Anatomical and physiological study of respiratory motor innervation in lampreys

Guimond, Jean-Charles; Auclair, François; Lund, James P.; Dubuc, Réjean

doi:10.1016/s0306-4522(03)00601-8

Cited by 28 publications

(26 citation statements)

References 17 publications

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“…All labeled neurons have similar morphological characteristics. They are arranged in an almost continuous column and can be distinguished from branchial motoneurons by large differences in size and morphology (see also Rovainen, 1974;Guimond et al, 2003;Bongianni et al, 2016). We are confident that Neurobiotin injections were performed into the pTRG in agreement with the anatomical landmarks previously described, i.e.…”

Section: Discussionmentioning

confidence: 60%

“…Nieuwenhuys, 1972;Villar-Cervin˜o et al, 2008). Respiratory motoneurons are located in the facial, glossopharyngeal and, especially, in the vagal nuclei (Rovainen, 1974(Rovainen, , 1977(Rovainen, , 1979Guimond et al, 2003), while the putative central neural mechanisms generating the respiratory rhythmic activity are located in the paratrigeminal respiratory group (pTRG), rostral to the trigeminal motor nucleus (Mutolo et al, 2007(Mutolo et al, , 2010(Mutolo et al, , 2011Cinelli et al, 2013Cinelli et al, , 2014Bongianni et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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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: Discussionmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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“…The isolated brainstem of the adult lamprey spontaneously generates respiratory neuronal activity in vitro (fictive respiration); this activity closely resembles that underlying the respiratory behavior of intact animals (Rovainen, 1977(Rovainen, , 1983Thompson, 1985;Russell, 1986;Bongianni et al, 1999Bongianni et al, , 2002Bongianni et al, , 2006Mutolo et al, 2007Mutolo et al, , 2010. The vast majority of respiratory motoneurons are located in the facial, glossopharyngeal, and especially vagal nuclei (Rovainen, 1974(Rovainen, , 1977(Rovainen, , 1979Guimond et al, 2003), while respiration-related neurons possibly responsible for respiratory rhythm generation have been encountered within the pTRG (Mutolo et al, 2007(Mutolo et al, , 2010. Recordings and microinjections within the pTRG as well as neighboring sites were performed under microscope control (Stemi 2000;Zeiss).…”

Section: Methodsmentioning

confidence: 99%

Identification of a Cholinergic Modulatory and Rhythmogenic Mechanism within the Lamprey Respiratory Network

Mutolo¹,

Cinelli²,

Bongianni³

et al. 2011

J. Neurosci.

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Acetylcholine (ACh) is well known to be involved in the control of breathing. However, no information is available on the role of ACh receptors (AChRs) within the lamprey respiratory network. The present study was performed on in vitro brainstem preparations of adult lampreys to investigate whether ACh affects respiratory activity possibly through an action on the paratrigeminal respiratory group (pTRG) that has been identified as an essential component of the respiratory network. Respiratory activity was monitored as vagal motor output. Bath application of 100 M physostigmine or 1 M nicotine increased respiratory frequency, while bath application of 100 M D-tubocurarine or 0.25 M ␣-bungarotoxin reduced respiratory frequency and increased the duration of vagal bursts. Since these effects were mimicked by microinjections of the same drugs into the pTRG, ACh proved to influence respiratory activity by acting on ␣7 nicotinic AChRs located within the pTRG. During apnea caused by partial blockade of ionotropic glutamate receptors at the level of the pTRG, bath application of bicuculline and strychnine restored the respiratory rhythm, although at reduced frequency. Similar results were obtained by the concurrent removal of both fast synaptic excitatory and inhibitory transmission. Blockade of pTRG ␣7 nicotinic AChRs suppressed this respiratory activity, thus indicating that pTRG neurons expressing these receptors contribute to respiratory rhythm generation. Together, these findings identify a novel cholinergic modulatory and possibly subsidiary rhythmogenic mechanism within the respiratory network of the adult lamprey and encourage further studies on the respiratory role of cholinergic receptors in different animal species.

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“…B and C adapted from Mutolo et al (2007) and Cinelli et al (2014), respectively. possibly, to obtain new hints for further investigations on the basic neural mechanisms operating in the respiratory network of higher vertebrates, including mammals. The vast majority of respiratory motoneurons are located in the facial, glossopharyngeal and, especially, vagal nuclei, while the neural aggregate responsible for respiratory rhythm generation appears to be located in a region rostrolateral to the trigeminal motor nucleus (Rovainen, 1977(Rovainen, , 1979(Rovainen, , 1983(Rovainen, , 1985Thompson, 1985;Russell, 1986;Bongianni et al, 1999Bongianni et al, , 2002Bongianni et al, , 2006Guimond et al, 2003;Martel et al, 2007;Mutolo et al, 2007). Mutolo et al (2007) reported that opioids have a modulatory role in the respiratory network and, in particular, that microinjections of the -opioid receptor agonist DAMGO at sites rostrolateral to the trigeminal motor nucleus abolish the respiratory rhythm.…”

Section: General Features Of the Lamprey Respiratory Systemmentioning

confidence: 99%

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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Anatomical and physiological study of respiratory motor innervation in lampreys

Cited by 28 publications

References 17 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

Identification of a Cholinergic Modulatory and Rhythmogenic Mechanism within the Lamprey Respiratory Network

Neural mechanisms underlying respiratory rhythm generation in the lamprey

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