Evolutionarily conserved organization of the dopaminergic system in lamprey: <scp>SN</scp>c/<scp>VTA</scp> afferent and efferent connectivity and <scp>D</scp>2 receptor expression

Pérez‐Fernández, Juan; Stephenson-Jones, Marcus; Suryanarayana, Shreyas M.; Robertson, Brita; Grillner, Sten

doi:10.1002/cne.23639

Cited by 81 publications

(113 citation statements)

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“…In lamprey (Ryczko et al, 2013) and salamander (Ryczko et al, 2016a), dopaminergic fibers were found around MLR cholinergic cells, a conserved landmark of the MLR (see Ryczko and Dubuc, 2013). We identified the origin of this dopaminergic innervation in lamprey (Figure 2G, Ryczko et al, 2013; see also Perez-Fernandez et al, 2014) and in salamander (Figure 2H, Ryczko et al, 2016a) as a diencephalic dopaminergic region called the posterior tuberculum. This region sends ascending projection to the striatum, and is considered homologous to the mammalian SNc and/or ventral tegmental area (Marin et al, 1997; Pombal et al, 1997; Puelles and Verney, 1998; Smeets et al, 2000; Rink and Wullimann, 2001; Blin et al, 2008; for review see Yamamoto and Vernier, 2011; Wullimann, 2014).…”

Section: A New Descending Dopaminergic Pathway Has Been Unraveledmentioning

confidence: 81%

“…The multiple alterations in the MLR in PD are compatible with such phenomenon (see Fornito et al, 2015). The reciprocal projections between the SNc and the PPN (McGeer and McGeer, 1984; Lavoie and Parent, 1994; Ryczko et al, 2013, 2016a; Perez-Fernandez et al, 2014) could also contribute to potentiate the transneuronal degeneration process. Nigral dopamine cell degeneration would cause a loss of the dopaminergic input to the MLR, causing MLR cells to degenerate.…”

Section: Possible Role Of the Descending Dopaminergic Pathway In Pdmentioning

confidence: 99%

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Dopamine and the Brainstem Locomotor Networks: From Lamprey to Human

2017

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In vertebrates, dopamine neurons are classically known to modulate locomotion via their ascending projections to the basal ganglia that project to brainstem locomotor networks. An increased dopaminergic tone is associated with increase in locomotor activity. In pathological conditions where dopamine cells are lost, such as in Parkinson's disease, locomotor deficits are traditionally associated with the reduced ascending dopaminergic input to the basal ganglia. However, a descending dopaminergic pathway originating from the substantia nigra pars compacta was recently discovered. It innervates the mesencephalic locomotor region (MLR) from basal vertebrates to mammals. This pathway was shown to increase locomotor output in lampreys, and could very well play an important role in mammals. Here, we provide a detailed account on the newly found dopaminergic pathway in lamprey, salamander, rat, monkey, and human. In lampreys and salamanders, dopamine release in the MLR is associated with the activation of reticulospinal neurons that carry the locomotor command to the spinal cord. Dopamine release in the MLR potentiates locomotor movements through a D1-receptor mechanism in lampreys. In rats, stimulation of the substantia nigra pars compacta elicited dopamine release in the pedunculopontine nucleus, a known part of the MLR. In a monkey model of Parkinson's disease, a reduced dopaminergic innervation of the brainstem locomotor networks was reported. Dopaminergic fibers are also present in human pedunculopontine nucleus. We discuss the conserved locomotor role of this pathway from lamprey to mammals, and the hypothesis that this pathway could play a role in the locomotor deficits reported in Parkinson's disease.

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Section: A New Descending Dopaminergic Pathway Has Been Unraveledmentioning

confidence: 81%

Section: Possible Role Of the Descending Dopaminergic Pathway In Pdmentioning

confidence: 99%

Dopamine and the Brainstem Locomotor Networks: From Lamprey to Human

2017

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“…To what extent the basal ganglia influence processing in tectum by disinhibition of local GABAergic neurons is as yet not clear. There is also in lamprey a dopaminergic projection from the substantia nigra pars compacta, which will potentiate (via dopamine D 1 receptor) or suppress (via dopamine D 2 receptor) the responses of the tectal output neurons (62,63). Finally, there is cholinergic input from the parabigeminal nucleus (isthmic nucleus in nonmammals) that can modulate the visuomotor pathway through projections to the superficial layer (59,64).…”

Section: Discussionmentioning

confidence: 99%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

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

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132

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The optic tectum (called superior colliculus in mammals) is critical for eye-head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex-yet phylogenetically conservedsensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gazecontrolling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution.optic tectum | superior colliculus | GABAergic inhibition | gaze control | evolution V isual scenes are composed of abundant stimuli, and the gaze needs continuously to be redirected toward different objectsan important task for the brain. Current models postulate that stimulus selection occurs through a process involving competitive interaction between different visual stimuli, resulting in the appropriate eye-head movement (1-5). The optic tectum (superior colliculus in mammals) has a causal role in the stimulus selection process (6-12) and not only in the control of saccades and eyehead gaze shifts (13-16). Although the collicular contribution to the selection process is of central importance, the underlying neuronal processes have remained elusive due to methodological limitations. It is our aim here to address this issue in a novel experimental model.The optic tectum is well developed in the lamprey, belonging to the oldest extant vertebrate group that evolved 560 million years ago (17), and it has remained conserved throughout vertebrate phylogeny (18)(19)(20)(21)(22). Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23-26). The intermediate and deep layers give rise to projections to brainstem areas and a motor map is formed that is responsible for the coordination of eye, head, and body movements (22,(27)(28)(29).To uncover the mechanisms underlying visual stimulus selection for gaz...

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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: 87%

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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Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression

Cited by 81 publications

References 91 publications

Dopamine and the Brainstem Locomotor Networks: From Lamprey to Human

Dopamine and the Brainstem Locomotor Networks: From Lamprey to Human

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

A descending dopamine pathway conserved from basal vertebrates to mammals

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