Descending brain‐spinal cord projections in a primitive vertebrate, the lamprey: Cerebrospinal fluid‐contacting and dopaminergic neurons

Barreiro‐Iglesias, Antón; Villar-Cerviño, Verona; Anadón, Ramón; Rodicio, Marı́a Celina

doi:10.1002/cne.21863

Cited by 36 publications

(44 citation statements)

References 91 publications

(72 reference statements)

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“…the dopaminergic innervation of the MLR. In lampreys, the diencephalic DA neurons projecting to the spinal cord, which may correspond to the A11 group, are periventricular cells of the mammillary area (41) and are distinct from those projecting to the MLR and striatum (22). In rats, we did not find cells labeled in A11 following tracer or virus injection in the MLR.…”

Section: Discussioncontrasting

confidence: 54%

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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Section: Discussioncontrasting

confidence: 54%

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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“…The origin of these neurons varies between non-mammalian classes of vertebrates, but the descending projections most commonly arise from a homologue of the paraventricular nucleus and at least one cell group in the ventral thalamus (Smeets and Timerick 1981;Berk and Finkelstein 1983;Prasada Rao et al 1987;Masino and Knudsen 1992;Rao et al 1993;New et al 1998;Cruce et al 1999;Sanchez-Camacho et al2002;Barreiro-Iglesias et al 2008). In common with a number of studies in mammals (Basbaum and Fields 1979;Sawchenko and Swanson 1982;Leong et al 1984;Holstege 1987a;Masson et al 1991;Hallbeck and Blomqvist 1999;Hallbeck 2000;Kc et al 2002), we found labeled neurons in the ipsilateral paraventricular hypothalamus, the medial part of ZID, and in LH and PH.…”

Section: Hypothalamic and Diencephalic Areasmentioning

confidence: 99%

Projections from the brain to the spinal cord in the mouse

2010

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The cells that project from the brain to the spinal cord have previously been mapped in a wide range of mammalian species, but have not been comprehensively studied in the mouse. We have mapped these cells in the mouse using retrograde tracing after large unilateral Fluoro-Gold (FG) and horseradish peroxidase (HRP) injections in the C1 and C2 spinal cord segments. We have identified over 30 cell groups that project to the spinal cord, and have confirmed that the pattern of major projections from the cortex, diencephalon, midbrain, and hindbrain in the mouse is typically mammalian, and very similar to that found in the rat. However, we report two novel findings: we found labeled neurons in the precuneiform area (an area which has been associated with the midbrain locomotor center in other species), and the epirubrospinal nucleus. We also found labeled cells in the medial division of central nucleus of the amygdala in a small number of cases. Our findings should be of value to researchers engaged in evaluating the impact of spinal cord injury and other spinal cord pathologies on the centers which give rise to descending pathways.

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“…This antibody recognizes a protein of 59 -61 kDa by Western blot and does not crossreact with dopamine-hydroxylase, phenylalanine hydroxylase, tryptophan hydroxylase, or phenyl ethanolamine-N-methyl transferase on Western blots (Chemicon specification sheet). It has been shown that there is extensive species homology for the TH molecule and this antibody has been used to analyze the catecholaminergic systems in many vertebrate classes, including amphibians (González and Smeets, 1991;Sanchez-González et al, 2005;Barreiro-Iglesias et al, 2008).…”

Section: Immunohistochemistrymentioning

confidence: 99%

Neuroprotection of midbrain dopaminergic cells in MPTP‐treated mice after near‐infrared light treatment

Shaw

Spana

Ashkan

et al. 2009

J of Comparative Neurology

126

121

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This study explores whether near-infrared (NIr) light treatment neuroprotects dopaminergic cells in the substantia nigra pars compacta (SNc) and the zona incerta-hypothalamus (ZI-Hyp) from degeneration in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. BALB/c albino mice were divided into four groups: 1) Saline, 2) Saline-NIr, 3) MPTP, 4) MPTP-NIr. The injections were intraperitoneal and they were followed immediately by NIr light treatment (or not). Two doses of MPTP, mild (50 mg/kg) and strong (100 mg/kg), were used. Mice were perfused transcardially with aldehyde fixative 6 days after their MPTP treatment. Brains were processed for tyrosine hydroxylase (TH) immunochemistry. The number of TH(+) cells was estimated using the optical fractionator method. Our major finding was that in the SNc there were significantly more dopaminergic cells in the MPTP-NIr compared to the MPTP group (35%-45%). By contrast, in the ZI-Hyp there was no significant difference in the numbers of cells in these two groups. In addition, our results indicated that survival in the two regions after MPTP insult was dose-dependent. In the stronger MPTP regime, the magnitude of loss was similar in the two regions ( approximately 60%), while in the milder regime cell loss was greater in the SNc (45%) than ZI-Hyp ( approximately 30%). In summary, our results indicate that NIr light treatment offers neuroprotection against MPTP toxicity for dopaminergic cells in the SNc, but not in the ZI-Hyp.

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Descending brain‐spinal cord projections in a primitive vertebrate, the lamprey: Cerebrospinal fluid‐contacting and dopaminergic neurons

Cited by 36 publications

References 91 publications

A descending dopamine pathway conserved from basal vertebrates to mammals

A descending dopamine pathway conserved from basal vertebrates to mammals

Projections from the brain to the spinal cord in the mouse

Neuroprotection of midbrain dopaminergic cells in MPTP‐treated mice after near‐infrared light treatment

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