Central respiratory activity of the tadpole in vitro brain stem is modulated diversely by nitric oxide

Harris, Michael B.; Wilson, Richard J. A.; Vasilakos, Konstantinon; Taylor, Barbara; Remmers, John E.

doi:10.1152/ajpregu.00513.2001

Cited by 24 publications

(22 citation statements)

References 65 publications

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“…The recovery in naloxone resulted in significant increases from baseline in these parameters [ Fig. 6(B)], suggesting that opioids may play a role in modulating lung episodes, perhaps in a similar fashion as other identified episode modulators (Hedrick and Morales, 1999;Straus et al, 2000a,b;Harris et al, 2002). However, naloxone has been used to facilitate the generation of locomotor rhythm in spinal cats (Pearson et al, 1992); the enhanced episodic behavior seen in the frog and tadpole brainstems exposed to naloxone may result from a more general mechanism of rhythm excitation.…”

Section: Buccal and Lung Oscillators Are Differentially Sensitive To mentioning

confidence: 89%

“…These putative oscillators are spatially separated, respond differently to GABA A agonists and antagonists (Galante et al, 1996;Broch et al, 2002), GABA B agonists and antagonists (Straus et al, 2000a,b), and nitric oxide (Hedrick and Morales, 1999;Harris et al, 2002), and only the putative lung oscillator is responsive to hypercapnia in the adult . We have proposed that while the putative buccal oscillator acts independently during buccal ventilation (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

et al. 2005

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Though the mechanics of breathing differ fundamentally between amniotes and "lower" vertebrates, homologous rhythm generators may drive air breathing in all lunged vertebrates. In both frogs and rats, two coupled oscillators, one active during the inspiratory (I) phase and the other active during the preinspiratory (PreI) phase, have been hypothesized to generate the respiratory rhythm. We used opioids to uncouple these oscillators. In the intact rat, complete arrest of the external rhythm by opioid-induced suppression of the putative I oscillator, that is, pre-Bötz-inger complex (PBC) oscillator, did not arrest the putative PreI oscillator. In the unanesthetized frog, the comparable PreI oscillator, that is, the putative buccal/ gill oscillator, was refractory to opioids even though the comparable I oscillator, the putative lung oscillator, was arrested. Studies in en bloc brainstem preparations derived from both juvenile frogs and metamorphic tadpoles confirmed these results and suggested that opioids may play a role in the clustering of lung bursts into episodes. As the frog and rat respiratory circuitry produce functionally equivalent motor outputs during lung inflation, these data argue for a close homology between the frog and rat oscillators. We suggest that the respiratory rhythm of all lunged vertebrates is generated by paired coupled oscillators. These may have originated from the gill and lung oscillators of the earliest air breathers.

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Section: Buccal and Lung Oscillators Are Differentially Sensitive To mentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

et al. 2005

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“…First, bullfrog respiratory patterns are modulated by NO and it is proposed that NO provides excitatory input to the respiratory central pattern generators (CPGs) [Hedrick and Morales, 1999;Harris et al, 2002;Hedrick et al, 2005]. The importance of NO to the activity of a variety of CPGs is emerging as a critical role of the transmitter [Scholz et al, 2001;Alford et al, 2003].…”

Section: Motor Systemsmentioning

confidence: 99%

“…Given the importance of NO to the generation of a variety of behaviors [Hedrick and Morales, 1999;Harris et al, 2002;Del Bel et al, 2005;Nelson et al, 2006;Panzica et al, 2006;Sanderson et al, 2006], we investigated the distribution of nitrergic cells in bullfrog brain and spinal cord. In the two comprehensive studies of NOS distribution in the ranid brain, only NADPHd was used as a marker for NOS Lázár and Losonczy, 1999].…”

Section: Introductionmentioning

confidence: 99%

Nitric Oxide Synthase and NADPH Diaphorase Distribution in the Bullfrog <i>(Rana catesbeiana)</i> CNS: Pathways and Functional Implications

Huynh¹,

Boyd²

2007

Brain Behav Evol

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The gas nitric oxide (NO) is emerging as an important regulator of normal physiology and pathophysiology in the central nervous system (CNS). The distribution of cells releasing NO is poorly understood in non-mammalian vertebrates. Nitric oxide synthase immunocytochemistry (NOS ICC) was thus used to identify neuronal cells that contain the enzyme required for NO production in the amphibian brain and spinal cord. NADPH-diaphorase (NADPHd) histochemistry was also used because the presence of NADPHd serves as a reliable indicator of nitrergic cells. Both techniques revealed stained cells in all major structures and pathways in the bullfrog brain. Staining was identified in the olfactory glomeruli, pallium and subpallium of the telencephalon; epithalamus, thalamus, preoptic area, and hypothalamus of the diencephalon; pretectal area, optic tectum, torus semicircularis, and tegmentum of the mesencephalon; all layers of the cerebellum; reticular formation; nucleus of the solitary tract, octaval nuclei, and dorsal column nuclei of the medulla; and dorsal and motor fields of the spinal cord. In general, NADPHd histochemistry provided better staining quality, especially in subpallial regions, although NOS ICC tended to detect more cells in the olfactory bulb, pallium, ventromedial thalamus, and cerebellar Purkinje cell layer. NOS ICC was also more sensitive for motor neurons and consistently labeled them in the vagus nucleus and along the length of the rostral spinal cord. Thus, nitrergic cells were ubiquitously distributed throughout the bullfrog brain and likely serve an essential regulatory function.

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“…Since LC neurons from frogs and rats exhibit similar responses to CO 2 /pH changes (46), a soluble adenylyl cyclasedependent process may elevate cAMP and, in turn, activate I h . Additionally, nitric oxide (NO) signaling has been shown to activate I h (58) and also facilitate respiratory discharge from the bullfrog brain stem (16,18). We speculate that activation of I h by NO signaling within the LC may contribute to portion of the excitatory action of NO in the respiratory network of amphibians.…”

Section: Insights Into the Amphibian Respiratory Control Systemmentioning

confidence: 95%

Activation state of the hyperpolarization-activated current modulates temperature-sensitivity of firing in locus coeruleus neurons from bullfrogs

Santin

Hartzler

2015

American Journal of Physiology-Regulatory, Integrative and Comp

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-Locus coeruleus neurons of anuran amphibians contribute to breathing control and have spontaneous firing frequencies that, paradoxically, increase with cooling. We previously showed that cooling inhibits a depolarizing membrane current, the hyperpolarization-activated current (Ih) in locus coeruleus neurons from bullfrogs, Lithobates catesbeianus (Santin JM, Watters KC, Putnam RW, Hartzler LK. Am J Physiol Regul Integr Comp Physiol 305: R1451-R1464, 2013). This suggests an unlikely role for I h in generating cold activation, but led us to hypothesize that inhibition of I h by cooling functions as a physiological brake to limit the cold-activated response. Using whole cell electrophysiology in brain slices, we employed 2 mM Cs ϩ (an Ih antagonist) to isolate the role of Ih in spontaneous firing and cold activation in neurons recorded with either control or I h agonist (cyclic AMP)-containing artificial intracellular fluid. I h did not contribute to the membrane potential (V m) and spontaneous firing at 20°C. Although voltage-clamp analysis confirmed that cooling inhibits I h, its lack of involvement in setting baseline firing and V m precluded its ability to regulate cold activation as hypothesized. In contrast, neurons dialyzed with cAMP exhibited greater baseline firing frequencies at 20°C due to I h activation. Our hypothesis was supported when the starting level of I h was enhanced by elevating cAMP because cold activation was converted to more ordinary cold inhibition. These findings indicate that situations leading to enhancement of I h facilitate firing at 20°C, yet the hyperpolarization associated with inhibiting a depolarizing cation current by cooling blunts the net V m response to cooling to oppose normal cold-depolarizing factors. This suggests that the influence of I h activation state on neuronal firing varies in the poikilothermic neuronal environment.temperature; Q10; neuronal excitability; hyperpolarization-activated current; respiratory control THE AMERICAN BULLFROG, Lithobates catesbeianus, has a broad geographical distribution within North America and undergoes rapid and variable temperature changes throughout a single day (21, 49). Owing to the temperature sensitivity of neurophysiological mechanisms, changes in temperature pose a challenge to regulating neurally controlled behaviors, like breathing, in the bullfrog and other poikilothermic animals. Despite rate increases of neurally controlled, rhythmic behaviors typically associated with temperature (41), aspects of the respiratory pattern are maintained across temperatures in amphibians and other ectothermic vertebrates. Specifically, breathing frequency has low temperature dependence (Q 10 ϳ 1.7) during changes at higher temperatures (2, 42), and tidal volume (i.e., the volume of air consumed in a breath) is insensitive to variations in temperature (27,51). Consistent with these observations in vivo, respiratory-related cranial nerve activity of the isolated bullfrog brain stem in vitro maintains burst frequency across higher temperatu...

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Central respiratory activity of the tadpole in vitro brain stem is modulated diversely by nitric oxide

Cited by 24 publications

References 65 publications

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

Nitric Oxide Synthase and NADPH Diaphorase Distribution in the Bullfrog <i>(Rana catesbeiana)</i> CNS: Pathways and Functional Implications

Activation state of the hyperpolarization-activated current modulates temperature-sensitivity of firing in locus coeruleus neurons from bullfrogs

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