The Transformation of a Unilateral Locomotor Command into a Symmetrical Bilateral Activation in the Brainstem

Brocard, Frédéric; Ryczko, Dimitri; Fénelon, Karine; Hatem, Raja; Gonzales, Delphine; Auclair, François; Dubuc, Réjean

doi:10.1523/jneurosci.3433-09.2010

Cited by 66 publications

(105 citation statements)

References 29 publications

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“…Based on previous studies (4,7,50,80), the reticulospinal (RS) neurons were retrogradely labeled with the calcium (Ca 2+ ) indicator Ca 2+ green-dextran amines (MW 3000, Invitrogen C-6765) injected as crystals at the level of the first spinal segment, immediately after a complete transection. The preparation was then transferred for 18-24 h in a chamber perfused with cooled (8-10°C), oxygenated Ringer's solution to allow the tracer to migrate to fill the RS cell bodies.…”

Section: Methodsmentioning

confidence: 99%

“…D-Glutamate (Sigma-Aldrich G1001, 5 mM in Ringer's solution) was microinjected locally in the PT of salamanders through a glass micropipette (tip diameter 4-6 μm) by applying trains (10 s, 2 Hz) of pressure pulses (5-20 psi) of various durations (50-200 ms) with a Picospritzer (Parker Hannifin) (e.g., refs. 4,7,22,84). Fast green was added to the solution for visualizing the injection site (e.g., refs.…”

Section: Methodsmentioning

confidence: 99%

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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: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

A descending dopamine pathway conserved from basal vertebrates to mammals

Ryczko

Cone

Alpert

et al. 2016

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

104

View full text Add to dashboard Cite

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“…We used 13 larval animals for these experiments. The procedure was as described elsewhere (10,35,36). To expose the brain and the rostral segments of the spinal cord, skin, muscles, and surrounding tissues were removed from the rostral part of the animal, down to the caudal gills.…”

Section: Methodsmentioning

confidence: 99%

“…Locomotor movements of body were recorded (30 frames per second) by a video camera (HDR-XR200; Sony) positioned 1 m above the recording chamber. Locomotor movements were tracked and analyzed by using custom written scripts in Matlab (MathWorks) previously used in our laboratory (11,35). Briefly, tracking markers were equidistantly distributed along the midline of the body by using geometrical analysis of the body.…”

Section: Methodsmentioning

confidence: 99%

“…Briefly, tracking markers were equidistantly distributed along the midline of the body by using geometrical analysis of the body. Swimming movements were monitored frame-byframe through local measurement of the angle between the longitudinal axis of nonmoving parts of the body and the line drawn by two successive markers (35). The local curvature angles were determined throughout the whole body.…”

Section: Methodsmentioning

confidence: 99%

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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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Bilateral connectivity in the brainstem respiratory networks of lampreys

Gariépy

Missaghi

Chartré

et al. 2012

J of Comparative Neurology

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This study examines the connectivity in the neural networks controlling respiration in the lampreys, a basal vertebrate. Previous studies have shown that the lamprey paratrigeminal respiratory group (pTRG) plays a crucial role in the generation of respiration. By using a combination of anatomical and physiological techniques, we characterized the bilateral connections between the pTRGs and descending projections to the motoneurons. Tracers were injected in the respiratory motoneuron pools to identify pre-motor respiratory interneurons. Retrogradely labeled cell bodies were found in the pTRG on both sides. Whole-cell recordings of the retrogradely labeled pTRG neurons showed rhythmical excitatory currents in tune with respiratory motoneuron activity. This confirmed that they were related to respiration. Intracellular labeling of individual pTRG neurons revealed axonal branches to the contralateral pTRG and bilateral projections to the respiratory motoneuronal columns. Stimulation of the pTRG induced excitatory postsynaptic potentials in ipsi- and contralateral respiratory motoneurons as well as in contralateral pTRG neurons. A lidocaine HCl (Xylocaine) injection on the midline at the rostrocaudal level of the pTRG diminished the contralateral motoneuronal EPSPs as well as a local injection of 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and (2R)-amino-5-phosphonovaleric acid (AP-5) on the recorded respiratory motoneuron. Our data show that neurons in the pTRG send two sets of axonal projections: one to the contralateral pTRG and another to activate respiratory motoneurons on both sides through glutamatergic synapses.

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The Transformation of a Unilateral Locomotor Command into a Symmetrical Bilateral Activation in the Brainstem

Cited by 66 publications

References 29 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

Bilateral connectivity in the brainstem respiratory networks of lampreys

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