A descending dopamine pathway conserved from basal vertebrates to mammals
Identifieur interne : 000129 ( Pmc/Curation ); précédent : 000128; suivant : 000130A descending dopamine pathway conserved from basal vertebrates to mammals
Auteurs : Dimitri Ryczko [Canada] ; Jackson J. Cone ; Michael H. Alpert ; Laurent Goetz [Canada] ; François Auclair [Canada] ; Catherine Dubé [Canada] ; Martin Parent [Canada] ; Mitchell F. Roitman ; Simon Alford ; Réjean Dubuc [Canada]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2016.
Abstract
In vertebrates, the contribution of dopamine neurons to locomotor control is traditionally attributed to their ascending projections to the basal ganglia that, in turn, project down to brainstem locomotor networks. We recently discovered in lampreys that brainstem networks receive a direct descending dopaminergic input that increases locomotor output. Here, we show that this descending dopaminergic pathway is conserved in higher vertebrates. We found that dopamine is released in salamander brainstem locomotor networks, together with reticulospinal cell activation, known to trigger locomotion. Dopamine is released in rat brainstem locomotor networks, and amphetamine potentiates dopamine release in vivo. Finally, brainstem locomotor networks in human tissue contain dopaminergic terminals. Our findings have important implications for understanding the locomotor role of dopamine in vertebrates.
Url:
DOI: 10.1073/pnas.1600684113
PubMed: 27071118
PubMed Central: 4855556
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Michael H. Alpert<affiliation><nlm:aff id="aff3">Department of Biological Sciences,<institution>University of Illinois at Chicago</institution>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>In vertebrates, the contribution of dopamine neurons to locomotor control is traditionally attributed to their ascending projections to the basal ganglia that, in turn, project down to brainstem locomotor networks. We recently discovered in lampreys that brainstem networks receive a direct descending dopaminergic input that increases locomotor output. Here, we show that this descending dopaminergic pathway is conserved in higher vertebrates. We found that dopamine is released in salamander brainstem locomotor networks, together with reticulospinal cell activation, known to trigger locomotion. Dopamine is released in rat brainstem locomotor networks, and amphetamine potentiates dopamine release in vivo. Finally, brainstem locomotor networks in human tissue contain dopaminergic terminals. Our findings have important implications for understanding the locomotor role of dopamine in vertebrates.</p>
</div>
</front>
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<title-group><article-title>A descending dopamine pathway conserved from basal vertebrates to mammals</article-title>
<alt-title alt-title-type="short">Conservation of dopaminergic inputs to the MLR</alt-title>
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<contrib-group><contrib contrib-type="author"><name><surname>Ryczko</surname>
<given-names>Dimitri</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
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<contrib contrib-type="author"><name><surname>Cone</surname>
<given-names>Jackson J.</given-names>
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<xref ref-type="aff" rid="aff2"><sup>b</sup>
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<contrib contrib-type="author"><name><surname>Alpert</surname>
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<xref ref-type="aff" rid="aff3"><sup>c</sup>
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<contrib contrib-type="author"><name><surname>Goetz</surname>
<given-names>Laurent</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
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<contrib contrib-type="author"><name><surname>Auclair</surname>
<given-names>François</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dubé</surname>
<given-names>Catherine</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
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<contrib contrib-type="author"><name><surname>Parent</surname>
<given-names>Martin</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
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<contrib contrib-type="author"><name><surname>Roitman</surname>
<given-names>Mitchell F.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
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<contrib contrib-type="author"><name><surname>Alford</surname>
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<xref ref-type="aff" rid="aff3"><sup>c</sup>
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<contrib contrib-type="author"><name><surname>Dubuc</surname>
<given-names>Réjean</given-names>
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<xref ref-type="aff" rid="aff1"><sup>a</sup>
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<aff id="aff1"><sup>a</sup>
Groupe de Recherche sur le Système Nerveux Central, Département de Neurosciences,<institution>Université de Montréal</institution>
, Montreal, QC,<country>Canada</country>
H3C 3J7;</aff>
<aff id="aff2"><sup>b</sup>
Department of Psychology,<institution>University of Illinois</institution>
, Chicago,<addr-line>IL</addr-line>
60607;</aff>
<aff id="aff3"><sup>c</sup>
Department of Biological Sciences,<institution>University of Illinois at Chicago</institution>
,<country>Chicago</country>
,<addr-line>IL</addr-line>
60607;</aff>
<aff id="aff4"><sup>d</sup>
Department of Psychiatry and Neuroscience, Faculty of Medicine, Centre de Recherche de l’Institut Universitaire en Santé Mentale de Québec,<institution>Université Laval</institution>
, Quebec, QC,<country>Canada</country>
G1J 2G3;</aff>
<aff id="aff5"><sup>e</sup>
Département des Sciences de l’Activité Physique,<institution>Université du Québec à Montréal</institution>
, Montreal, QC,<country>Canada</country>
H3C 3P8</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. Email: <email>rejean.dubuc@gmail.com</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Sten Grillner, Karolinska Institute, Stockholm, Sweden, and approved March 15, 2016 (received for review January 14, 2016)</p>
</fn>
<fn fn-type="con"><p>Author contributions: D.R., F.A., and R.D. designed research; D.R., J.J.C., M.H.A., L.G., F.A., and C.D. performed research; D.R., J.J.C., M.H.A., L.G., F.A., C.D., M.P., M.F.R., S.A., and R.D. analyzed data; and D.R., F.A., and R.D. wrote the paper.</p>
</fn>
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<pub-date pub-type="ppub"><day>26</day>
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<abstract abstract-type="executive-summary"><title>Significance</title>
<p>In vertebrates, the contribution of dopamine neurons to locomotor control is traditionally attributed to their ascending projections to the basal ganglia that, in turn, project down to brainstem locomotor networks. We recently discovered in lampreys that brainstem networks receive a direct descending dopaminergic input that increases locomotor output. Here, we show that this descending dopaminergic pathway is conserved in higher vertebrates. We found that dopamine is released in salamander brainstem locomotor networks, together with reticulospinal cell activation, known to trigger locomotion. Dopamine is released in rat brainstem locomotor networks, and amphetamine potentiates dopamine release in vivo. Finally, brainstem locomotor networks in human tissue contain dopaminergic terminals. Our findings have important implications for understanding the locomotor role of dopamine in vertebrates.</p>
</abstract>
<abstract><p>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.</p>
</abstract>
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