Bilateral connectivity in the brainstem respiratory networks of lampreys

Gariépy, Jean-François; Missaghi, Kianoush; Chartré, Shannon; Robert, Maxime; Auclair, François; Dubuc, Réjean

doi:10.1002/cne.22804

Cited by 20 publications

(28 citation statements)

References 60 publications

(72 reference statements)

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“…(Mutolo et al, 2007(Mutolo et al, , 2010(Mutolo et al, , 2011Cinelli et al, 2013Cinelli et al, , 2014Bongianni et al, 2016). Consistently with previous results (Garie´py et al, 2012a), small to medium-sized retrogradely labeled neurons were found in the contralateral pTRG (see also Bongianni et al, 2016). Reciprocal connections between the two pTRGs along with the bilateral ascending projections to the pTRG may account for the bilateral effects obtained by unilateral microinjections into the respiratory motoneuron regions (see Cinelli et al, 2014).…”

Section: Discussionsupporting

confidence: 88%

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Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

et al. 2016

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Abstract-Neurons within the vagal motoneuron region of the lamprey have been shown to modulate respiratory activity via ascending excitatory projections to the paratrigeminal respiratory group (pTRG), the proposed respiratory rhythm generator. The present study was performed on in vitro brainstem preparations of the lamprey to provide a characterization of ascending projections within the whole respiratory motoneuron column with regard to the distribution of neurons projecting to the pTRG and related neurochemical markers. Injections of Neurobiotin were performed into the pTRG and the presence of glutamate, GABA and glycine immunoreactivity was investigated by doublelabeling experiments. Interestingly, retrogradely labeled neurons were found not only in the vagal region, but also in the facial and glossopharyngeal motoneuron regions. They were also present within the sensory octavolateral area (OLA). The results show for the first time that neurons projecting to the pTRG are immunoreactive for glutamate, surrounded by GABA-immunoreactive structures and associated with the presence of glycinergic cells. Consistently, GABA A or glycine receptor blockade within the investigated regions increased the respiratory frequency. Furthermore, microinjections of agonists and antagonists of ionotropic glutamate receptors and of the GABA A receptor agonist muscimol showed that OLA neurons do not contribute to respiratory rhythm generation. The results provide evidence that glutamatergic ascending pathways to the pTRG are subject to a potent inhibitory control and suggest that disinhibition is one important mechanism subserving their function. The general characteristics of inhibitory control involved in rhythmic activities, such as respiration, appear to be highly conserved throughout vertebrate evolution.

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Section: Discussionsupporting

confidence: 88%

“…2B-I. Unilateral injections in the pTRG also confirmed the presence of cross-connections between the two pTRGs (Garie´py et al, 2012a) by showing many small to medium-sized labeled neurons in the contralateral pTRG (Fig. 2C).…”

Section: Resultssupporting

confidence: 61%

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

et al. 2016

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“…This region corresponds closely to the pTRG as defined in our previous studies (Mutolo et al, 2007(Mutolo et al, , 2011. Neurons located in the pTRG project to the ipsilateral and contralateral vagal motor nucleus as well as to the contralateral pTRG (Rovainen, 1985;Thompson, 1985;Russell, 1986;Gariépy et al, 2012;Cinelli et al, 2013). The results obtained with microinjections of several neuroactive drugs, such as DAMGO, substance P (SP), acetylcholine (ACh), glutamate or GABA receptor agonists and antagonists, exactly into this region (Mutolo et al, 2007(Mutolo et al, , 2011Cinelli et al, 2013Cinelli et al, , 2014 help to identify and characterize the pTRG and to support the notion that it corresponds to the respiratory CPG (see below).…”

Section: Anatomical and Functional Characterization Of The Ptrgsupporting

confidence: 73%

Neural mechanisms underlying respiratory rhythm generation in the lamprey

Bongianni

Mutolo

Cinelli

et al. 2016

Respiratory Physiology & Neurobiology

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a b s t r a c tThe isolated brainstem of the adult lamprey spontaneously generates respiratory activity. The paratrigeminal respiratory group (pTRG), the proposed respiratory central pattern generator, has been anatomically and functionally characterized. It is sensitive to opioids, neurokinins and acetylcholine. Excitatory amino acids, but not GABA and glycine, play a crucial role in the respiratory rhythmogenesis. These results are corroborated by immunohistochemical data. While only GABA exerts an important modulatory control on the pTRG, both GABA and glycine markedly influence the respiratory frequency via neurons projecting from the vagal motoneuron region to the pTRG. Noticeably, the removal of GABAergic transmission within the pTRG causes the resumption of rhythmic activity during apnea induced by blockade of glutamatergic transmission. The same result is obtained by microinjections of substance P or nicotine into the pTRG during apnea. The results prompted us to present some considerations on the phylogenesis of respiratory pattern generation. They may also encourage comparative studies on the basic mechanisms underlying respiratory rhythmogenesis of vertebrates.

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“…The procedure was similar to that previously used in lampreys (22,57,58) and salamanders (7). Biocytin (Sigma-Aldrich B-4261) and TRDA (Molecular Probes D-3328) were used for retrograde tracing.…”

Section: Methodsmentioning

confidence: 99%

“…Fast green was added to the solution for visualizing the injection site (e.g., refs. 7,22,37,50,58). The number of moles of ejected glutamate was estimated by measuring the volume of a droplet ejected in the air following a single pressure pulse multiplied by the number of pressure pulses (e.g., refs.…”

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.

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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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Bilateral connectivity in the brainstem respiratory networks of lampreys

Cited by 20 publications

References 60 publications

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

Neural mechanisms underlying respiratory rhythm generation in the lamprey

A descending dopamine pathway conserved from basal vertebrates to mammals

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