly cross the midline. Whereas PFC- and NAc-projecting neurons are indistinguishably intermingled within the ventral portion of dopaminergic nuclei in middle and caudal midbrain, M1-projecting neurons are only located within the dorsal part of the rostral midbrain. Within M1, the forelimb representation receives sevenfold more dopaminergic projections than the hindlimb representation. This strong rostro-caudal gradient as well as the topographical preference to dorsal structures suggest that projections to M1 emerged late in the development of the dopaminergic systems in and form a functionally distinct system.

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Acknowledgments

This study was funded by grants from the Swiss National Foundation (SNF, NCCR Neuro). We thank Clement Osei-Atiemo for his support.

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Correspondence to Andreas R. Luft.

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221_2015_4211_MOESM1_ESM.pdf

Supplementary figure 1. Schematic illustration of injection sites. On schematic drawings of representative brain sections, typical injection sites are indicated: (a) M1 forelimb representation, (b) M1 hindlimb representation, (c) prefrontal cortex and (d) core region of the nucleus accumbens. M1, primary motor cortex; M2, secondary motor cortex; S1, primary sensory cortex; PFC, prefrontal cortex; NAc, core region of the nucleus accumbens. Scale bar: 1 mm (PDF 338 kb)

221_2015_4211_MOESM2_ESM.pdf

Supplementary figure 2. Histological verification of injection sites. (a) Intracortical injection of the retrograde tracer Fast Blue. CC, corpus callosum; M1, primary motor cortex. Scale bar: 0.5 mm. (b) Injection site of the retrograde tracer Micro Ruby in the prefrontal cortex. Fluorescent image of a tracer depot (indicated by arrowhead) is merged with a structural image performed by brightfield microscopy. fmi, forceps minor of the corpus callosum; M1, primary motor cortex; M2, secondary motor cortex; and PFC, prefrontal cortex. Scale bar: 1 mm. (c) Injection side of the retrograde tracer Micro Ruby into the nucleus accumbens. Fluorescent image of a tracer deposit (indicated by arrowhead) is merged with a structural image performed by brightfield microscopy. fmi, forceps minor; CC, corpus callosum; cNA, core region of nucleus accumbens; cPu, caudate putamen; LV, lateral ventricle; and S1, primary sensory cortex. Scale bar: 1 mm (PDF 309577 kb)

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Hosp, J.A., Nolan, H.E. & Luft, A.R. Topography and collateralization of dopaminergic projections to primary motor cortex in rats. Exp Brain Res 233, 1365–1375 (2015). https://doi.org/10.1007/s00221-015-4211-2

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  • DOI: https://doi.org/10.1007/s00221-015-4211-2

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