Afferents of the lamprey striatum with special reference to the dopaminergic system: A combined tracing and immunohistochemical study

Pombal, Manuel A.; Manira, Abdeljabbar El; Grillner, Sten

doi:10.1002/(sici)1096-9861(19970915)386:1<71::aid-cne8>3.0.co;2-a

Cited by 111 publications

(111 citation statements)

References 63 publications

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“…In lampreys, only a few meso-diencephalic DA neurons send ascending projections to the striatum (9,22); the majority of DA neurons send a direct descending projection to the MLR (22,23), where DA is released and increases locomotor output through D1 receptors (22). These results demonstrate that the descending dopaminergic pathway to the MLR is an important modulator of locomotor output, but it remains to be determined whether this pathway is conserved in higher vertebrates.…”

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confidence: 86%

A descending dopamine pathway conserved from basal vertebrates to mammals

Ryczko

Cone

Alpert

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

104

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Dopamine neurons are classically known to modulate locomotion indirectly through ascending projections to the basal ganglia that project down to brainstem locomotor networks. Their loss in Parkinson's disease is devastating. In lampreys, we recently showed that brainstem networks also receive direct descending dopaminergic inputs that potentiate locomotor output. Here, we provide evidence that this descending dopaminergic pathway is conserved to higher vertebrates, including mammals. In salamanders, dopamine neurons projecting to the striatum or brainstem locomotor networks were partly intermingled. Stimulation of the dopaminergic region evoked dopamine release in brainstem locomotor networks and concurrent reticulospinal activity. In rats, some dopamine neurons projecting to the striatum also innervated the pedunculopontine nucleus, a known locomotor center, and stimulation of the dopaminergic region evoked pedunculopontine dopamine release in vivo. Finally, we found dopaminergic fibers in the human pedunculopontine nucleus. The conservation of a descending dopaminergic pathway across vertebrates warrants re-evaluating dopamine's role in locomotion.D opaminergic neurons represent a vital neuromodulatory component essential for vertebrate motor control, and their loss in neurodegenerative disease is devastating. The meso-diencephalic dopamine (DA) neurons are known to provide ascending projections to the basal ganglia, which, in turn, provide input to cortical structure in mammals but also project caudally to the mesencephalic locomotor region (MLR), a highly conserved structure that controls locomotion in all vertebrates investigated to date (1-7; for review, see ref. 8). A growing body of evidence supports the view that basal ganglia connectivity is highly conserved among vertebrates, from lampreys to mammals (9-11; for review, see ref. 12), with some interspecies differences recently highlighted (13). As such, the homology between DA cell populations remains to be resolved in vertebrates. As a general rule, DA neurons from the meso-diencephalon send projections to the striatum in all vertebrates. In lampreys and teleosts, those neurons are located only in the diencephalon (posterior tuberculum), but in tetrapods and cartilaginous fishes (14) they are located in both the diencephalon and the mesencephalon. An increasing number of authors seem to agree with the hypothesis that at least some of the mesodiencephalic DA neurons located in the diencephalon are homologous in all vertebrates, and thus, homologous to at least a portion of the mammalian substantia nigra pars compacta (SNc)/ ventral tegmental area (VTA) (13, 15-19; for review, see ref. 20). Alternatively, it was suggested that the posterior tuberculum DA neurons projecting to the striatum in zebrafish are homologs of the mammalian DA neurons of the A11 group (21). This will be discussed below in light of the results of the present study.In lampreys, only a few meso-diencephalic DA neurons send ascending projections to the striatum (9, 22); the majority ...

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mentioning

confidence: 86%

A descending dopamine pathway conserved from basal vertebrates to mammals

Ryczko

Cone

Alpert

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

104

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“…Parkinson disease) conditions. TH immunofluorescence (3). The rostrocaudal extent of the population in spawning phase animals is around 500 μm, spreading approximately 100 to 300 μm from the midline (Fig.…”

Section: Significancementioning

confidence: 98%

“…4). In lampreys, the PT is considered homologous to the SNc and/or VTA of mammals because of its DA projection to the striatum (3). Further, we determined a role for this DA pathway in the control of locomotion.…”

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confidence: 99%

Forebrain dopamine neurons project down to a brainstem region controlling locomotion

Ryczko

Grätsch

Auclair

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The contribution of dopamine (DA) to locomotor control is traditionally attributed to ascending dopaminergic projections from the substantia nigra pars compacta and the ventral tegmental area to the basal ganglia, which in turn project down to the mesencephalic locomotor region (MLR), a brainstem region controlling locomotion in vertebrates. However, a dopaminergic innervation of the pedunculopontine nucleus, considered part of the MLR, was recently identified in the monkey. The origin and role of this dopaminergic input are unknown. We addressed these questions in a basal vertebrate, the lamprey. Here we report a functional descending dopaminergic pathway from the posterior tuberculum (PT; homologous to the substantia nigra pars compacta and/or ventral tegmental area of mammals) to the MLR. By using triple labeling, we found that dopaminergic cells from the PT not only project an ascending pathway to the striatum, but send a descending projection to the MLR. In an isolated brain preparation, PT stimulation elicited excitatory synaptic inputs into patch-clamped MLR cells, accompanied by activity in reticulospinal cells. By using voltammetry coupled with electrophysiological recordings, we demonstrate that PT stimulation evoked DA release in the MLR, together with the activation of reticulospinal cells. In a semi-intact preparation, stimulation of the PT elicited reticulospinal activity together with locomotor movements. Microinjections of a D1 antagonist in the MLR decreased the locomotor output elicited by PT stimulation, whereas injection of DA had an opposite effect. It appears that this descending dopaminergic pathway has a modulatory role on MLR cells that are known to receive glutamatergic projections and promotes locomotor output.motor system | Parkinson disease D opamine (DA) neurons of the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA) modulate motor behaviors, including locomotion, through ascending projections to the basal ganglia, the output of which projects to the mesencephalic locomotor region (MLR) (1-3), a brainstem region known to control locomotion in all vertebrate species tested to date (reviewed in ref. 4). DA is known to control the excitability of striatal cells, and a dysfunction of the ascending DA pathway to the striatum is considered to be the main cause for the motor deficits in Parkinson disease (1). However, there have been hints of descending DA projections that would be in position to directly modulate the MLR and hence locomotor activity. In monkeys, DA terminals of unknown origin were observed in the pedunculopontine nucleus (PPN) (5), considered part of the MLR (reviewed in ref. 4). In addition, there is an axonal projection from the SNc to the PPN in rats, but the transmitter system is unknown (6).We examined the DA system in a basal vertebrate, the lamprey, and found a previously unknown descending DA pathway from the posterior tuberculum (PT) to the MLR, which comprises the PPN and the laterodorsal tegmental nucleus (LDT) in lampreys (ref. 7; reviewed...

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“…In mammals, cholinergic as well as parvalbumin-and somatostatin-expressing GABAergic interneurons express dopamine receptors (Yan and Surmeier, 1997;Yan et al, 1997, Centonze et al, 2002, 2003 and contribute to the regulation of the direct and indirect projecting SPNs (Gerfen and Surmeier 2011). Cholinergic neurons have also been observed in the lamprey striatum (Pombal et al, 2001), as have neurons with the physiological hallmarks of fast-spiking parvalbumin-expressing neurons . Whether these interneurons also express dopamine receptors and contribute to the excitability differences we observe in lamprey remains to be determined.…”

Section: Dopamine Receptor Expression In Striatal Projection Neuronsmentioning

confidence: 99%

“…Elements of this neuromodulatory organization may be conserved, because the striatum of non-mammalian vertebrates (lamprey, amphibians, reptiles, and birds) also receives a large dopaminergic projection from the homolog of the SNc/VTA and express D 1 and D 2 receptors (Reiner et al, 1998;Chu et al, 2001;Pombal et al, 2007;Robertson et al, 2012). Furthermore, in turtles and birds, dopamine excites striatal neurons that express D 1 receptors and inhibits neurons that express D 2 receptors (Ding and Perkel, 2002;Barral et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Dopamine Differentially Modulates the Excitability of Striatal Neurons of the Direct and Indirect Pathways in Lamprey

et al. 2013

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The functions of the basal ganglia are critically dependent on dopamine. In mammals, dopamine differentially modulates the excitability of the direct and indirect striatal projection neurons, and these populations selectively express dopamine D 1 and D 2 receptors, respectively. Although the detailed organization of the basal ganglia is conserved throughout the vertebrate phylum, it was unknown whether the differential dopamine modulation of the direct and indirect pathways is present in non-mammalian species. We aim here to determine whether the receptor expression and opposing dopaminergic modulation of the direct and indirect pathways is present in one of the phylogenetically oldest vertebrates, the river lamprey. Using in situ hybridization and patch-clamp recordings, we show that D 1 receptors are almost exclusively expressed in the striatal neurons projecting directly to the homolog of the substantia nigra pars reticulata. In addition, the majority of striatal neurons projecting to the homolog of the globus pallidus interna/globus pallidus externa express D 1 or D 2 receptors. As in mammals, application of dopamine receptor agonists differentially modulates the excitability of these neurons, increasing the excitability of the D 1 -expressing neurons and decreasing the excitability of D 2 -expressing neurons. Our results suggest that the segregated expression of the D 1 and D 2 receptors in the direct and indirect striatal projection neurons has been conserved across the vertebrate phylum. Because dopamine receptor agonists differentially modulate these pathways, increasing the excitability of the direct pathway and decreasing the excitability of the indirect pathway, this organization may be conserved as a mechanism that biases the networks toward action selection.

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Afferents of the lamprey striatum with special reference to the dopaminergic system: A combined tracing and immunohistochemical study

Cited by 111 publications

References 63 publications

A descending dopamine pathway conserved from basal vertebrates to mammals

A descending dopamine pathway conserved from basal vertebrates to mammals

Forebrain dopamine neurons project down to a brainstem region controlling locomotion

Dopamine Differentially Modulates the Excitability of Striatal Neurons of the Direct and Indirect Pathways in Lamprey

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