Respiratory rhythms generated in the lamprey rhombencephalon

Martel, B.; Guimond, Jean-Charles; Gariépy, Jean François; Gravel, Jocelyn; Auclair, François; Kolta, Arlette; Lund, James P.; Dubuc, Réjean

doi:10.1016/j.neuroscience.2007.05.023

Cited by 35 publications

(67 citation statements)

References 48 publications

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“…The suppression of respiratory activity caused by bath application of ionotropic glutamate receptor antagonists (Bongianni et al, 1999;Mutolo et al, 2011) is mimicked by microinjections of these drugs into the pTRG (Martel et al, 2007;Cinelli et al, 2013Cinelli et al, , 2014, thus supporting the hypothesis that this region is crucial for respiratory rhythm generation. Examples of the apnea caused by ionotropic glutamate receptor blockade are reported in Fig.…”

Section: Glutamatergic Mechanisms In the Respiratory Rhythmogenesismentioning

confidence: 55%

“…Of note, bicuculline applied to the vagal motoneuron region during apnea caused by ionotropic glutamate receptor blockade does not restore the respiratory rhythm, thus suggesting that this region does not possess the rhythmogenic properties hypothesized by previous studies (see e.g. Kawasaki, 1979Kawasaki, , 1984Thompson, 1985Thompson, , 1990Martel et al, 2007). However, the functional role of GABAergic and glycinergic inputs to neurons located in the vagal motoneuron region remains unclear.…”

Section: Gabaergic and Glycinergic Mechanisms In The Respiratory Networkmentioning

confidence: 81%

“…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%

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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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Section: Glutamatergic Mechanisms In the Respiratory Rhythmogenesismentioning

confidence: 55%

Section: Gabaergic and Glycinergic Mechanisms In The Respiratory Networkmentioning

confidence: 81%

Section: General Features Of the Lamprey Respiratory Systemmentioning

confidence: 99%

See 1 more Smart Citation

Neural mechanisms underlying respiratory rhythm generation in the lamprey

Bongianni

Mutolo

Cinelli

et al. 2016

Respiratory Physiology & Neurobiology

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“…Endogenously released excitatory amino acids, but not GABA and glycine, have been shown to have an essential role in the respiratory rhythmogenesis (Rovainen, 1983;Martel et al, 2007;Bongianni et al, 1999Bongianni et al, , 2006Bongianni et al, , 2016Cinelli et al, 2013Cinelli et al, , 2014. Only GABAergic influences have a modulatory role at the pTRG level.…”

Section: Introductionmentioning

confidence: 99%

“…The isolated brainstem of the adult lamprey, a lower vertebrate that diverged from the main vertebrate line $560 million years ago (Kumar and Hedges, 1998), spontaneously generates a stable and regular respiratory neuronal activity in vitro (fictive respiration) for at least 12 h; this activity is very similar to that underlying respiration in intact animals (Rovainen, 1977(Rovainen, , 1983Thompson, 1985;Russell, 1986;Bongianni et al, 1999Bongianni et al, , 2002Bongianni et al, , 2006Mutolo et al, 2007Mutolo et al, , 2010Mutolo et al, , 2011Martel et al, 2007;Cinelli et al, 2013Cinelli et al, , 2014. The lateral walls of its central nervous system consist of two longitudinal zones or plates: the ventral primarily motor basal plate and the dorsal primarily sensory alar plate that comprises the octavolateral area (OLA; see e.g.…”

Section: Introductionmentioning

confidence: 99%

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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