Neurochemical characterization of sea lamprey taste buds and afferent gustatory fibers: Presence of serotonin, calretinin, and CGRP immunoreactivity in taste bud bi‐ciliated cells of the earliest vertebrates

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

doi:10.1002/cne.21844

Cited by 38 publications

(56 citation statements)

References 89 publications

(129 reference statements)

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“…The AB144P antibody has been used on lampreys for many years by different research teams, and its selectivity against ChAT is well demonstrated (7,31,32). The AB152 antibody against TH has been used reliably on lampreys in many independent studies on DA neurons (24,33,34). The specificity of the MAB5300 antibody for DA was tested by ELISA by the manufacturer, and its pattern of labeling in our material corresponded closely to that reported with other DA antibodies in the lamprey (29,30).…”

Section: Methodssupporting

confidence: 74%

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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Section: Methodssupporting

confidence: 74%

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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“…It has been widely used in lampreys, salamanders, rats, and human to label DA neurons (manufacturer's information) (22,28,(69)(70)(71)(72)(73). The 22941 TH antibody was used here on human tissue based on its successful use by Parent et al (74).…”

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

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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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“…If the taste buds of lampreys lack facial nerve innervation, this would indicate that this is an evolutionary novelty of gnathostome vertebrates. However, it is now known that in lampreys the rostral part of the first gill, which bears taste buds [Barreiro-Iglesias et al, 2008c], is innervated by the facial nerve [Guimond et al, 2003]. Therefore, the possible facial nerve innervation of the taste buds located on the first gill of lampreys should be determined by use of modern tract-tracing techniques.…”

Section: General Organizationmentioning

confidence: 99%

“…Since the first studies by Baatrup in the 1980s on the ultrastructure and physiology of the taste buds of lampreys [Baatrup, 1983a[Baatrup, , b, 1985a, the gustatory system of lampreys has not received much attention. However, recent neurochemical data on the taste buds of sea lampreys have revealed some interesting new aspects of the early evolution of taste buds in vertebrates [Barreiro-Iglesias et al, 2008c]. In the present review, we aim to summarize the current knowledge of the organization and physiology of the gustatory system of lampreys.…”

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confidence: 99%