Evidence for rhombomeric organization of multiple respiratory oscillators in the bullfrog brainstem

Klingler, Michael; Hedrick, Michael S.

doi:10.1016/j.resp.2012.12.007

Cited by 9 publications

(9 citation statements)

References 22 publications

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“…) argues that the powerstroke generator also has some endogenous capacity for rhythm generation. In addition, a recent brainstem transection study in frogs suggests more than two regions of the brainstem possess weak endogenous rhythmogenic capability when physically isolated (Klingler and Hedrick, ). Thus, based on current data, we hypothesize three rhythmogenic components regulating movement of air in and out of the buccal cavity and controlling lung ventilation: the buccal oscillator, and the lung priming and lung powerstroke oscillators.…”

Section: Discussionmentioning

confidence: 99%

“…; Wilson et al . ; Gargaglioni and Milsom, ; Kinkead, ; Klingler and Hedrick, ; Ranohavimparany et al . ).…”

Section: Introductionunclassified

“…According to this architecture, rhythm and phase cannot easily be partitioned to a discrete anatomical location. Despite the potential for yielding insight into the architecture of rhythmogenic circuits of higher organisms, respiratory rhythmogenesis in non-mammalian amniotes has been less well studied, with knowledge mainly restricted to embryonic stages (Fortin et al 2003;Johnson et al 2007;Klingler and Hedrick, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Most studies in non-mammalian amniotes have focused on frogs (Hedrick, 2005;Vasilakos et al 2006;Wilson et al 2006;Gargaglioni and Milsom, 2007;Kinkead, 2009;Klingler and Hedrick, 2013;Ranohavimparany et al 2014). Frogs exhibit tidal buccal ventilation, involving continuous movement of the buccal cavity (Vasilakos et al 2005) and lung ventilation, phase-locked to buccal ventilation and often occurring in episodes Milsom et al 1999).…”

Section: Introductionmentioning

confidence: 99%

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Three brainstem areas involved in respiratory rhythm generation in bullfrogs

Baghdadwala

Duchcherer

Paramonov

et al. 2015

The Journal of Physiology

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Key pointsr For most multiphasic motor patterns, rhythm and pattern are produced by the same circuit elements. For respiration, however, these functions have long been assumed to occur separately.r In frogs, the ventilatory motor pattern produced by the isolated brainstem consists of buccal and biphasic lung bursts. Previously, two discrete necessary and sufficient sites for lung and buccal bursts were identified.r Here we identify a third site, the Priming Area, important for and having neuronal activity correlated with the first phase of biphasic lung bursts.r As each site is important for burst generation of a separate phase, we suggest each major phase of ventilation is produced by an anatomically distinct part of an extensive brainstem network.r Embedding of discrete circuit elements producing major phases of respiration within an extensive rhythmogenic brainstem network may be a shared architectural characteristic of vertebrates.Abstract Ventilation in mammals consists of at least three distinct phases: inspiration, post-inspiration and late-expiration. While distinct brainstem rhythm generating and pattern forming networks have long been assumed, recent data suggest the mammalian brainstem contains two coupled neuronal oscillators: one for inspiration and the other for active expiration. However, whether additional burst generating ability is required for generating other phases of ventilation in mammals is controversial. To investigate brainstem circuit architectures capable of producing multiphasic ventilatory rhythms, we utilized the isolated frog brainstem. This preparation produces two types of ventilatory motor patterns, buccal and lung bursts. Lung bursts can be divided into two phases, priming and powerstroke. Previously we identified two putative oscillators, the Buccal and Lung Areas. The Lung Area produces the lung powerstroke and the Buccal Area produces buccal bursts and -we assumed -the priming phase of lung bursts. However, here we identify an additional brainstem region that generates the priming phase. This Priming Area extends rostral and caudal of the Lung Area and is distinct from the Buccal Area. Using AMPA microinjections and reversible synaptic blockade, we demonstrate selective excitation and ablation (respectively) of priming phase activity. We also demonstrate that the Priming Area contains neurons active selectively during the priming phase. Thus, we propose that three distinct neuronal components generate the multiphase respiratory motor pattern produced by the frog brainstem: the buccal, priming and powerstroke burst generators. This raises the possibility that a similar multi-burst generator architecture mediates the three distinct phases of ventilation in mammals.M.I. Baghdadwala and M. Duchcherer contributed equally to this work.

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Section: Discussionmentioning

confidence: 99%

“…; Wilson et al . ; Gargaglioni and Milsom, ; Kinkead, ; Klingler and Hedrick, ; Ranohavimparany et al . ).…”

Section: Introductionunclassified

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Three brainstem areas involved in respiratory rhythm generation in bullfrogs

Baghdadwala

Duchcherer

Paramonov

et al. 2015

The Journal of Physiology

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“…If the lung area acts as an endogenous oscillator, it should continue to burst when isolated from other parts of the brainstem. Arguing against the role of the lung area as an endogenous oscillator, transection experiments that isolated this region in a thick slice along with the vagus nerve rootlet do not show respiratory-related motor output in post-metamorphic frogs; specifically, only 2 out of 11 preparations produced any motor activity ( Klingler and Hedrick, 2013 ). In addition, raising the extracellular K + concentration, as commonly done in mammalian preparations, does not reliably initiate the rhythm in a thick slice, with only 3 out of 10 preparations having activity ( Klingler and Hedrick, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Activation of respiratory-related bursting in an isolated medullary section from adult bullfrogs

Saunders,

Santin

2023

Journal of Experimental Biology

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Breathing is generated by a rhythmic neural circuit in the brainstem, which contains conserved elements across vertebrate groups. In adult frogs, the ‘lung area’ located in the reticularis parvocellularis is thought to represent the core rhythm generator for breathing. Although this region is necessary for breathing-related motor output, whether it functions as an endogenous oscillator when isolated from other brainstem centers is not clear. Therefore, we generated thick brainstem sections that encompass the lung area to determine whether it can generate breathing-related motor output in a highly reduced preparation. Brainstem sections did not produce activity. However, subsaturating block of glycine receptors reliably led to the emergence of rhythmic motor output that was further enhanced by blockade of GABAA receptors. Output occurred in singlets and multi-burst episodes resembling the intact network. However, burst frequency was slower and individual bursts had longer durations than those produced by the intact preparation. In addition, burst frequency was reduced by noradrenaline and μ-opioids, and increased by serotonin, as observed in the intact network and in vivo. These results suggest that the lung area can be activated to produce rhythmic respiratory-related motor output in a reduced brainstem section and provide new insights into respiratory rhythm generation in adult amphibians. First, clustering breaths into episodes can occur within the rhythm-generating network without long-range input from structures such as the pons. Second, local inhibition near, or within, the rhythmogenic center may need to be overridden to express the respiratory rhythm.

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