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

Mutolo, Donatella; Cinelli, Elenia; Bongianni, Fulvia; Pantaleo, Tito

doi:10.1523/jneurosci.2764-11.2011

Cited by 25 publications

(65 citation statements)

References 49 publications

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“…they were localized in a dorsal aspect of the anterior rhombencephalic reticular nucleus (ARRN), at the level of the I 1 and close to the SL. (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).…”

Section: Discussionsupporting

confidence: 90%

“…The brain was exposed dorsally and a transection was made caudal to the obex. The roof of the isthmic region was cut along the midline and the alar plates were spread laterally and pinned down (see Mutolo et al, 2007Mutolo et al, , 2010Mutolo et al, , 2011Cinelli et al, 2013Cinelli et al, , 2014.…”

Section: Anatomical Experimentsmentioning

confidence: 99%

“…Animal preparation and experimental procedures have been already fully described (Bongianni et al, 1999(Bongianni et al, , 2002(Bongianni et al, , 2006Mutolo et al, 2007Mutolo et al, , 2010Mutolo et al, , 2011Cinelli et al, 2013Cinelli et al, , 2014. Of note, the preparation was similar to that employed in the anatomical experiments, except that the brain tissue rostral to the optic tectum was cut and removed.…”

Section: Electrophysiological Experimentsmentioning

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%

“…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: Discussionsupporting

confidence: 90%

Section: Anatomical Experimentsmentioning

confidence: 99%

Section: Electrophysiological Experimentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

et al. 2016

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Cholinergic projections to the preBötzinger complex

Biancardi,

Yang,

Ding

et al. 2023

J of Comparative Neurology

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Rhythmic inspiratory activity is generated in the preBötzinger complex (preBötC), a neuronal network located bilaterally in the ventrolateral medulla. Cholinergic neurotransmission affects respiratory rhythmogenic neurons and inhibitory glycinergic neurons in the preBötC. Acetylcholine has been extensively investigated given that cholinergic fibers and receptors are present and functional in the preBötC, are important in sleep/wake cycling, and modulate inspiratory frequency through its action on preBötC neurons. Despite its role in modulating inspiratory rhythm, the source of acetylcholine input to the preBötC is not known. In the present study, we used retrograde and anterograde viral tracing approaches in transgenic mice expressing Cre‐recombinase driven by the choline acetyltransferase promoter to identify the source of cholinergic inputs to the preBötC. Surprisingly, we observed very few, if any, cholinergic projections originating from the laterodorsal and pedunculopontine tegmental nuclei (LDT/PPT), two main cholinergic, state‐dependent systems long hypothesized as the main source of cholinergic inputs to the preBötC. On the contrary, we identified glutamatergic and GABAergic/glycinergic neurons in the PPT/LDT that send projections to the preBötC. Although these neurons contribute minimally to the direct cholinergic modulation of preBötC neurons, they could be involved in state‐dependent regulation of breathing. Our data also suggest that the source of cholinergic inputs to the preBötC appears to originate from cholinergic neurons in neighboring regions of the medulla, the intermediate reticular formation, the lateral paragigantocellularis, and the nucleus of the solitary tract.

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